Interspecific competition, hybridization, and reproductive isolation in secondary contact: missing perspectives on males and females

Interspecific competition, hybridization, and reproductive isolation in secondary contact:... Research on sexual selection and hybridization has focused on female mate choice and male–male competition. While the evolutionary outcomes of interspecific female preference have been well explored, we are now gaining a better understanding of the processes by which male–male compe- tition between species in secondary contact promotes reproductive isolation versus hybridization. What is relatively unexplored is the interaction between female choice and male competition, as they can oppose one another or align with similar outcomes for reproductive isolation. The role of female–female competition in hybridization is also not well understood, but could operate similarly to male–male competition in polyandrous and other systems where costs to heterospecific mating are low for females. Reproductive competition between either sex of sympatric species can cause the divergence and/or convergence of sexual signals and recognition, which in turn influences the likelihood for interspecific mating. Future work on species interactions in secondary contact should test the relative influences of both mate choice and competition for mates on hybridization out- comes, and should not ignore the possibilities that females can compete over mating resources, and males can exercise mate choice. Key words: female–female competition, hybridization, male–male competition, reproductive isolation, sexual selection. Introduction species because of their greater investment in gametes and fewer Traditional perspectives on sexual selection and opportunities for multiple mating relative to males (Bateman 1948; hybridization Andersson 1994). In contrast, males are expected to maximize fit- Sexual signals and mating behaviors influence whether sympatric ness by mating as frequently as possible (Darwin 1871; Bateman species interbreed, and can therefore promote or impede behavioral 1948; Andersson 1994). The traditional perspective of sexual selec- reproductive isolation (Irwin and Price 1999; see Box 1: tion underlays the predictions for evolutionary outcomes in different Definitions). Interspecific hybridization is common and is estimated scenarios of secondary contact. For instance when hybridization is to occur in 10% of animals (Mallet 2005). Traditionally, research maladaptive, lineages in secondary contact are expected to evolve on the role of sexual selection in hybridization has focused on the divergence in sexually selected traits and in species recognition of importance of mate choice and species discrimination from the per- mates to avoid heterospecific mating, a process known as reinforce- spective of choosy females, and competition from the lens of aggres- ment (Coyne and Orr 1989; Servedio and Noor 2003). The predic- sive and indiscriminate males (Moore 1987; Grant and Grant 1997; tions for reinforcement have been developed from the perspective of Sætre et al. 1997; Parker and Partridge 1998; Wirtz 1999; Randler females, who face higher fitness costs of heterospecific mating mis- 2002). This conventional view considers females the gatekeepers of takes and are therefore predicted to discriminate more strongly V C The Author (2017). Published by Oxford University Press. 75 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 76 Current Zoology, 2018, Vol. 64, No. 1 this can result in high reproductive costs for females, termed the so- Box 1. Definitions called “satyr effect” (Ribeiro and Spielman 1986). Interspecific male–male competition is not widely considered to promote repro- ductive isolation except as it relates to female choice (but see 1B, Agonistic character displacement: divergence in competitive Competitive asymmetry and reproductive exclusion). signals or traits in sympatry to reduce costly interspecific Rapid divergence in sexually selected traits between closely interactions. related lineages in allopatry can promote reproductive isolation Asymmetric introgression: the unidirectional exchange of through the maintenance of species-specific signals and recognition alleles from 1 species to another. when these lineages come into secondary contact (Coyne and Orr Behavioral reproductive isolation: reduced gene flow due to 2004; Hudson and Price 2014; Weber and Strauss 2016; Cooney divergent mating signals and preferences. et al. 2017). Character shifts in sexual traits can also result from spe- Competitive asymmetry: the superior competitive ability and/ cies interactions in secondary contact. These processes have been or dominance of 1 species over another. widely explored in terms of interspecific male–female interactions Heterosis: hybrid vigor, when hybrids are competitively supe- concerning reinforcement of male traits and female recognition of rior to their parental species. those traits (see 1A, Character displacement: ecological, reproduc- Introgressive hybridization: interbreeding between 2 distinct tive, and agonistic). However, interspecific male–male interactions lineages that results in gene flow. can also impact the evolution of sexual traits, which in turn can Hybrid swarm: hybridization that erodes parental species influence hybridization outcomes. For instance, when lineages that boundaries. compete over similar ecological and/or mating resources come into Interspecific intrasexual conflict: antagonistic coevolution contact, their competitive interactions can cause selection on traits between males and females of interacting species. that influence fighting ability and competitor recognition, which can Reproductive character displacement: divergence in mating subsequently influence the evolution of reproductive isolation signals or traits in sympatry to reduce costly interspecific and/or facilitate hybridization. This process, known as agonistic mating. character displacement (ACD), can result in either divergence or Interspecific reproductive competition: competition for mates convergence of phenotypic traits involved in competitor recognition and/or mating resources between species. and fighting ability, depending on the intensity of resource competi- Reproductive exclusion: sexual interactions between species tion between species (Grether et al. 2009). Divergence in competitor that cause one to become locally extinct. signals and recognition is expected to promote reproductive isola- Secondary contact: Geographic overlap between 2 genetically tion (see Figure 1, conceptual framework). However, even species distinct lineages that derived from a common ancestor and with diverged competitive traits may hybridize if males of the domi- underwent a phase of allopatric isolation. Social selection: a form of selection resulting from all social nant species (e.g., the lineage that is superior in aggression, body interactions in order to gain access to resources, including size, and/or competitive ability) monopolize mating resources shared but not limited to mates. with males of the subordinate species. Convergence in competitive signals is expected to facilitate territorial interactions over shared, limited resources, but can also increase the likelihood of hybridiza- tion if those signals also play a role in mate recognition. Alternatively, convergence that results in the exclusion of 1 species against heterospecifics than males (Sætre et al. 1997; Parker and could promote reproductive isolation. In addition to male trait evo- Partridge 1998; Wirtz 1999; Servedio et al. 2009; Hudson and Price lution, female mate preferences may diverge or utilize a different 2014). An open question is to what extent does male–male competi- sexual trait to avoid hybridization (Hankison and Morris 2003; tion between lineages influence hybridization outcomes in secondary Seddon and Tobias 2010; Hudson and Price 2014). contact, and when is female mate choice predicted to support or oppose these outcomes? Updating perspectives on sexual selection and Recent empirical and theoretical work has brought increasing hybridization attention to the function of male–male competition in speciation Studies on mating behavior and hybridization often draw a dichot- (Doorn et al. 2004; Seehausen and Schluter 2004; Dijkstra et al. omy between competitive males mating indiscriminately and choosy 2007; Qvarnstro ¨ m et al. 2012; Drury et al. 2016). Reproductive females limiting heterospecific mating. This dichotomy is oversim- competition, also known as intrasexual selection, is a component of plified in several ways. For instance, male mate choice can facilitate sexual selection that involves fighting over mating resources such as mate discrimination within and between Timema stick insects territories and mates. Competition is an important determinant of (Arbuthnott and Crespi 2009), thereby reducing interspecific gene mating success for many taxa, especially those with polygynous or flow. Additionally, females can prefer heterospecifics when they polyandrous mating systems where reproductive success is highly resemble high-quality conspecifics and/or ancestral preferences have skewed toward dominant individuals (Emlen and Oring 1977; not diverged, as in female orange-backed fairy wrens Malurus mela- Clutton-Brock 2007). Interspecific competition is common (Peiman nocephalus melanocephalus that prefer red-backed males resembling and Robinson 2010), and interspecific reproductive competition can another subspecies M. m. cruentatus (Baldassarre and Webster occur when species compete for shared territorial and/or signaling 2013) and in female tungara frogs (Physalaemus pustulosus species space involved in mate attraction and reproduction (Grether et al. group) that prefer call features of heterospecific males (Ryan and 2009; Burdfield-Steel and Shuker 2011; Pfennig and Pfennig 2012). Rand 1993). In this review, I propose that we have overlooked an Low fitness costs to heterospecific mating for males can facilitate additional component of sexual selection that could influence introgressive hybridization when males compete over heterospecific hybridization and reproductive isolation in secondary contact: mates via male–male competition (Arnqvist and Rowe 2005), but female–female competition. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Lipshutz  Female competition and speciation 77 Figure 1. Conceptual framework of how competition between species in secondary contact can promote reproductive isolation and/or hybridization. Path labels (e.g., 1A) correspond to sections throughout the manuscript. Despite a growing understanding of male–male competition and isolation and 2) competition facilitates introgression—the exchange speciation, empirical and theoretical studies on the roles of female– of alleles from one species to another. I also emphasize that the out- female competition as well as male mate choice in hybridization are comes of interspecific interactions in secondary contact should be lacking (but see Wong et al. 2005; Servedio 2007; Kozak et al. considered in the context of both competition and mate choice, as 2009; Roberts and Mendelson 2017). There are many studies dem- well as from the perspectives of both the signaler and the receiver, onstrating that females compete over mating resources (reviewed in and I review what may be the first case of female–female competi- tion promoting hybridization (Figure 2). Rosvall 2011; Cain and Ketterson 2012) and males can be choosy of mates (reviewed in Kraaijeveld et al. 2007; Edward and Chapman 2011). Empirical studies across a wide variety of taxa including fish, When Competition in Secondary Contact lizards, and birds suggest that female aggression is adaptive in a Promotes Reproductive Isolation number of social contexts (Stockley and Campbell 2013) including Sexual selection can be a diversifying force in driving the evolution territory defense (Woodley and Moore 1999; Desjardins et al. 2006; of traits involved in mate choice and competition for mates both Gill et al. 2007; Reedy et al. 2017) and reproductive success (While within and between species (Lande 1981; Panhuis et al. 2001; et al. 2009). Likewise, adaptive mate choice has been demonstrated Coyne and Orr 2004; Ritchie 2007). Closely related lineages are for males in several insect species that face high reproductive costs often more divergent in secondary sexual characteristics than other such as sperm limitation and choose among females that vary in phenotypic traits (West-Eberhard 1983; Allender et al. 2003). quality of signals advertising fecundity (Bonduriansky 2001; Nandy Sexual characteristics specifically involved in competition include et al. 2012). As little attention as female competition and aggression those directly used in fighting, such as body size and weaponry, as have received in the literature, the role of female–female competition well as traits important in signaling dominance, such as coloration in hybridization has received far less. As a first step to addressing and vocalizations (Andersson 1994). Along with divergence in ago- this gap, we need to compare the evolution of competitive traits and nistic signals, the visual and auditory sensory systems that receive recognition in females to those of males, and predict the potential and recognize these signals may also diverge between heterospecific outcomes for hybridization in secondary contact. Future work competitors (Peiman and Robinson 2010; Pfennig and Pfennig should also focus on the role of male mate choice in speciation, but 2012; Okamoto and Grether 2013). Because these sexual traits are the current review will focus on comparing interspecific male–male often used both to attract mates as well as to compete for mating and female–female competition. resources (Berglund et al. 1996), their divergence between species Here, I examine the role that interspecific reproductive competi- can have consequences for reproductive isolation. For instance, tion plays in hybridization, specifically between closely related line- character divergence that reduces interspecific interactions will limit ages (species, subspecies, and divergent populations) in secondary gene flow between species. Below I describe patterns of divergence contact when reproductive isolation is incomplete. Other reviews in competitive traits and recognition resulting from interspecific have focused on the diversifying role of male–male competition in interactions, and explore how this divergence can promote repro- promoting speciation (e.g., Qvarnstro ¨ m et al. 2012), but here I ductive isolation via reproductive exclusion and sexual conflict. expand this perspective to improve our understanding of both male– male and female–female competition and their evolutionary out- Character displacement: ecological, reproductive, and comes in secondary contact, which can either facilitate or impede reproductive isolation (see Figure 1, conceptual framework). agonistic I review the empirical and theoretical evidence supporting evolution- Character shifts in competitive traits and competitor recognition ary scenarios in which 1) competition promotes reproductive could take place due to different sexual, social, and ecological Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 78 Current Zoology, 2018, Vol. 64, No. 1 Figure 2. Females of 2 polyandrous, sex-role reversed shorebird species that hybridize in Panama show competitive asymmetries in morphology (left panel) and aggressive behavior (middle panel). J. spinosa females (right panel top) have larger body mass, longer wing spurs used for fighting, and are more aggressive than J. jacana females (right panel bottom), which may explain the asymmetric introgression of mtDNA in the hybrid zone. Figure adapted from Lipshutz (2017). Illustrations by Stephanie McClelland. selection pressures on each lineage evolving independently in allopa- and Pfennig 2010) which could initiate the speciation process (Schluter 2001; Pfennig and Pfennig 2009). tric isolation (Rice and Pfennig 2007), or to selection pressures For closely related species in secondary contact that have not occurring from contact with a heterospecific in sympatry (Grether diverged in their secondary sexual characteristics, similar mating sig- et al. 2009; Pfennig and Pfennig 2009). Three main processes of trait nals can result in species recognition errors and heterospecific mat- shifts due to interspecific interactions are ecological character dis- ing (Gro ¨ ning and Hochkirch 2008), which can in turn lead to the placement (ECD), reproductive character displacement (RCD), and evolution of RCD. RCD is a process that selects for greater sexual ACD, and they can result in either divergence or convergence in trait divergence and/or species discrimination in sympatry compared sympatry (Grant 1972). Competitive ecological interactions in sec- with allopatry, and can be indicative of the reinforcement process. ondary contact have been widely explored (reviewed in Pfennig and Much empirical and theoretical research has investigated how selec- Pfennig 2012; Weber and Strauss 2016). ECD is a process that pro- tion resulting from mate misrecognition and maladaptive hybridiza- duces greater shifts in ecological niches of species in sympatry than tion can drive divergence in mating signals and/or preferences in allopatry. ECD can arise when disruptive selection causes coexist- (Ptacek 2000; Coyne and Orr 2004; Pfennig and Pfennig 2009). ing species to diverge in their ecological niches, thereby reducing Like ECD, RCD can minimize interspecific contact, including repro- interspecific competition over a previously shared ecological ductive competition, if the traits that diverge also function in com- resource such as food (Brown and Wilson 1956; Losos et al. 2000; petitive interactions. Both ECD and RCD can influence each other, Schluter 2001). Both the resource utilized and trait associated with when species that compete for ecological resources also have similar the resource use are expected to change between the sympatric spe- sexual signals (reviewed in Pfennig and Pfennig 2009). Species dis- cies (e.g., prey type and jaw morphology in larval feeding of crimination between divergent signals can be tested using playback spadefoot toads Spea bombifrons and Spea multiplicata; Pfennig experiments, but their implementation and interpretations can be and Murphy 2003). Divergent ECD is predicted to promote repro- challenging for both male and female behavior (see Box 2). ductive isolation in several ways. The divergence in resource acquisi- Similarity in agonistic signals and competitor recognition can tion traits may reduce contact between species, and therefore also select for divergence or convergence between species in secon- impede interspecific gene flow (reviewed in Coyne and Orr 2004; dary contact, a process known as ACD. ACD evolves to reduce mal- Price 2008). Additionally, ecological divergence between sympatric adaptive interspecific competition over mating resources (Grether species can drive divergence in sexual signals, which can lead to et al. 2009), and can change the degree and/or outcome of interspe- reproductive isolation. In Darwin’s finches, for example, ecologi- cific interactions (Cody 1969; Grether et al. 2013). ACD has cally adaptive divergence in beak morphology is correlated with received relatively less attention than ECD and RCD, and fewer divergence in song, which is used in territorial defense and mate empirical cases are known. In the rubyspot damselfly genus choice (Huber and Podos 2006; Podos 2010). In the medium ground Hetaerina, males of some species use wing coloration for competitor finch Geospiza fortis, large and small beak morphs demonstrate recognition, and similarity in male wing coloration causes misidenti- positive assortative pairing, and gene flow is reduced between fication between species (Anderson and Grether 2010a). morphs (Huber et al. 2007). If offspring produced by matings Observational and experimental studies revealed that interspecific between these populations are intermediate in phenotype and there- territorial aggression in sympatry selected for shifts in agonistic sig- fore are competitively inferior in either niche, ecologically depend- nals (Anderson and Grether 2010a) and competitor recognition ent postmating isolation can evolve (Pfennig and Rice 2007; Rice (Anderson and Grether 2010b). Similar patterns have been found in Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Lipshutz  Female competition and speciation 79 Box 2. Interpretation of playback experiments To experimentally measure the extent of premating reproductive isolation between 2 species, studies compare mating signal divergence along with relative responses, that is, discrimination, between conspecific and heterospecific signals. For paired design playback studies in which males discriminate between conspecific and het- erospecific stimuli, this is interpreted as evidence for reproductive isolation because divergent mating signals would reduce heterospecific gene flow (Baker 2001; Slabbekoorn and Smith 2002; Podos 2010; Lipshutz et al. 2017). Males whose territorial signals are not recognized by neighboring heterospecifics will face difficulty establishing and defending their territories in sympatry (Searcy and Nowicki 2005), which could promote reproductive isolation if they are forced to set up territories elsewhere. Tests in sympatry often reveal that males do not dis- criminate between heterospecific and conspecific signals—this is interpreted as lack of a behavioral barrier, which could promote hybridization (Gee 2005; den Hartog et al. 2008). For the majority of playback studies it is common to test only 1 sex, males, and indirectly infer similar signal discrimination and/or preference by females. This practice is prevalent because it is easier to conduct male playback experiments than female preference experiments in many taxa. However, such an interpreta- Male white-crowned sparrow responding to simulated tion of discriminatory response is problematic, in that it assumes that the relative territorial intrusion during playback experiment. Photo salience of conspecific and heterospecific signals to an individual territory holder by Elizabeth P. Derryberry. is a suitable proxy for female discrimination and even female preference. While male signals can be important for both male–male competition and female choice, the 2 sexes may not have evolved the same dis- criminatory abilities, nor should we expect them to respond similarly to a potential heterospecific competitor versus a potential heter- ospecific mate. We should therefore be interested in the direct value of territorial playback experiments—for understanding species recognition in territorial defense, rather than indirectly interpreting tendency for reproductive isolation between males and females. To understand how male and female discrimination between conspecific and heterospecific sexual signals compare, we should explic- itly test responses in both males and females of the same species. One successful example of this is a recent study in the Ficedula fly- catchers, which found that females discriminate between conspecific and heterospecific sexual signals in sympatry, whereas males did not (Wheatcroft and Qvarnstro ¨ m 2017). Given that sexual signals are often multimodal (e.g., acoustic and visual) and multicompo- nent (e.g., multiple messages encoded) (Hebets and Papaj 2005), future work should also test the relative salience of specific compo- nents of signals for species recognition in males versus females. the auditory signal reception of dendrobatid frogs Allobates femora- ECD can be difficult and these processes may not be mutually exclu- lis (Ame ´ zquita et al. 2006) and the male nuptial color of three- sive (Grether et al. 2009; Okamoto and Grether 2013). For instance, spined sticklebacks (Gasterosteus aculeatus spp.) (Albert et al. character displacement in bill morphology, male song, and response 2007). One open question is whether the character shift is expected to song have been demonstrated between sympatric species of to occur more often for the competitively inferior species, due to African tinkerbirds Pogoniulus bilineatus and P. subsulphureus (Kirschel et al. 2009), but the mechanism driving character displace- selection for access to resources monopolized by the dominant ment is not known. Clear cases of ACD must demonstrate that species. Divergence in competitive signals also involved in mate recogni- divergence in male traits is due to competition over mating resour- tion can promote reproductive isolation if females discriminate ces, and not due to selection for species-specific mate recognition by between these species-specific competitive signals and prefer to mate females (Okamoto and Grether 2013), which has been shown in the Hetaerina damselflies (Drury and Grether 2014). The traditional with conspecifics (Okamoto and Grether 2013). In the hybrid zone perspectives of sexual selection emphasize RCD on male sexual between pied flycatchers Ficedula hypoleuca and collared flycatch- ers Ficedula albicollis, both ACD and RCD may explain a diver- traits and female recognition, and ACD on male agonistic traits and gence in male plumage in sympatry, which both reduces recognition (see Figure 1, pathway 1A of conceptual framework). An apparent knowledge gap is whether RCD can occur on female heterospecific aggression and heterospecific pairing. Brown morph sexual traits and male recognition, and ACD can occur for female F. hypoleuca males are found in sympatry with competitively domi- agonistic traits and competitor recognition. Evidence is likely to be nant and black F. albicollis, and they receive less interspecific aggres- found in systems where male exercise mate choice and females com- sion than F. hypoleuca black morphs (Sætre et al. 1993; Alatalo pete over shared mating resources. et al. 1994). Female F. hypoleuca prefer brown conspecifics in sym- patry with F. albicollis, but prefer black conspecifics in allopatry (Sætre et al. 1997; Sæther et al. 2007). Because the same traits are Competitive asymmetry and reproductive exclusion often used for species recognition by both potential competitors and Divergence in competitive morphology and behavior of lineages in mates (Berglund et al. 1996), disentangling ACD from RCD and allopatry can result in the superior competitive ability of one lineage Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 80 Current Zoology, 2018, Vol. 64, No. 1 over the other upon secondary contact. A recent review found that Interspecific intrasexual conflict most aggressive interactions between closely related bird species Agonistic interactions can occur not only between the same sex of different species (e.g., male–male and female–female interspecific were asymmetric (Martin et al. 2017). Competitive asymmetry that interactions), but also between males and females of different species reduces interactions between species can lead to reproductive isola- (e.g., female–male interspecific interactions). Female aggression tion. For instance, if one of the species is a superior competitor and resources are limited, the dominant species may displace the subor- against male heterospecifics can promote reproductive isolation. For example, females at risk of interspecific pairings between salmon dinate species via competitive exclusion (Gause 1934; Hardin and brown trout showed higher rates of aggression against hetero- 1960). The expectations for ecological competitive exclusion are specific males and reduced the number of eggs available for spawn- similar to those for reproductive exclusion, also known as sexual ing (Beall et al. 1997). In other cases, however, females are unable exclusion—when the dominance of one species in monopolizing ter- to exert conspecific mate choice, for example in insect and water- ritories and mates displaces the less competitive species and excludes fowl species where males force copulations (Mckinney et al. 1983; them from establishing residence in sympatry (Kuno 1992; Arnqvist and Rowe 2002). This antagonistic coevolution between Hochkirch et al. 2007; Gro ¨ ning and Hochkirch 2008). As the out- females and males is known as sexual conflict, when the 2 sexes come of both ecological competitive exclusion and reproductive have different evolutionary interests (Parker and Partridge 1998). exclusion is that the species cannot coexist (Pfennig and Pfennig Within species, sexual conflict can be a driver of speciation, and can 2012), local extinction that reduces interspecific interactions could promote rapid evolutionary divergence of reproductive traits promote reproductive isolation between populations. For example, (Arnqvist et al. 2000; Martin and Hosken 2003). For instance, sex- an experiment with Callosobruchus maculatus and C. chinensis ual conflict can result in antagonistic coevolution of genital mor- weevils demonstrated that indiscriminate male mating attempts phology as well as color signaling and perception, resulting in sexual toward heterospecifics, linked with intolerance by female C. macula- polymorphisms (Hosken and Stockley 2004; Brennan et al. 2010; tus females, resulted in reduced reproduction, population decline, Gavrilets 2014). Female Ischnura ramburii have evolved male visual and local extinction of C. maculatus (Kishi et al. 2009). The expan- mimicry to resist male harassment, which can promote mate recog- sion of a more dominant and/or invasive species’ range, exacerbated nition errors by males (Gering 2017). A color polymorphism in the by anthropogenic changes such as habitat modification and climate wing patterns of Colias butterflies allows females with the rare change, can accelerate the geographical displacement of a less domi- “alba” morph to avoid reproductive interference, as a means of nant species (Rhymer and Simberloff 1996; Krosby et al. 2015). resistance to interspecific male mating harassment (Nielsen and When the species co-occur throughout their distribution, or the Watt 2000). Female sexual polymorphisms due to variation in resist- more dominant species expands its range (Canestrelli et al. 2016), ance or toleration of unwanted mating could lead to speciation, but the less dominant species could become locally extinct (Duckworth this has largely been explored within a species (Svensson et al. 2008; Pfennig and Pfennig 2012). In a simulation study, the compet- 2009). Interspecific sexual conflict, between males and females of itive ability of a native plant species via faster pollen-tube growth different species, could occur if heterospecific mating promoted by rates and enhanced seedling competition was predicted to prevent indiscriminate males is opposed by female preference for conspe- the risk of extinction due to both natural hybridization with invad- cifics. There are several cases of forced copulations resulting in ing plant species and competition with hybrids and invasives (Wolf hybrids (Randler 2005; Rohwer et al. 2014) but it is unknown et al. 2001). Species that are already rare are more vulnerable to whether females have evolved postmating divergence in genital mor- extinction by hybridization (Levin et al. 1996). Reproductive exclu- phology or other traits to avoid coercive heterospecific mating. To sion is expected to promote reproductive isolation, but examples are what extent does interspecific sexual conflict, involving the opposi- limited. Evidence of this process is likely difficult to observe in tion of competition and mate choice, promote reproductive isolation nature because it does not leave a genetic trace, as is the case with between species? hybridization. The consequences of male–male competition for reproductive When Competition in Secondary Contact exclusion and reproductive isolation are likely to be similar in Facilitates Introgressive Hybridization female–female competition, if females of one species outcompete another for mating resources, for example territories for breeding. Reproductive competition between sympatric lineages can also pro- Female–female agonistic interactions that occur within species have mote hybridization, if interspecific interactions over shared mating been predicted to promote diversification and incipient speciation. resources occur and reproductive isolation is incomplete. The pre- Females of some haplochromine cichlid species with bright colora- vious section explained how divergence in competitive traits tion are territorial and aggressive, and use color as a cue in social between lineages could lead to reproductive exclusion, but competi- interactions (Seehausen et al. 1999). An experimental assay in the tive asymmetry can also facilitate a dominant lineage’s monopoliza- cichlid species Neochromis omnicaeruleus demonstrated that tion of breeding with both conspecific and heterospecific mates. females bias aggression toward females of their own color morph Some patterns indicating these processes include asymmetric intro- (Dijkstra et al. 2009). Neochromis omnicaeruleus exhibits mutual gression of genetic loci and phenotypic traits, as well as moving mate choice (Seehausen et al. 1999), and females compete for males hybrid zones. Hybridization itself can result in the superior competi- of the same morph. Furthermore, female coloration is associated tive ability of hybrids relative to their parental taxa, which can fur- with behavioral dominance among female morphs (Dijkstra et al. ther promote backcrossing. While one outcome of interspecific 2009). How competitive interactions between females of the same reproductive competition is divergence in sexual traits, competitive species compare to female competition between 2 species, and signals that facilitate territorial interactions can also converge whether both of these processes are expected to contribute to diver- between species, which can also promote hybridization. The major- sification and reproductive isolation, is an exciting avenue for future ity of evidence for these processes has been found between males of research. species that compete for mating resources, but recent evidence Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Lipshutz  Female competition and speciation 81 suggests that female–female competition can also promote females (Supriatna 1991; Bergman and Beehner 2003). Genetic pat- hybridization. terns of introgression for autosomal loci and mtDNA suggest that hybridization occurs between M. tonkeana males and M. maura females (Evans et al. 2001). Unidirectional introgression of mtDNA, Competitive asymmetry and directional hybridization autosomal loci, and/or phenotypic traits can be explained by sexual Competitive asymmetry can lead to asymmetric introgression,in selection, either due to the competitive dominance of 1 species, or to which loci and traits that confer a reproductive advantage and are inherited from a competitively superior parental species progress mate choice favoring 1 species. It can also be found between females into the hybrid zone farther than background neutral loci (Barton of a rare species and males of a common species in sympatry (Wirtz 1979; Pia ´ lek and Barton 1997). For example, an asymmetry in 1999). Patterns suggesting unidirectional hybridization can addi- male–male competition between 2 lineages of common wall lizards tionally be explained by the reduction in fitness from 1 cross type Podarcis muralis may be promoting directional hybridization due to deleterious epistatic interactions—so-called “Darwin’s (While et al. 2015). The lineages are divergent in competitive Corollary to Haldane’s Rule (Turelli and Moyle 2007). Studies test- morphology—males of the northern Italian subspecies Podarcis ing whether pre-mating behaviors can explain patterns of asymmet- muralis nigriventris have larger heads, stronger bite force, and ric introgression should also consider alternative, but not necessarily greater testes mass compared with the Western Europe subspecies mutually exclusive hypotheses of post-mating and postzygotic repro- Podarcis muralis brogniardii. Podarcis muralis nigriventris males ductive isolation (e.g., Carling and Brumfield 2008). For example, are more aggressive and dominant to P.m. brogniardii males in terri- unidirectional hybridization between 2 sunfish species Lepomis torial interactions, which allows them to monopolize high-quality macrochirus and Lepomis gibbosus was explained by both asym- territories and courtship of both conspecific and heterospecific metric conspecific sperm precedence and hybrid inviability of 1 cross females (MacGregor et al. 2017). Sexual traits associated with P.m. (Immler et al. 2011). nigriventris males, including head size and dorsal and ventral colora- Asymmetric introgression can also lead to a moving hybrid zone. tion, are introgressing into the hybrid zone (While et al. 2015). Moving hybrids zones can occur between sympatric species with Directional hybridization can occur particularly when male– asymmetric competitive interactions that result in the geographic male competition is a stronger determinant of mating than female and/or genetic displacement of the inferior competitor via hybridiza- mate preferences (e.g., Reichard et al. 2005). For example, in experi- tion. Especially when an aggressive phenotype is linked with greater mental secondary contact among Tropheus cichlid fish of different dispersal (Duckworth and Badyaev 2007; Canestrelli et al. 2016), color morphs, dominance of the red male morph interfered with range expansion of the superior competitor can cause a hybrid zone positive assortative mating preferences by females and promoted to move over time. In the Setophaga hybrid zone between hermit asymmetric hybridization (Sefc et al. 2015). When males of a domi- Setophaga occidentalis and Townsend’s S. townsendi warblers, nant lineage displace lower-ranked males of the subordinate lineage S. occidentalis are superior competitors over breeding territories and from breeding territories, their conspecific females are left with no mates, and hybrids are intermediate to parentals in aggression choice but to join the territory of a heterospecific in order to repro- (Pearson 2000; Owen-Ashley and Butler 2004). While hybridization duce (Wirtz 1999). However, particularly when hybridization is is restricted to narrow zones, S. townsendi mtDNA is found in a maladaptive, females could still exercise choice for conspecifics phenotypically pure S. occidentalis population (Krosby and Rohwer through extra-pair mating with nearby conspecific males. This hap- 2009), and a resampling of hybrid zone sites 10–20 years later indi- pens, for example, in fur seals that pursue extra-territory insemina- cated they have become more townsendi-like over time (Krosby and tions when their phenotype did not match that of territorial mates Rohwer 2010). This geographic replacement of the competitively (Goldsworthy et al. 1999). The outcomes of interspecific male–male inferior S. occidentalis (Krosby and Rohwer 2010) could ultimately competition for hybridization in the Podarcis wall lizards may be result in its extinction. Hybridization between species with asym- influenced by weak female preference as well as by male mate choice metric competitive abilities can have important conservation for conspecifics (Heathcote et al. 2016). Although P.m. nigriventris implications—resulting in the extirpation of the less competitive lin- males outcompete P.m. brogniardii males for mating opportunities eage through genetic or demographic swamping, but also facilitating in the hybrid zone, P.m. nigriventris males prefer to mate guard the genetic rescue (reviewed in Allendorf et al. 2001; Mooney and largest females, which are typically also P.m. nigriventris, thereby Cleland 2001; Todesco et al. 2016; vonHoldt et al. 2017). Female promoting assortative mating and reducing gene flow between the 2 choice in conjunction with male–male competition can also facilitate lineages (Heathcote et al. 2016). These examples demonstrate some hybrid zone movement. For example, females of both black-capped of the ways competition and mate choice can interact to promote (Poecile atricapillus) and Carolina (Poecile carolinensis) chickadees similar or opposing outcomes for hybridization. When possible, display mate choice for dominant males, which are typically P. caro- empirical studies on the behavioral mechanisms of hybridization linensis (Bronson et al. 2003). The dominance of P. carolinensis should investigate the contributions of both male and female behav- males over territories and mates can explain its northward range ior separately, to understand the interactions between competition expansion and the northern movement of the hybrid zone, but cli- and mate choice (Wong and Candolin 2005). mate change can also explain this movement (Taylor et al. 2014). Unidirectional hybridization resulting from competitive asymme- Because hybrid zone movement can be explained by many other tries can yield increased prevalence of 1 heterospecific cross—for drivers including mate choice, postzygotic genetic incompatibilities, example, mating between females of 1 species with males of the and environmental change (Buggs 2007), hypotheses for competi- competitively dominant species, but the reciprocal cross is rare. A tion as a driver of asymmetric introgression and hybrid zone move- pattern of mitochondrial DNA (mtDNA) of only 1 parental species ment should be explicitly tested, for example by comparing found in hybrids can suggest unidirectional hybridization. For exam- aggression to simulated territorial intrusion (e.g., Billerman and ple in hybridizing macaques, the Tonkean macaque (Macaca ton- keana) has more intense male–male competition for mates, and may Carling 2017; Lipshutz 2017). These are not mutually exclusive be outcompeting the Moor macaque (M. maura) for M. maura processes, however, as the presence of competitive asymmetries is a Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 82 Current Zoology, 2018, Vol. 64, No. 1 necessary but not sufficient demonstration that competition is a key hybridization—phenotypic hybrids only had J. spinosa mtDNA hap- driver of hybrid zone movement. lotypes, suggesting predominant crosses between J. spinosa females When mate choice is based on an evaluation of traits also and J. jacana males (Miller et al. 2014). Unidirectional introgression involved in competitive interactions, it can be difficult to disentangle of J. spinosa mtDNA across the hybrid zone may be explained by the effects of reproductive competition from mate choice on hybrid- interspecific female–female competition for mates, whereby ization (e.g., Mennill et al. 2002). In the golden-collared Manacus the larger body size, spur length, and higher aggression of female candei and white-collared Manacus vitellinus manakin hybrid zone, J. spinosa allow them to exclude female J. jacana from obtaining ter- male–male competition may be driving asymmetric introgression of ritories in mixed-species populations (Lipshutz 2017). While inter- gold plumage across the hybrid zone, as M. candei males are more specific female–female competition over territories and mates may aggressive than M. vitellinus males and plumage color is associated be more likely to influence hybridization outcomes in species with with aggression (Mcdonald et al. 2001). However, this pattern may polyandrous mating systems, to what extent does female–female also be driven by female preference for M. candei males in mixed competition impact the likelihood of hybridization in other mating leks (Brumfield et al. 2001; Stein and Uy 2006). As with identifying systems? the drivers hybrid zone movement and distinguishing between ACD and RCD, we should test alternative hypothesis for competition ver- Adaptive introgression of competitive traits sus mate choice in driving asymmetric introgression, for example Heterospecific mating is often considered an accidental byproduct with experimental tests of interspecific competition (While et al. of incomplete species recognition, which reduces fitness due to 2015) and mate choice (Heathcote et al. 2016) in the same system. wasted time, energy, and gametes. However, hybridization can also be adaptive (Willis 2013). While this review has thus far examined Female–female competitive asymmetry how competition influences the likelihood for hybridization, hetero- Could competitive asymmetries between females of sympatric spe- typic mating can also increase competitive ability. For example, cies promote hybridization, in a similar fashion to males? Within a hybrid tadpoles between S. bombifrons and S. multiplicata develop species, competitive phenotypes in females can influence mating suc- more rapidly and are more likely to achieve metamorphosis than S. cess. In the social lizard Egernia whitii, more aggressive females bombifrons tadpoles, which can facilitate survival in ephemeral have more extra-pair offspring (While et al. 2009). Between species, ponds. Spea bombifrons females become more likely to hybridize female–female competition for mating opportunities is less under- with S. multiplicata males when water levels are low (Pfennig et al. stood. Interspecific female–female competition for male sperm has 2002; Pfennig and Rice 2007), suggesting that unidirectional hybrid- been documented between mollies Poecilia latipinna and a unisexual ization is adaptive in certain environments. Inheritance of competi- species of hybrid origin Poecilia formosa from crossings of P. lati- tive traits from the dominant parental lineage could also provide pinna and P. mexicana (Riesch et al. 2008). In order to trigger hybrids with a selective advantage over the competitively inferior embryogenesis, hybrid female P. formosa require sperm from either lineage. parental species, known as sexual parasitism (Schlupp 2009). While Heterosis, or hybrid vigor, occurs when hybrids are competi- P. formosa was more aggressive toward P. latipinna than vice versa, tively superior to their parental species (Birchler 2003), and can also it is unknown what role interspecific female competition plays in result in reduction or extinction of parental species. A pattern of maintaining the Poecilia species complex (Makowicz and Schlupp hybrids outcompeting their parental taxa is particularly associated 2015). That aggressive females are more promiscuous could influ- with invasive species (Py sek et al. 2003; Suehs et al. 2004). Hybrids ence their likelihood of mating with a heterospecific. Costs of heter- between 2 morphs of invasive Thiarid snail Melanoides tuberculata ospecific mating may be higher in females because of gametic and are produced sexually, but the hybrid morphs reproduce asexually parental investment (Wirtz 1999), but these costs may be lowered if via apomictic parthenogenesis (Samadi et al. 1999). Hybrid morphs females mate with multiple males. For example, one experimental are superior competitors to their parental taxa in natural habitats by study of Gryllus crickets demonstrated that mating barriers between having greater colonization ability and larger bodied offspring hybridizing species were weakest among females of the more poly- (Facon et al. 2005, 2008), and are mostly female (B. Facon, personal androus species (Veen et al. 2011). Females of the more polyandrous communication). There are several other examples where hybrids species, Gryllus bimaculatus discriminated less and mated more are superior competitors to parentals, for example in several crosses with heterospecific males. Therefore, we might expect females in of Darwin’s finches (Geospiza sp.) where hybrids have higher breed- polyandrous systems, especially those that compete for mates, to ing success (Grant and Grant 1992), and in hybrid gulls between Larus occidentalis and Larus glaucescens because of the combina- mate less discriminately than females in monogamous mating systems. tion of adaptive traits from parentals in an intermediate environ- Interspecific female–female competition in polyandrous mating ment (Good et al. 2000). Heterosis can also be a mechanism of systems, in which females compete for access to male mates, may be speciation if hybrids are reproductively isolated from their parental analogous to interspecific male–male competition. Because polyan- species. This can occur due to an inversion (Lowry and Willis 2010) drous females have multiple opportunities to breed, they may face or allopolyploidy (Comai 2005; Van de Peer et al. 2017), which is lower costs of heterospecific mating (Arnqvist et al. 2000). One more common for plants (Abbott et al. 2016) but also documented example is a hybrid zone between 2 polyandrous sex-role reversed in animals (Mable et al. 2011). Heterosis can also be associated with bird species, the wattled jacana Jacana jacana and the Northern a hybrid swarm because of the production of highly fit recombinant jacana Jacana spinosa (Miller et al. 2014; Figure 2). Female jacanas genotypes that erode parental genetic boundaries, for example in the of both species control access to mates by competing for territories copepod Tigriopus californicus (Hwang et al. 2011). In a hybrid encompassing a harem of males. Females are under stronger selec- swarm between Pecos pupfish (Cyprinodon pecosensis) and sheeps- tion for increased aggression and larger body size and spur weap- head minnow (C. variegatus), male–male competition is asymmetric onry, while males provide parental care (Jenni and Collier 1972; (Rosenfield and Kodric-Brown 2003). Male C. variegatus as well as Emlen and Wrege 2004a, 2004b). There is an asymmetry of F1 hybrids outcompeted male C. pecosensis for mates, suggesting Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Lipshutz  Female competition and speciation 83 hybrid vigor can promote extensive hybridization via competition. When females compete, is the evolution of competitive signals The adaptiveness of hybridization is based on the fitness of hybrids and recognition in females predicted to have similar outcomes for hybridization as those found in males? For species in which both relative to parental species, and this can be challenging to quantify males and females defend territories, we might expect the sexes to but useful for understanding how and why hybridization occurs. For have similar patterns of agonistic signal evolution. This can depend species in which hybridization is maladaptive, introgression of traits on whether the agonistic signals are also used in mate choice deci- that increase a hybrid individual’s competitive advantage may be sions for either sex (Wong and Candolin 2005). If male signals are undermined by lower survival due to incompatibilities for other loci. under selection in both choice and competition contexts, but female signals are not, then we might predict fewer constraints on the direc- Convergence in agonistic signals tion of evolution of female signals. In a scenario where convergence Although studies of interspecific competition typically focus on the in agonistic signals facilitates interspecific territorial interactions, evolution of trait divergence, competition over shared mating female agonistic signals may be more likely to converge in secondary resources can actually drive convergence in signals and signal recog- contact, whereas male signals may be expected to be more divergent nition involved in territorial defense to facilitate aggressive interac- to facilitate species recognition. However, if males use female ago- tions between heterospecifics (Cody 1969; Tobias and Seddon 2009; nistic signals to select a mate, then we should see similar patterns of Vokurkova ´ et al. 2013). Convergence in competitive signals has convergence in the agonistic signals of both sexes. In a sympatric been found within an avian radiation of ovenbirds (Furnariidae), species pair of Neotropical antbirds, Hypocnemis peruviana and H. whereby species coexistence predicted convergence in male song subflava, both males and females sing to defend territories, and (Tobias et al. 2013). Agonistic signal convergence could evolve due interspecific aggression is intense (Tobias and Seddon 2009). Both to direct interactions in competing over shared ecological or mating male and female songs converged in sympatry, likely due to social resources (Grether et al. 2009; Dufour et al. 2015; Laiolo 2017), or selection, which includes competition for ecological resources in because of acoustic adaptation to a shared environment (e.g., addition to mate acquisition (West-Eberhard 1983; Tobias et al. Cardoso and Price 2010). Convergence in competitive signals can 2012). Interestingly, female songs showed greater similarity in also occur due to hybridization (Grant et al. 2004; Secondi et al. acoustic structure in sympatry than male songs, potentially because 2011), either if signals are genetically determined and are intermedi- of selection on male song for females to discriminate between con- ate to parental signals (e.g., de Kort et al. 2002; Gee 2005), or due specifics and heterospecifics and avoid hybridization (Searcy and to learning if offspring imprint on the songs of heterospecifics (e.g., Brenowitz 1988). Although hybridization does not occur between Secondi et al. 2003; Haavie et al. 2004). these species, this study can provide insight for female versus male While signal convergence between sympatric species is expected agonistic signal evolution resulting from interspecific interactions. to facilitate competitor recognition and interspecific territoriality Female territorial signals may be less constrained by conspecific (Grether et al. 2009), it could also increase the probability of hetero- mate recognition than male signals, and can therefore evolve more specific pairing and hybridization, especially in species that use the strongly in response to interspecific competition than male signals. same signals to both defend territories and attract a mate (Berglund Currently, there are no known studies of ACD in female competitive et al. 1996; Wong and Candolin 2005). For example, in sympatric traits and/or species recognition. Are female agonistic signals more Ficedula flycatchers, the pied flycatcher F. hypoleuca song converges likely to converge or diverge in secondary contact with closely with the song of the more dominant collared flycatcher (F. albicollis) related competitors, in comparison to male signals? by incorporating learned parts of its song repertoire (Haavie et al. 2004). This mixed singing leads to heterospecific pairing and increases the likelihood of hybridization (Qvarnstro ¨ m et al. 2006). Conclusions and Next Steps However, the convergence of male song and song discrimination to This review has examined the processes by which reproductive com- facilitate territorial competition is opposed by stricter female choice petition between species in secondary contact promotes reproductive in sympatry (Wheatcroft and Qvarnstro ¨ m 2017). These findings, isolation versus hybridization. When possible, I have compared the that divergence in species recognition can evolve in females along evidence for male–male competition to that of female–female com- with convergence in male sexual signals, provide a more inclusive petition, but thus far both theoretical and empirical studies are rare understanding of reproductive isolation in the flycatcher system. for female competition. Interspecific competition that promotes the This study adds to an emerging understanding that signal discrimi- divergence of sexual traits and/or recognition between species via nation may diverge between the sexes, based on different selective character displacement, as well interspecific interactions that result pressures of mate and competitor recognition. In another example, a in reproductive exclusion, can promote reproductive isolation study of 2 sympatric Hypocnemis antbird species found that females (Figure 1: Conceptual framework). While evidence for ECD, RCD, discriminate between conspecific and heterospecific males in sympa- and ACD includes the involvement of both males and females, try, despite convergence in male song (Seddon and Tobias 2010). reproductive exclusion has only been documented in males. Concerning interspecific communication in secondary contact, the Competition between species in secondary contact can also promote evolution of signal recognition is expected to facilitate competition hybridization, for instance when a dominant species monopolizes over a shared mating resource in males and to avoid maladaptive mating resources, sometimes leading to asymmetric introgression. hybridization in females. Both convergent and divergent character Convergence in sexual traits and recognition due to competition can displacement on the same sexual signals and their recognition can also increase the likelihood for hybridization if the same traits are therefore have opposing outcomes for reproductive isolation in involved in mate choice. Hybridization itself can cause the introgres- males versus females (see Box 2). When this tension exists, the selec- sion of competitive traits, which can facilitate further hybridization. tive pressures resulting divergent RCD dominate those favoring con- Evidence for the involvement of both males and females has been vergent ACD, due to the costs of reproduction outweighing the costs found in all of these processes, though the male examples are strik- of aggression (Okamoto and Grether 2013). ingly more prevalent. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 84 Current Zoology, 2018, Vol. 64, No. 1 Allender CJ, Seehausen O, Knight ME, Turner GF, Maclean N, 2003. Our understanding of how male–male competition influences Divergent selection during speciation of Lake Malawi cichlid fishes inferred hybridization outcomes is solidifying. Still, the predictions for how from parallel radiations in nuptial coloration. Proc Natl Acad Sci USA 100: female choice can reinforce reproductive isolation via selection for 14074–14079. male trait divergence are more clearly developed than the predic- Allendorf FW, Leary RF, Spruell P, Wenburg JK, 2001. The problems with tions for how male–male competition can influence hybridization. hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622. This is paradoxical, because most empirical studies examining Alatalo RV, Gustafsson L, Lundberg A, 1994. Male coloration and species rec- whether sexual trait divergence promotes reproductive isolation are ognition in sympatric flycatchers. Proc R Soc Lond B 256:113–118. carried out by testing male–male interactions and not male–female Ame ´ zquita A, Ho ¨ dl W, Lima AP, Castellanos L, Erdtmann L et al., 2006. interactions, due to logistical challenges (see Box 2: Playback Masking interference and the evolution of the acoustic communication sys- tem in the Amazonian dendrobatid frog Allobates Femoralis. Evolution 60: experiments). Only by testing both competition and mate choice 1874–1887. within the same study systems can we disentangle whether the mat- Anderson CN, Grether GF, 2010a. Character displacement in the fighting col- ing behavior of males and females impedes or promotes the evolu- ours of Hetaerina damselflies. Proc R Soc B Biol Sci 277:3669–3675. tion of reproductive isolation. Anderson CN, Grether GF, 2010b. Interspecific aggression and character dis- Does taking a non-traditional perspective change our under- placement of competitor recognition in Hetaerina damselflies. Proc R Soc B standing of how sexual selection impacts the process of reproductive Biol Sci 277:549–555. isolation? For those systems in which females of different species Andersson M, 1994. Sexual Selection. Princeton: Princeton University Press. compete for shared mating resources, the likelihood for female– Arbuthnott D, Crespi BJ, 2009. Courtship and mate discrimination within and female competition to promote reproductive isolation versus between species of Timema walking-sticks. Anim Behav 78:53–59. Arnqvist G, Edvardsson M, Friberg U, Nilsson T, 2000. Sexual conflict pro- facilitate hybridization depends on the cost of mating with a hetero- motes speciation in insects. Proc Natl Acad Sci USA 97:10460–10464. specific. Mating behavior is just one component of species interac- Arnqvist G, Rowe L, 2002. Antagonistic coevolution between the sexes in a tions that influences the potential for hybridization between lineages group of insects. Nature 415:787–789. in secondary contact, and the evolutionary context of interacting lin- Arnqvist G, Rowe L, 2005. Sexual Conflict. Princeton: Princeton University eages is important to consider. The outcomes for reproductive isola- Press. tion depend not only on interspecific competition and mate choice, Baker MC, 2001. Bird song research: the past 100 years. Bird Behav 14:3–50. but also the fitness costs to hybridization, which can be related to Baldassarre D, Webster M, 2013. Experimental evidence that extra-pair mat- the age of divergence between the interacting lineages and accumu- ing drives asymmetrical introgression of a sexual trait. Proc R Soc B Biol Sci 280:1–7. lation of genetic incompatibilities (Pfennig 1998; Ord et al. 2011; Barton NH, 1979. The dynamics of hybrid zones. Heredity 43:341–359. Drury et al. 2015). For instance, the accumulation of intrinsic Bateman AJ, 1948. Intra-sexual selection in Drosophila. Heredity 2:349–368. genetic incompatibility over time is likely to select for species recog- Beall E, Moran P, Pendas A, Izquierdo J, Garcia Vazquez E, 1997. nition traits to avoid heterospecific mating. As females typically Hybridization in natural populations of salmonids in South-West Europe have higher gametic and parental investment and fewer opportuni- and in an experimental channel. Bull Fr Peche Piscic 344:271–285. ties for multiple mating attempts, one prediction is that male compe- Berglund A, Bisazza A, Pilastro A, 1996. Armaments and ornaments: an evolu- tition is more likely to result in hybridization than female tionary explanation of traits of dual utility. Biol J Linn Soc 58:385–399. competition. Future empirical and theoretical work should explicitly Bergman TJ, Beehner JC, 2003. Hybrid zones and sexual selection: insights test this prediction on the outcome of intraspecific competition for from the Awash baboon hybrid zone (Papio hamadryas Anubis P. h. ham- adryas). In: Jones C, editor. Sexual Selection and Primates: New Insights hybridization in males versus females, in the context of the strength and Directions. Norman: American Society of Primatologists, 500–537. of intrinsic incompatibilities between sympatric lineages. Billerman SM, Carling MD, 2017. Differences in aggressive responses do not contribute to shifts in a sapsucker hybrid zone. Auk 134:202–214. Birchler JA, 2003. In search of the molecular basis of heterosis. Plant Cell Acknowledgments Online 15:2236–2239. Thanks to Ole Seehausen and his group at EAWAG and the Bonduriansky R, 2001. The evolution of male mate choice in insects: a synthe- University of Bern, including Ayana De Brito Martins, Joana Meier, sis of ideas and evidence. Biol Rev Camb Philos Soc 76: Florian Moser, Marcel Hasler, as well as K. Okamoto, Erik Enbody, S1464793101005693. Elizabeth Derryberry, special editor Robin Tinghitella, and three Brennan PLR, Clark CJ, Prum RO, 2010. Explosive eversion and functional morphology of the duck penis supports sexual conflict in waterfowl genita- anonymous reviewers for comments on the manuscript. lia. Proc R Soc B 277:1309–1314. Bronson CL, Grubb TC, Sattler GD, Braun MJ, 2003. Mate preference: a pos- sible causal mechanism for a moving hybrid zone. Anim Behav 65:489–500. Funding Brown W, Wilson EO, 1956. Character displacement. Syst Zool 5:49–64. S.E.L. was supported by a National Science Foundation (NSF) Graduate Brumfield RT, Jernigan RW, McDonald DB, 2001. Evolutionary implications Research Opportunities Worldwide (GROW) Fellowship in Switzerland and of divergent clines in an avian (Manacus: Aves) hybrid zone. Evolution 55: NSF Graduate Research Fellowship under Grant No. 1154145. Any opinion, 2070–2087. findings, and conclusions or recommendations expressed in this material are Buggs RJA, 2007. Empirical study of hybrid zone movement. Heredity 99: those of the author and do not necessarily reflect the views of the NSF. 301–312. Burdfield-Steel ER, Shuker DM, 2011. Reproductive interference. Curr Biol 21:R450–R451. References Cain KE, Ketterson ED, 2012. Competitive females are successful females; Abbott RJ, Barton NH, Good JM, 2016. Genomics of hybridization and its phenotype, mechanism and selection in a common songbird. Behav Ecol evolutionary consequences. Mol Ecol 25:2325–2332. Sociobiol 66:241–252. Albert AYK, Millar NP, Schluter D, 2007. Character displacement of male Canestrelli D, Porretta D, Lowe WH, Bisconti R, Carere C et al., 2016. The nuptial colour in threespine sticklebacks Gasterosteus aculeatus. Biol J Linn tangled evolutionary legacies of range expansion and hybridization. Trends Soc 91:37–48. Ecol Evol 31:677–688. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Lipshutz  Female competition and speciation 85 Carling MD, Brumfield RT, 2008. Haldane’s rule in an avian system: using Gause F, 1934. The struggle for existence. Yale J Biol Med 7:609. cline theory and divergence population genetics to test for differential intro- Gavrilets S, 2014. Is sexual conflict an “engine of speciation”? Cold Spring gression of mitochondrial, autosomal, and sex-linked loci across the Harb Perspect Biol 6:1–14. Passerina bunting hybrid zone. Evolution 62:2600–2615. Gee JM, 2005. No species barrier by call in an avian hybrid zone between Cardoso GC, TD Price, 2010. Community convergence in bird song. Evol California and Gambel’s quail Callipepla californica and C. gambelii. Biol J Ecol 24:447–461. Linn Soc 86:253–264. Clutton-Brock T, 2007. Sexual selection in males and females. Science 318: Gering EJ, 2017. Male-mimicking females increase male–male interactions, 1882–1885. and decrease male survival and condition in a female-polymorphic damsel- Cody L, 1969. Convergent characteristics in sympatric species: a possible rela- fly. Evolution 71:1390–1396. tion to interspecific competition and aggression. Condor 71:222–239. Gill SA, Alfson ED, Hau M, 2007. Context matters: female aggression and tes- Comai L, 2005. The advantages and disadvantages of being polyploid. Nat tosterone in a year-round territorial neotropical songbird Thryothorus leu- Rev Genet 6:836–846. cotis. Proc R Soc B 274:2187–2194. Cooney CR, Tobias JA, Weir JT, Botero CA, Seddon N, 2017. Sexual selec- Goldsworthy S, Boness D, Fleischer R, 1999. Mate choice among sympatric tion, speciation and constraints on geographical range overlap in birds. Ecol fur seals: female preference for conphenotypic males. Behav Ecol Sociobiol Lett 20:863–871. 45:253–267. Coyne JA, Orr AH, 2004. Speciation. Sunderland (MA): Sinauer Associates. Good TP, Ellis JC, Annett CA, Pierotti R, 2000. Bounded hybrid superiority in Coyne JA, Orr HA, 1989. Patterns of speciation in Drosophila. Evolution 43: an avian hybrid zone: effects of mate, diet, and habitat choice. Evolution 54: 362–381. 1774–1783. Darwin C, 1871. The Descent of Man and Selection in Relation to Sex. Grant PR, 1972. Convergent and divergent character displacement. Biol J London: Murray. Linn Soc 4:39–68. Desjardins JK, Hazelden MR, Van Der Kraak GJ, Balshine S, 2006. Male and Grant PR, Grant BR, 1992. Hybridization of bird species. Science 256: female cooperatively breeding fish provide support for the “Challenge 193–197. Hypothesis.” Behav Ecol 17:149–154. Grant PR, Grant BR, 1997. Genetics and the origin of bird species. Proc Natl Dijkstra PD, Van Dijk S, Groothuis TGG, Pierotti MER, Seehausen O, 2009. Acad Sci USA 94:7768–7775. Behavioral dominance between female color morphs of a Lake Victoria Grant PR, Grant BR, Markert JA, Keller LF, Petren K, 2004. Convergent evo- cichlid fish. Behav Ecol 20:593–600. lution of Darwin’s finches caused by introgressive hybridization and selec- Dijkstra PD, Seehausen O, Pierotti MER, Groothuis TGG, 2007. Male–male tion. Evolution 58:1588–1599. competition and speciation: aggression bias towards differently coloured Grether GF, Anderson CN, Drury JP, Kirschel ANG, Losin N et al., 2013. The rivals varies between stages of speciation in a Lake Victoria cichlid species evolutionary consequences of interspecific aggression. Ann N Y Acad Sci complex. J Evol Biol 20:496–502. 1289:48–68. Doorn GSV, Dieckmann U, Weissing FJ, 2004. Sympatric speciation by sexual Grether GF, Losin N, Anderson CN, Okamoto K, 2009. The role of interspe- selection: a critical reevaluation. Am Nat 163:709–725. cific interference competition in character displacement and the evolution of Drury J, Clavel J, Manceau M, Morlon H, 2016. Estimating the effect of com- competitor recognition. Biol Rev 84:617–635. petition on trait evolution using maximum likelihood inference. Syst Biol Gro ¨ ning J, Hochkirch A, 2008. Reproductive interference between animal spe- 65:700–710. cies. Q Rev Biol 83:257–282. Drury JP, Grether GF, 2014. Interspecific aggression, not interspecific mating, Haavie J, Borge T, Bures S, Garamszegi LZ, Lampe HM et al., 2004. drives character displacement in the wing coloration of male rubyspot dam- Flycatcher song in allopatry and sympatry: convergence, divergence and selflies Hetaerina. Proc R Soc B 281:20141737. reinforcement. J Evol Biol 17:227–237. Drury JP, Okamoto KW, Anderson CN, Grether GF, 2015. Reproductive Hankison SJ, Morris MR, 2003. Avoiding a compromise between sexual selec- interference explains persistence of aggression between species. Proc R Soc tion and species recognition: female swordtail fish assess multiple B 282:20142256. species-specific cues. Behav Ecol 14:282–287. Duckworth RA, 2008. Adaptive dispersal strategies and the dynamics of a Hardin G, 1960. The competitive exclusion principle. Science 131: range expansion. Am Nat 172:S4–S17. 1292–1297. Duckworth RA, Badyaev AV, 2007. Coupling of dispersal and aggression den Hartog PM, Slabbekoorn H, ten Cate C, 2008. Male territorial vocaliza- facilitates the rapid range expansion of a passerine bird. Proc Natl Acad Sci tions and responses are decoupled in an avian hybrid zone. Philos Trans R USA 104:15017–15022. Soc B 363:2879–2889. Dufour CMS, Meynard C, Watson J, Rioux C, Benhamou S et al., 2015. Space Heathcote RJP, While GM, Macgregor HEA, Sciberras J, Leroy C et al., 2016. use variation in co-occurring sister species: response to environmental varia- Male behaviour drives assortative reproduction during the initial stage of tion or competition? PLoS ONE 10:1–15. secondary contact. J Evol Biol 29:1003–1015. Edward DA, Chapman T, 2011. The evolution and significance of male mate Hebets E, Papaj DR, 2005. Complex signal function: developing a framework choice. Trends Ecol Evol 26:647–654. of testable hypotheses complex signal function: developing a framework of Emlen ST, Oring LW, 1977. Ecology, sexual selection, and evolution of mat- testable hypotheses. Behav Ecol Sociobiol 57:197–214. ing systems. Science 197:215–223. Hochkirch A, Gro ¨ning J, Bu ¨ cker A, 2007. Sympatry with the devil: reproduc- Emlen ST, Wrege PH, 2004a. Division of labour in parental care behaviour of tive interference could hamper species coexistence. J Anim Ecol 76: a sex-role-reversed shorebird, the wattled jacana. Anim Behav 68:847–855. 633–642. Emlen ST, Wrege PH, 2004b. Size dimorphism, intrasexual competition, and Hosken D, Stockley P, 2004. Sexual selection and genital evolution. Trends sexual selection in wattled jacana Jacana jacana, a sex-role-reversed shore- Ecol Evol 19:87–93. bird in Panama. Auk 121:391–403. Huber SK, Leon LFD, Hendry AP, Bermingham E, Podos J, 2007. Evans BJ, Supriatna J, Melnick DJ, 2001. Hybridization and population genet- Reproductive isolation of sympatric morphs in a population of Darwin’s ics of two macaque species in Sulawesi, Indonesia. Evolution 55: 1686–1702. finches. Proc R Soc B 274:1709–1714. Facon B, Jarne P, Pointier JP, David P, 2005. Hybridization and invasiveness Huber SK, Podos J, 2006. Beak morphology and song features covary in a pop- ulation of Darwin’s finches Geospiza fortis. Biol J Linn Soc 88:489–498. in the freshwater snail Melanoides tuberculata: hybrid vigour is more impor- Hudson EJ, Price TD, 2014. Pervasive reinforcement and the role of sexual tant than increase in genetic variance. J Evol Biol 18:524–535. Facon B, Pointier JP, Jarne P, Sarda V, David P, 2008. High genetic variance in selection in biological speciation. J Hered 105:821–833. life-history strategies within invasive populations by way of multiple intro- Hwang AS, Northrup SL, Alexander JK, Vo KT, Edmands S, 2011. Long-term ductions. Curr Biol 18:363–367. experimental hybrid swarms between moderately incompatible Tigriopus Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 86 Current Zoology, 2018, Vol. 64, No. 1 californicus populations: hybrid inferiority in early generations yields to Mckinney F, Derrickson SR, Mineau P, 1983. Forced copulation in waterfowl. hybrid superiority in later generations. Conserv Genet 12:895–909. Behaviour 86:250–293. Immler S, Hamilton MB, Poslusny NJ, Birkhead TR, Epifanio JM, 2011. Mennill DJ, Ratcliffe LM, Boag PT, 2002. Female eavesdropping on male Post-mating reproductive barriers in two unidirectionally hybridizing sun- song contests in songbirds. Science 296:873. fish (Centrarchidae: Lepomis). J Evol Biol 24:111–120. Miller MJ, Lipshutz SE, Smith NG, Bermingham E, 2014. Genetic and pheno- Irwin DE, Price TD, 1999. Sexual imprinting, learning and speciation. typic characterization of a hybrid zone between polyandrous Northern and Heredity 82:347–354. Wattled Jacanas in Western Panama. BMC Evol Biol 14:14. Jenni DA, Collier G, 1972. Polyandry in the American Jac¸ana. Auk 89: Mooney HA, Cleland EE, 2001. The evolutionary impact of invasive species. 743–765. Proc Natl Acad Sci USA 98:5446–5451. Kirschel ANG, Blumstein DT, Smith TB, 2009. Character displacement of Moore WS, 1987. Random mating in the Northern Flicker hybrid zone: impli- song and morphology in African tinkerbirds. Proc Natl Acad Sci USA 106: cations for the evolution of bright and contrasting plumage patterns in birds. 8256–8261. Evolution 41:539–546. Kishi S, Nishida T, Tsubaki Y, 2009. Reproductive interference determines per- Nandy B, Joshi A, Ali ZS, Sen S, Prasad NG, 2012. Degree of adaptive male mate sistence and exclusion in species interactions. J Anim Ecol 78:1043–1049. choice is positively correlated with female quality variance. Sci Rep 2:1–8. de Kort SR, den Hartog PM, ten Cate C, 2002. Diverge or merge? The effect of Nielsen MG, Watt WB, 2000. Interference competition and sexual selection sympatric occurrence on the territorial vocalizations of the vinaceous dove promote polymorphism in Colias (Lepidoptera, Pieridae). Funct Ecol 14: Streptopelia vinacea and the ring-necked dove S. capicola. J Avian Biol 33: 718–730. 150–158. Okamoto KW, Grether GF, 2013. The evolution of species recognition in com- Kozak GM, Reisland M, Boughmann JW, 2009. Sex differences in mate recog- petitive and mating contexts: the relative efficacy of alternative mechanisms nition and conspecific preference in species with mutual mate choice. of character displacement. Ecol Lett 16:670–678. Evolution 63:353–365. Ord TJ, King L, Young AR, 2011. Contrasting theory with the empirical data Kraaijeveld K, Kraaijeveld-Smit FJL, Komdeur J, 2007. The evolution of of species recognition. Evolution 65:2572–2591. mutual ornamentation. Anim Behav 74:657–677. Owen-Ashley NT, Butler LK, 2004. Androgens, interspecific competition and Krosby M, Rohwer S, 2009. A 2000 km genetic wake yields evidence for species replacement in hybridizing warblers. Proc R Soc B 271:S498–S500. northern glacial refugia and hybrid zone movement in a pair of songbirds. Panhuis TM, Butlin R, Zuk M, Tregenza T, 2001. Sexual selection and specia- Proc R Soc B 276:615–621. tion. Trends Ecol Evol 16:364–371. Krosby M, Rohwer S, 2010. Ongoing movement of the hermit warbler X Parker GA, Partridge L, 1998. Sexual conflict and speciation. Philos Trans R Townsend’s warbler hybrid zone. PLoS ONE 5:e14164. Soc B 353:261–274. Krosby M, Wilsey CB, McGuire JL, Duggan JM, Nogeire TM et al., 2015. Pearson SF, 2000. Behavioral asymmetries in a moving hybrid zone. Behav Climate-induced range overlap among closely related species. Nat Clim Ecol 11:84–92. Chang 5:883–886. Van de Peer Y, Mizrachi E, Marchal K, 2017. The evolutionary significance of Kuno E, 1992. Competitive exclusion through reproductive interference. Res polyploidy. Nat Rev Genet 8:206–216. Popul Ecol 34:275–284. Peiman KS, Robinson BW, 2010. Ecology and evolution of resource-related Laiolo P, 2017. Phenotypic similarity in sympatric crow species: evidence of heterospecific aggression. Q Rev Biol 85:133–158. social convergence? Evolution 71:1051–1060. Pfennig D, Murphy P, 2003. A test of alternative hypotheses for character Lande R, 1981. Models of speciation by sexual selection on polygenic traits. divergence between coexisting species. Ecology 84:1288–1297. Proc Natl Acad Sci USA 78:3721–3725. Pfennig DW, Pfennig KS, 2012. Evolution’s Wedge: Competition and the Levin DA, Francisco-Ortega J, Jansen RK, 1996. Hybridization and the extinc- Origins of Diversity. Oakland (CA): University of California Press. tion of rare plant species. Conserv Biol 10:10–16. Pfennig DW, Rice AM, 2007. An experimental test of character displacement’s Lipshutz SE, 2017. Divergent competitive phenotypes between females of two role in promoting postmating isolation between conspecific populations in sex-role reversed species. Behav Ecol Sociobiol 71:106. contrasting competitive environments. Evolution 61:2433–2443. Lipshutz SE, Overcast IA, Hickerson MJ, Brumfield RT, Derryberry EP, 2017. Pfennig KS, 1998. The evolution of mate choice and the potential for conflict Behavioral response to song and genetic divergence in two subspecies ofwhi- between species and mate-quality recognition. Proc R Soc B 265: te-crowned sparrows Zonotrichia leucophrys. Mol Ecol 26:3011–3027. 1743–1748. Losos JB, Creer D, Glossip D, Goellner R, Hampton A et al., 2000. Pfennig KS, Pfennig DW, 2009. Character displacement: ecological and repro- Evolutionary implications of phenotypic plasticity in the hindlimb of the liz- ductive responses to a common evolutionary problem. Q Rev Biol 84: ard Anolis sagrei. Evolution 54:301–305. 253–276. Lowry DB, Willis JH, 2010. A widespread chromosomal inversion polymor- Pfennig KS, Simovich MA, Merila ¨ J, 2002. Differential selection to avoid phism contributes to a major life-history transition, local adaptation, and hybridization in two toad species. Evolution 56:1840–1848. reproductive isolation. PLoS Biol 8:e1000500. Pia ´ lek J, Barton NH, 1997. The spread of an advantageous allele across a bar- Mable BK, Alexandrou MA, Taylor MI, 2011. Genome duplication in rier: the effects of random drift and selection against heterozygotes. amphibians and fish: an extended synthesis. J Zool 284:151–182. Genetics 145:493–504. MacGregor HEA, While GM, Barrett J, Pe ´ rez I de Lanuza G, Carazo P et al., Podos J, 2010. Acoustic discrimination of sympatric morphs in Darwin’s 2017. Experimental contact zones reveal causes and targets of sexual selec- finches: a behavioural mechanism for assortative mating? Philos Trans R tion in hybridizing lizards. Funct Ecol 31:742–752. Soc B 365:1031–1039. Makowicz AM, Schlupp I, 2015. Effects of female–female aggression in a sex- Price TD, 2008. Speciation in Birds. Greenwood Village: Roberts and ual/unisexual species complex. Ethology 121:903–914. Company Publishers. Mallet J, 2005. Hybridization as an invasion of the genome. Trends Ecol Evol Ptacek M, 2000. The role of mating preferences in shaping interspecific diver- 20:229–237. gence in mating signals in vertebrates. Behav Process 51:111–134. Martin OY, Hosken DJ, 2003. The evolution of reproductive isolation Py sek P, Brock JH, Bı´mova ´ K, Manda ´ k B, Jaro sı´k V et al., 2003. Vegetative through sexual conflict. Nature 423:979–982. Martin PR, Freshwater C, Ghalambor CK, 2017. The outcomes of most regeneration in invasive Reynoutria (Polygonaceae) taxa: the determinant of invasibility at the genotype level. Am J Bot 90:1487–1495. aggressive interactions among closely related bird species are asymmetric. Qvarnstro ¨ m A, Haavie J, Saether S, Eriksson D, Pa ¨ rt T, 2006. Song similarity PeerJ 5:e2847. Mcdonald DB, Clay RP, Brumfield RT, Braun MJ, 2001. Sexual selection on predicts hybridization in flycatchers. J Evol Biol 19:1202–1209. plumage and behavior in an avian hybrid zone: experimental tests of Qvarnstro ¨ m A, Vallin N, Rudh A, 2012. The role of male contest competition male–male interactions. Evolution 55:1443–1451. over mates in speciation. Curr Zool 58:493–509. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Lipshutz  Female competition and speciation 87 Randler C, 2002. Avian hybridization, mixed pairing and female choice. Anim Seddon N, Tobias JA, 2010. Character displacement from the receiver’s per- Behav 63:103–119. spective: species and mate recognition despite convergent signals in subo- scine birds. Proc R Soc B 277:2475–2483. Randler C, 2005. Do forced extrapair copulations and interspecific brood Seehausen O, Van Alphen JJM, Lande R, 1999. Color polymorphism and sex amalgamation facilitate natural hybridisation in wildfowl? Behaviour 142: ratio distortion in a cichlid fish as an incipient stage in sympatric speciation 477–488. Reedy AM, Pope BD, Kiriazis NM, Giordano CL, Sams CL et al., 2017. by sexual selection. Ecol Lett 2:367–378. Seehausen O, Schluter D, 2004. Male–male competition and nuptial-colour Female anoles display less but attack more quickly than males in response to displacement as a diversifying force in Lake Victoria cichlid fishes. Proc R territorial intrusions. Behav Ecol 28:1323–1328. Soc B 271:1345–1353. Reichard M, Bryja J, Ondra ckova´M, Da ´ vidova ´ M, Kaniewska P et al., 2005. Sefc KM, Hermann CM, Steinwender B, Brindl H, Zimmermann H et al., Sexual selection for male dominance reduces opportunities for female mate 2015. Asymmetric dominance and asymmetric mate choice oppose premat- choice in the European bitterling Rhodeus sericeus. Mol Ecol 14:1533–1542. ing isolation after allopatric divergence. Ecol Evol 5:1549–1562. Rhymer JM, Simberloff D, 1996. Extinction by hybridization and introgres- Servedio M, Saether S, Saetre G, 2009. Reinforcement and learning. Evol Ecol sion. Annu Rev Ecol Syst 27:83–109. 23:109–123. Ribeiro JM, Spielman A, 1986. The satyr effect: a model predicting parapatry Servedio MR, 2007. Male versus female mate choice: sexual selection and the and species extinction. Am Nat 128:513–528. evolution of species recognition via reinforcement. Evolution 61: Rice AM, Pfennig DW, 2007. Character displacement: in situ evolution of 2772–2789. novel phenotypes or sorting of pre-existing variation? J Evol Biol 20: Servedio MR, Noor MAF, 2003. The role of reinforcement in speciation: 448–459. theory and data. Annu Rev Ecol Evol Syst 34:339–364. Rice AM, Pfennig DW, 2010. Does character displacement initiate speciation? Slabbekoorn H, Smith TB, 2002. Bird song, ecology and speciation. Philos Evidence of reduced gene flow between populations experiencing divergent Trans R Soc B 357:493–503. selection. J Evol Biol 23:854–865. Stein AC, Uy JAC, 2006. Unidirectional introgression of a sexually selected Riesch R, Schlupp I, Plath M, 2008. Female sperm limitation in natural popu- trait across an avian hybrid zone: a role for female choice? Evolution 60: lations of a sexual/asexual mating complex (Poecilia latipinna, Poecilia for- 1476–1485. mosa). Biol Lett 4:266–269. Stockley P, Campbell A, 2013. Female competition and aggression: interdisci- Ritchie MG, 2007. Sexual selection and speciation. Annu Rev Ecol Evol Syst plinary perspectives. Philos Trans R Soc B 368:20130073. 38:79–102. Suehs CM, Affre L, Me ´ dail F, 2004. Invasion dynamics of two alien Roberts NS, Mendelson TC, 2017. Male mate choice contributes to behaviou- Carpobrotus (Aizoaceae) taxa on a Mediterranean island: II. Reproductive ral isolation in sexually dimorphic fish with traditional sex roles. Anim strategies. Heredity 92:550–556. Behav 130:1–7. Supriatna J, 1991. Hybridization between Macaca maurus and M. tonkeana:a Rohwer S, Harris RB, Walsh HE, 2014. Rape and the prevalence of hybrids in test of species status using behavioral and morphogenetic analyses [Ph.D. broadly sympatric species: a case study using albatrosses. PeerJ 2:e409. dissertation]. Department of Anthropology, University of New Mexico. Rosenfield JA, Kodric-Brown A, 2003. Sexual selection promotes hybridiza- Svensson EI, Abbott JK, Gosden TP, Coreau A, 2009. Female polymorphisms, tion between Pecos pupfish, Cyprinodon pecosensis and sheepshead min- sexual conflict and limits to speciation processes in animals. Evol Ecol 23: now, C. variegatus. J Evol Biol 16:595–606. 93–108. Rosvall KA, 2011. Intrasexual competition in females: evidence for sexual Taylor SA, White TA, Hochachka WM, Ferretti V, Curry RL et al., 2014. selection? Behav Ecol 22:1131–1140. Climate-mediated movement of an avian hybrid zone. Curr Biol 24: Ryan MJ, Rand AS, 1993. Sexual selection and signal evolution: the ghost of 671–676. biases past. Philos Trans Biol Sci 340:187–195. Tobias JA, Cornwallis CK, Derryberry EP, Claramunt S, Brumfield RT et al., Sætre G-P, Kral M, Bicik V, 1993. Experimental evidence for interspecific 2013. Species coexistence and the dynamics of phenotypic evolution in female mimicry in sympatric Ficedula flycatchers. Evolution 47:939–945. adaptive radiation. Nature 506:359–363. Sætre G-P, Moum T, Bures S, Kral M, Adamjan M et al., 1997. A sexually Tobias JA, Montgomerie R, Lyon BE, 2012. The evolution of female orna- selected character displacement in flycatchers reinforces premating isola- ments and weaponry: social selection, sexual selection and ecological com- tion. Nature 387:589–592. petition. Philos Trans R Soc B 367:2274–2293. Sæther SA, Sætre G-P, Borge T, Wiley C, Svedin N et al., 2007. Sex chromoso- Tobias JA, Seddon N, 2009. Signal design and perception in hypocnemis ant- me-linked species recognition and evolution of reproductive isolation in fly- birds: evidence for convergent evolution via social selection. Evolution 63: catchers. Science 318:95–97. 3168–3189. Samadi S, Mava ´ rez J, Pointier JP, Delay B, Jarne P, 1999. Microsatellite and Todesco M, Pascual MA, Owens GL, Ostevik KL, Moyers BT et al., 2016. morphological analysis of population structure in the parthenogenetic fresh- Hybridization and extinction. Evol Appl 9:892–908. water snail Melanoides tuberculata: insights into the creation of clonal vari- Turelli M, Moyle LC, 2007. Asymmetric postmating isolation: Darwin’s cor- ability. Mol Ecol 8:1141–1153. ollary to Haldane’s rule. Genetics 176:1059–1088. Schlupp I, 2009. Chapter 5 Behavior of Fishes in the Sexual/Unisexual Mating Veen T, Faulks J, Rodrı´guez-Munoz ~ R, Tregenza T, 2011. Premating repro- System of the Amazon Molly Poecilia formosa. Advances in the Study of ductive barriers between hybridising cricket species differing in their degree Behavior 39:153–183. of polyandry. PLoS ONE 6:e19531. Schluter D, 2001. Ecology and the origin of species. Trends Ecol Evol 16: Vokurkova ´ J, Petruskova ´ T, Reifova ´ R, Kozman A, Mo rkovsk y L et al., 2013. 372–380. The causes and evolutionary consequences of mixed singing in two hybridiz- Searcy WA, Brenowitz EA, 1988. Sexual differences in species recognition of ing songbird species (Luscinia spp.). PLoS ONE 8:e60172. avian song. Nature 332:152–154. vonHoldt BM, Brzeski KE, Wilcove DS, Rutledge L, 2017. Redefining the role Searcy WA, Nowicki S, 2005. The Evolution of Animal Communication: of admixture and genomics in species conservation. Conserv Lett 0:1–16. Reliability and Deception in Signaling Systems. Princeton: Princeton Weber MG, Strauss SY, 2016. Coexistence in close relatives: beyond competi- University Press. tion and reproductive isolation in sister taxa. Annu Rev Ecol Evol Syst 47: Secondi J, Bordas P, Hipsley CA, Bensch S, 2011. Bilateral song convergence 359–381. in a passerine hybrid zone: Genetics contribute in one species only. Evol West-Eberhard MJ, 1983. Sexual selection, social competition, and speciation. Biol 38:441–452. Q Rev Biol 58:155–183. Secondi J, Bretagnolle V, Compagnon C, Faivre B, 2003. Species-specific song Wheatcroft D, Qvarnstro ¨ m A, 2017. Reproductive character displacement of convergence in a moving hybrid zone between two passerines. Biol J Linn female, but not male song discrimination in an avian hybrid zone. Evolution Soc 80:507–517. 71:1776–1786. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 88 Current Zoology, 2018, Vol. 64, No. 1 While GM, Michaelides S, Heathcote RJP, Macgregor HEA, Zajac N et al., Wolf DE, Takebayashi N, Rieseberg LH, 2001. Predicting the risk of extinc- 2015. Sexual selection drives asymmetric introgression in wall lizards. Ecol tion through hybridization. Conserv Biol 15:1039–1053. Lett 18:1366–1375. Wong BBM, Candolin U, 2005. How is female mate choice affected by male While GM, Sinn DL, Wapstra E, 2009. Female aggression predicts mode of competition? Biol Rev 80:559. paternity acquisition in a social lizard. Proc R Soc B 276:2021–2029. Wong BBM, Fisher HS, Rosenthal GG, 2005. Species recognition by male Willis PM, 2013. Why do animals hybridize? Acta Ethol 16:127–134. swordtails via chemical cues. Behav Ecol 16:818–822. Wirtz P, 1999. Mother species–father species: unidirectional hybridization in Woodley S, Moore M, 1999. Female territorial aggression and steroid hor- animals with female choice. Anim Behav 58:1–12. mones in mountain spiny lizards. Anim Behav 57:1083–1089. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Current Zoology Oxford University Press

Interspecific competition, hybridization, and reproductive isolation in secondary contact: missing perspectives on males and females

Free
14 pages

Loading next page...
 
/lp/ou_press/interspecific-competition-hybridization-and-reproductive-isolation-in-zeLJuqKJeO
Publisher
Oxford University Press
Copyright
© The Author (2017). Published by Oxford University Press.
ISSN
1674-5507
eISSN
2396-9814
D.O.I.
10.1093/cz/zox060
Publisher site
See Article on Publisher Site

Abstract

Research on sexual selection and hybridization has focused on female mate choice and male–male competition. While the evolutionary outcomes of interspecific female preference have been well explored, we are now gaining a better understanding of the processes by which male–male compe- tition between species in secondary contact promotes reproductive isolation versus hybridization. What is relatively unexplored is the interaction between female choice and male competition, as they can oppose one another or align with similar outcomes for reproductive isolation. The role of female–female competition in hybridization is also not well understood, but could operate similarly to male–male competition in polyandrous and other systems where costs to heterospecific mating are low for females. Reproductive competition between either sex of sympatric species can cause the divergence and/or convergence of sexual signals and recognition, which in turn influences the likelihood for interspecific mating. Future work on species interactions in secondary contact should test the relative influences of both mate choice and competition for mates on hybridization out- comes, and should not ignore the possibilities that females can compete over mating resources, and males can exercise mate choice. Key words: female–female competition, hybridization, male–male competition, reproductive isolation, sexual selection. Introduction species because of their greater investment in gametes and fewer Traditional perspectives on sexual selection and opportunities for multiple mating relative to males (Bateman 1948; hybridization Andersson 1994). In contrast, males are expected to maximize fit- Sexual signals and mating behaviors influence whether sympatric ness by mating as frequently as possible (Darwin 1871; Bateman species interbreed, and can therefore promote or impede behavioral 1948; Andersson 1994). The traditional perspective of sexual selec- reproductive isolation (Irwin and Price 1999; see Box 1: tion underlays the predictions for evolutionary outcomes in different Definitions). Interspecific hybridization is common and is estimated scenarios of secondary contact. For instance when hybridization is to occur in 10% of animals (Mallet 2005). Traditionally, research maladaptive, lineages in secondary contact are expected to evolve on the role of sexual selection in hybridization has focused on the divergence in sexually selected traits and in species recognition of importance of mate choice and species discrimination from the per- mates to avoid heterospecific mating, a process known as reinforce- spective of choosy females, and competition from the lens of aggres- ment (Coyne and Orr 1989; Servedio and Noor 2003). The predic- sive and indiscriminate males (Moore 1987; Grant and Grant 1997; tions for reinforcement have been developed from the perspective of Sætre et al. 1997; Parker and Partridge 1998; Wirtz 1999; Randler females, who face higher fitness costs of heterospecific mating mis- 2002). This conventional view considers females the gatekeepers of takes and are therefore predicted to discriminate more strongly V C The Author (2017). Published by Oxford University Press. 75 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 76 Current Zoology, 2018, Vol. 64, No. 1 this can result in high reproductive costs for females, termed the so- Box 1. Definitions called “satyr effect” (Ribeiro and Spielman 1986). Interspecific male–male competition is not widely considered to promote repro- ductive isolation except as it relates to female choice (but see 1B, Agonistic character displacement: divergence in competitive Competitive asymmetry and reproductive exclusion). signals or traits in sympatry to reduce costly interspecific Rapid divergence in sexually selected traits between closely interactions. related lineages in allopatry can promote reproductive isolation Asymmetric introgression: the unidirectional exchange of through the maintenance of species-specific signals and recognition alleles from 1 species to another. when these lineages come into secondary contact (Coyne and Orr Behavioral reproductive isolation: reduced gene flow due to 2004; Hudson and Price 2014; Weber and Strauss 2016; Cooney divergent mating signals and preferences. et al. 2017). Character shifts in sexual traits can also result from spe- Competitive asymmetry: the superior competitive ability and/ cies interactions in secondary contact. These processes have been or dominance of 1 species over another. widely explored in terms of interspecific male–female interactions Heterosis: hybrid vigor, when hybrids are competitively supe- concerning reinforcement of male traits and female recognition of rior to their parental species. those traits (see 1A, Character displacement: ecological, reproduc- Introgressive hybridization: interbreeding between 2 distinct tive, and agonistic). However, interspecific male–male interactions lineages that results in gene flow. can also impact the evolution of sexual traits, which in turn can Hybrid swarm: hybridization that erodes parental species influence hybridization outcomes. For instance, when lineages that boundaries. compete over similar ecological and/or mating resources come into Interspecific intrasexual conflict: antagonistic coevolution contact, their competitive interactions can cause selection on traits between males and females of interacting species. that influence fighting ability and competitor recognition, which can Reproductive character displacement: divergence in mating subsequently influence the evolution of reproductive isolation signals or traits in sympatry to reduce costly interspecific and/or facilitate hybridization. This process, known as agonistic mating. character displacement (ACD), can result in either divergence or Interspecific reproductive competition: competition for mates convergence of phenotypic traits involved in competitor recognition and/or mating resources between species. and fighting ability, depending on the intensity of resource competi- Reproductive exclusion: sexual interactions between species tion between species (Grether et al. 2009). Divergence in competitor that cause one to become locally extinct. signals and recognition is expected to promote reproductive isola- Secondary contact: Geographic overlap between 2 genetically tion (see Figure 1, conceptual framework). However, even species distinct lineages that derived from a common ancestor and with diverged competitive traits may hybridize if males of the domi- underwent a phase of allopatric isolation. Social selection: a form of selection resulting from all social nant species (e.g., the lineage that is superior in aggression, body interactions in order to gain access to resources, including size, and/or competitive ability) monopolize mating resources shared but not limited to mates. with males of the subordinate species. Convergence in competitive signals is expected to facilitate territorial interactions over shared, limited resources, but can also increase the likelihood of hybridiza- tion if those signals also play a role in mate recognition. Alternatively, convergence that results in the exclusion of 1 species against heterospecifics than males (Sætre et al. 1997; Parker and could promote reproductive isolation. In addition to male trait evo- Partridge 1998; Wirtz 1999; Servedio et al. 2009; Hudson and Price lution, female mate preferences may diverge or utilize a different 2014). An open question is to what extent does male–male competi- sexual trait to avoid hybridization (Hankison and Morris 2003; tion between lineages influence hybridization outcomes in secondary Seddon and Tobias 2010; Hudson and Price 2014). contact, and when is female mate choice predicted to support or oppose these outcomes? Updating perspectives on sexual selection and Recent empirical and theoretical work has brought increasing hybridization attention to the function of male–male competition in speciation Studies on mating behavior and hybridization often draw a dichot- (Doorn et al. 2004; Seehausen and Schluter 2004; Dijkstra et al. omy between competitive males mating indiscriminately and choosy 2007; Qvarnstro ¨ m et al. 2012; Drury et al. 2016). Reproductive females limiting heterospecific mating. This dichotomy is oversim- competition, also known as intrasexual selection, is a component of plified in several ways. For instance, male mate choice can facilitate sexual selection that involves fighting over mating resources such as mate discrimination within and between Timema stick insects territories and mates. Competition is an important determinant of (Arbuthnott and Crespi 2009), thereby reducing interspecific gene mating success for many taxa, especially those with polygynous or flow. Additionally, females can prefer heterospecifics when they polyandrous mating systems where reproductive success is highly resemble high-quality conspecifics and/or ancestral preferences have skewed toward dominant individuals (Emlen and Oring 1977; not diverged, as in female orange-backed fairy wrens Malurus mela- Clutton-Brock 2007). Interspecific competition is common (Peiman nocephalus melanocephalus that prefer red-backed males resembling and Robinson 2010), and interspecific reproductive competition can another subspecies M. m. cruentatus (Baldassarre and Webster occur when species compete for shared territorial and/or signaling 2013) and in female tungara frogs (Physalaemus pustulosus species space involved in mate attraction and reproduction (Grether et al. group) that prefer call features of heterospecific males (Ryan and 2009; Burdfield-Steel and Shuker 2011; Pfennig and Pfennig 2012). Rand 1993). In this review, I propose that we have overlooked an Low fitness costs to heterospecific mating for males can facilitate additional component of sexual selection that could influence introgressive hybridization when males compete over heterospecific hybridization and reproductive isolation in secondary contact: mates via male–male competition (Arnqvist and Rowe 2005), but female–female competition. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Lipshutz  Female competition and speciation 77 Figure 1. Conceptual framework of how competition between species in secondary contact can promote reproductive isolation and/or hybridization. Path labels (e.g., 1A) correspond to sections throughout the manuscript. Despite a growing understanding of male–male competition and isolation and 2) competition facilitates introgression—the exchange speciation, empirical and theoretical studies on the roles of female– of alleles from one species to another. I also emphasize that the out- female competition as well as male mate choice in hybridization are comes of interspecific interactions in secondary contact should be lacking (but see Wong et al. 2005; Servedio 2007; Kozak et al. considered in the context of both competition and mate choice, as 2009; Roberts and Mendelson 2017). There are many studies dem- well as from the perspectives of both the signaler and the receiver, onstrating that females compete over mating resources (reviewed in and I review what may be the first case of female–female competi- tion promoting hybridization (Figure 2). Rosvall 2011; Cain and Ketterson 2012) and males can be choosy of mates (reviewed in Kraaijeveld et al. 2007; Edward and Chapman 2011). Empirical studies across a wide variety of taxa including fish, When Competition in Secondary Contact lizards, and birds suggest that female aggression is adaptive in a Promotes Reproductive Isolation number of social contexts (Stockley and Campbell 2013) including Sexual selection can be a diversifying force in driving the evolution territory defense (Woodley and Moore 1999; Desjardins et al. 2006; of traits involved in mate choice and competition for mates both Gill et al. 2007; Reedy et al. 2017) and reproductive success (While within and between species (Lande 1981; Panhuis et al. 2001; et al. 2009). Likewise, adaptive mate choice has been demonstrated Coyne and Orr 2004; Ritchie 2007). Closely related lineages are for males in several insect species that face high reproductive costs often more divergent in secondary sexual characteristics than other such as sperm limitation and choose among females that vary in phenotypic traits (West-Eberhard 1983; Allender et al. 2003). quality of signals advertising fecundity (Bonduriansky 2001; Nandy Sexual characteristics specifically involved in competition include et al. 2012). As little attention as female competition and aggression those directly used in fighting, such as body size and weaponry, as have received in the literature, the role of female–female competition well as traits important in signaling dominance, such as coloration in hybridization has received far less. As a first step to addressing and vocalizations (Andersson 1994). Along with divergence in ago- this gap, we need to compare the evolution of competitive traits and nistic signals, the visual and auditory sensory systems that receive recognition in females to those of males, and predict the potential and recognize these signals may also diverge between heterospecific outcomes for hybridization in secondary contact. Future work competitors (Peiman and Robinson 2010; Pfennig and Pfennig should also focus on the role of male mate choice in speciation, but 2012; Okamoto and Grether 2013). Because these sexual traits are the current review will focus on comparing interspecific male–male often used both to attract mates as well as to compete for mating and female–female competition. resources (Berglund et al. 1996), their divergence between species Here, I examine the role that interspecific reproductive competi- can have consequences for reproductive isolation. For instance, tion plays in hybridization, specifically between closely related line- character divergence that reduces interspecific interactions will limit ages (species, subspecies, and divergent populations) in secondary gene flow between species. Below I describe patterns of divergence contact when reproductive isolation is incomplete. Other reviews in competitive traits and recognition resulting from interspecific have focused on the diversifying role of male–male competition in interactions, and explore how this divergence can promote repro- promoting speciation (e.g., Qvarnstro ¨ m et al. 2012), but here I ductive isolation via reproductive exclusion and sexual conflict. expand this perspective to improve our understanding of both male– male and female–female competition and their evolutionary out- Character displacement: ecological, reproductive, and comes in secondary contact, which can either facilitate or impede reproductive isolation (see Figure 1, conceptual framework). agonistic I review the empirical and theoretical evidence supporting evolution- Character shifts in competitive traits and competitor recognition ary scenarios in which 1) competition promotes reproductive could take place due to different sexual, social, and ecological Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 78 Current Zoology, 2018, Vol. 64, No. 1 Figure 2. Females of 2 polyandrous, sex-role reversed shorebird species that hybridize in Panama show competitive asymmetries in morphology (left panel) and aggressive behavior (middle panel). J. spinosa females (right panel top) have larger body mass, longer wing spurs used for fighting, and are more aggressive than J. jacana females (right panel bottom), which may explain the asymmetric introgression of mtDNA in the hybrid zone. Figure adapted from Lipshutz (2017). Illustrations by Stephanie McClelland. selection pressures on each lineage evolving independently in allopa- and Pfennig 2010) which could initiate the speciation process (Schluter 2001; Pfennig and Pfennig 2009). tric isolation (Rice and Pfennig 2007), or to selection pressures For closely related species in secondary contact that have not occurring from contact with a heterospecific in sympatry (Grether diverged in their secondary sexual characteristics, similar mating sig- et al. 2009; Pfennig and Pfennig 2009). Three main processes of trait nals can result in species recognition errors and heterospecific mat- shifts due to interspecific interactions are ecological character dis- ing (Gro ¨ ning and Hochkirch 2008), which can in turn lead to the placement (ECD), reproductive character displacement (RCD), and evolution of RCD. RCD is a process that selects for greater sexual ACD, and they can result in either divergence or convergence in trait divergence and/or species discrimination in sympatry compared sympatry (Grant 1972). Competitive ecological interactions in sec- with allopatry, and can be indicative of the reinforcement process. ondary contact have been widely explored (reviewed in Pfennig and Much empirical and theoretical research has investigated how selec- Pfennig 2012; Weber and Strauss 2016). ECD is a process that pro- tion resulting from mate misrecognition and maladaptive hybridiza- duces greater shifts in ecological niches of species in sympatry than tion can drive divergence in mating signals and/or preferences in allopatry. ECD can arise when disruptive selection causes coexist- (Ptacek 2000; Coyne and Orr 2004; Pfennig and Pfennig 2009). ing species to diverge in their ecological niches, thereby reducing Like ECD, RCD can minimize interspecific contact, including repro- interspecific competition over a previously shared ecological ductive competition, if the traits that diverge also function in com- resource such as food (Brown and Wilson 1956; Losos et al. 2000; petitive interactions. Both ECD and RCD can influence each other, Schluter 2001). Both the resource utilized and trait associated with when species that compete for ecological resources also have similar the resource use are expected to change between the sympatric spe- sexual signals (reviewed in Pfennig and Pfennig 2009). Species dis- cies (e.g., prey type and jaw morphology in larval feeding of crimination between divergent signals can be tested using playback spadefoot toads Spea bombifrons and Spea multiplicata; Pfennig experiments, but their implementation and interpretations can be and Murphy 2003). Divergent ECD is predicted to promote repro- challenging for both male and female behavior (see Box 2). ductive isolation in several ways. The divergence in resource acquisi- Similarity in agonistic signals and competitor recognition can tion traits may reduce contact between species, and therefore also select for divergence or convergence between species in secon- impede interspecific gene flow (reviewed in Coyne and Orr 2004; dary contact, a process known as ACD. ACD evolves to reduce mal- Price 2008). Additionally, ecological divergence between sympatric adaptive interspecific competition over mating resources (Grether species can drive divergence in sexual signals, which can lead to et al. 2009), and can change the degree and/or outcome of interspe- reproductive isolation. In Darwin’s finches, for example, ecologi- cific interactions (Cody 1969; Grether et al. 2013). ACD has cally adaptive divergence in beak morphology is correlated with received relatively less attention than ECD and RCD, and fewer divergence in song, which is used in territorial defense and mate empirical cases are known. In the rubyspot damselfly genus choice (Huber and Podos 2006; Podos 2010). In the medium ground Hetaerina, males of some species use wing coloration for competitor finch Geospiza fortis, large and small beak morphs demonstrate recognition, and similarity in male wing coloration causes misidenti- positive assortative pairing, and gene flow is reduced between fication between species (Anderson and Grether 2010a). morphs (Huber et al. 2007). If offspring produced by matings Observational and experimental studies revealed that interspecific between these populations are intermediate in phenotype and there- territorial aggression in sympatry selected for shifts in agonistic sig- fore are competitively inferior in either niche, ecologically depend- nals (Anderson and Grether 2010a) and competitor recognition ent postmating isolation can evolve (Pfennig and Rice 2007; Rice (Anderson and Grether 2010b). Similar patterns have been found in Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Lipshutz  Female competition and speciation 79 Box 2. Interpretation of playback experiments To experimentally measure the extent of premating reproductive isolation between 2 species, studies compare mating signal divergence along with relative responses, that is, discrimination, between conspecific and heterospecific signals. For paired design playback studies in which males discriminate between conspecific and het- erospecific stimuli, this is interpreted as evidence for reproductive isolation because divergent mating signals would reduce heterospecific gene flow (Baker 2001; Slabbekoorn and Smith 2002; Podos 2010; Lipshutz et al. 2017). Males whose territorial signals are not recognized by neighboring heterospecifics will face difficulty establishing and defending their territories in sympatry (Searcy and Nowicki 2005), which could promote reproductive isolation if they are forced to set up territories elsewhere. Tests in sympatry often reveal that males do not dis- criminate between heterospecific and conspecific signals—this is interpreted as lack of a behavioral barrier, which could promote hybridization (Gee 2005; den Hartog et al. 2008). For the majority of playback studies it is common to test only 1 sex, males, and indirectly infer similar signal discrimination and/or preference by females. This practice is prevalent because it is easier to conduct male playback experiments than female preference experiments in many taxa. However, such an interpreta- Male white-crowned sparrow responding to simulated tion of discriminatory response is problematic, in that it assumes that the relative territorial intrusion during playback experiment. Photo salience of conspecific and heterospecific signals to an individual territory holder by Elizabeth P. Derryberry. is a suitable proxy for female discrimination and even female preference. While male signals can be important for both male–male competition and female choice, the 2 sexes may not have evolved the same dis- criminatory abilities, nor should we expect them to respond similarly to a potential heterospecific competitor versus a potential heter- ospecific mate. We should therefore be interested in the direct value of territorial playback experiments—for understanding species recognition in territorial defense, rather than indirectly interpreting tendency for reproductive isolation between males and females. To understand how male and female discrimination between conspecific and heterospecific sexual signals compare, we should explic- itly test responses in both males and females of the same species. One successful example of this is a recent study in the Ficedula fly- catchers, which found that females discriminate between conspecific and heterospecific sexual signals in sympatry, whereas males did not (Wheatcroft and Qvarnstro ¨ m 2017). Given that sexual signals are often multimodal (e.g., acoustic and visual) and multicompo- nent (e.g., multiple messages encoded) (Hebets and Papaj 2005), future work should also test the relative salience of specific compo- nents of signals for species recognition in males versus females. the auditory signal reception of dendrobatid frogs Allobates femora- ECD can be difficult and these processes may not be mutually exclu- lis (Ame ´ zquita et al. 2006) and the male nuptial color of three- sive (Grether et al. 2009; Okamoto and Grether 2013). For instance, spined sticklebacks (Gasterosteus aculeatus spp.) (Albert et al. character displacement in bill morphology, male song, and response 2007). One open question is whether the character shift is expected to song have been demonstrated between sympatric species of to occur more often for the competitively inferior species, due to African tinkerbirds Pogoniulus bilineatus and P. subsulphureus (Kirschel et al. 2009), but the mechanism driving character displace- selection for access to resources monopolized by the dominant ment is not known. Clear cases of ACD must demonstrate that species. Divergence in competitive signals also involved in mate recogni- divergence in male traits is due to competition over mating resour- tion can promote reproductive isolation if females discriminate ces, and not due to selection for species-specific mate recognition by between these species-specific competitive signals and prefer to mate females (Okamoto and Grether 2013), which has been shown in the Hetaerina damselflies (Drury and Grether 2014). The traditional with conspecifics (Okamoto and Grether 2013). In the hybrid zone perspectives of sexual selection emphasize RCD on male sexual between pied flycatchers Ficedula hypoleuca and collared flycatch- ers Ficedula albicollis, both ACD and RCD may explain a diver- traits and female recognition, and ACD on male agonistic traits and gence in male plumage in sympatry, which both reduces recognition (see Figure 1, pathway 1A of conceptual framework). An apparent knowledge gap is whether RCD can occur on female heterospecific aggression and heterospecific pairing. Brown morph sexual traits and male recognition, and ACD can occur for female F. hypoleuca males are found in sympatry with competitively domi- agonistic traits and competitor recognition. Evidence is likely to be nant and black F. albicollis, and they receive less interspecific aggres- found in systems where male exercise mate choice and females com- sion than F. hypoleuca black morphs (Sætre et al. 1993; Alatalo pete over shared mating resources. et al. 1994). Female F. hypoleuca prefer brown conspecifics in sym- patry with F. albicollis, but prefer black conspecifics in allopatry (Sætre et al. 1997; Sæther et al. 2007). Because the same traits are Competitive asymmetry and reproductive exclusion often used for species recognition by both potential competitors and Divergence in competitive morphology and behavior of lineages in mates (Berglund et al. 1996), disentangling ACD from RCD and allopatry can result in the superior competitive ability of one lineage Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 80 Current Zoology, 2018, Vol. 64, No. 1 over the other upon secondary contact. A recent review found that Interspecific intrasexual conflict most aggressive interactions between closely related bird species Agonistic interactions can occur not only between the same sex of different species (e.g., male–male and female–female interspecific were asymmetric (Martin et al. 2017). Competitive asymmetry that interactions), but also between males and females of different species reduces interactions between species can lead to reproductive isola- (e.g., female–male interspecific interactions). Female aggression tion. For instance, if one of the species is a superior competitor and resources are limited, the dominant species may displace the subor- against male heterospecifics can promote reproductive isolation. For example, females at risk of interspecific pairings between salmon dinate species via competitive exclusion (Gause 1934; Hardin and brown trout showed higher rates of aggression against hetero- 1960). The expectations for ecological competitive exclusion are specific males and reduced the number of eggs available for spawn- similar to those for reproductive exclusion, also known as sexual ing (Beall et al. 1997). In other cases, however, females are unable exclusion—when the dominance of one species in monopolizing ter- to exert conspecific mate choice, for example in insect and water- ritories and mates displaces the less competitive species and excludes fowl species where males force copulations (Mckinney et al. 1983; them from establishing residence in sympatry (Kuno 1992; Arnqvist and Rowe 2002). This antagonistic coevolution between Hochkirch et al. 2007; Gro ¨ ning and Hochkirch 2008). As the out- females and males is known as sexual conflict, when the 2 sexes come of both ecological competitive exclusion and reproductive have different evolutionary interests (Parker and Partridge 1998). exclusion is that the species cannot coexist (Pfennig and Pfennig Within species, sexual conflict can be a driver of speciation, and can 2012), local extinction that reduces interspecific interactions could promote rapid evolutionary divergence of reproductive traits promote reproductive isolation between populations. For example, (Arnqvist et al. 2000; Martin and Hosken 2003). For instance, sex- an experiment with Callosobruchus maculatus and C. chinensis ual conflict can result in antagonistic coevolution of genital mor- weevils demonstrated that indiscriminate male mating attempts phology as well as color signaling and perception, resulting in sexual toward heterospecifics, linked with intolerance by female C. macula- polymorphisms (Hosken and Stockley 2004; Brennan et al. 2010; tus females, resulted in reduced reproduction, population decline, Gavrilets 2014). Female Ischnura ramburii have evolved male visual and local extinction of C. maculatus (Kishi et al. 2009). The expan- mimicry to resist male harassment, which can promote mate recog- sion of a more dominant and/or invasive species’ range, exacerbated nition errors by males (Gering 2017). A color polymorphism in the by anthropogenic changes such as habitat modification and climate wing patterns of Colias butterflies allows females with the rare change, can accelerate the geographical displacement of a less domi- “alba” morph to avoid reproductive interference, as a means of nant species (Rhymer and Simberloff 1996; Krosby et al. 2015). resistance to interspecific male mating harassment (Nielsen and When the species co-occur throughout their distribution, or the Watt 2000). Female sexual polymorphisms due to variation in resist- more dominant species expands its range (Canestrelli et al. 2016), ance or toleration of unwanted mating could lead to speciation, but the less dominant species could become locally extinct (Duckworth this has largely been explored within a species (Svensson et al. 2008; Pfennig and Pfennig 2012). In a simulation study, the compet- 2009). Interspecific sexual conflict, between males and females of itive ability of a native plant species via faster pollen-tube growth different species, could occur if heterospecific mating promoted by rates and enhanced seedling competition was predicted to prevent indiscriminate males is opposed by female preference for conspe- the risk of extinction due to both natural hybridization with invad- cifics. There are several cases of forced copulations resulting in ing plant species and competition with hybrids and invasives (Wolf hybrids (Randler 2005; Rohwer et al. 2014) but it is unknown et al. 2001). Species that are already rare are more vulnerable to whether females have evolved postmating divergence in genital mor- extinction by hybridization (Levin et al. 1996). Reproductive exclu- phology or other traits to avoid coercive heterospecific mating. To sion is expected to promote reproductive isolation, but examples are what extent does interspecific sexual conflict, involving the opposi- limited. Evidence of this process is likely difficult to observe in tion of competition and mate choice, promote reproductive isolation nature because it does not leave a genetic trace, as is the case with between species? hybridization. The consequences of male–male competition for reproductive When Competition in Secondary Contact exclusion and reproductive isolation are likely to be similar in Facilitates Introgressive Hybridization female–female competition, if females of one species outcompete another for mating resources, for example territories for breeding. Reproductive competition between sympatric lineages can also pro- Female–female agonistic interactions that occur within species have mote hybridization, if interspecific interactions over shared mating been predicted to promote diversification and incipient speciation. resources occur and reproductive isolation is incomplete. The pre- Females of some haplochromine cichlid species with bright colora- vious section explained how divergence in competitive traits tion are territorial and aggressive, and use color as a cue in social between lineages could lead to reproductive exclusion, but competi- interactions (Seehausen et al. 1999). An experimental assay in the tive asymmetry can also facilitate a dominant lineage’s monopoliza- cichlid species Neochromis omnicaeruleus demonstrated that tion of breeding with both conspecific and heterospecific mates. females bias aggression toward females of their own color morph Some patterns indicating these processes include asymmetric intro- (Dijkstra et al. 2009). Neochromis omnicaeruleus exhibits mutual gression of genetic loci and phenotypic traits, as well as moving mate choice (Seehausen et al. 1999), and females compete for males hybrid zones. Hybridization itself can result in the superior competi- of the same morph. Furthermore, female coloration is associated tive ability of hybrids relative to their parental taxa, which can fur- with behavioral dominance among female morphs (Dijkstra et al. ther promote backcrossing. While one outcome of interspecific 2009). How competitive interactions between females of the same reproductive competition is divergence in sexual traits, competitive species compare to female competition between 2 species, and signals that facilitate territorial interactions can also converge whether both of these processes are expected to contribute to diver- between species, which can also promote hybridization. The major- sification and reproductive isolation, is an exciting avenue for future ity of evidence for these processes has been found between males of research. species that compete for mating resources, but recent evidence Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Lipshutz  Female competition and speciation 81 suggests that female–female competition can also promote females (Supriatna 1991; Bergman and Beehner 2003). Genetic pat- hybridization. terns of introgression for autosomal loci and mtDNA suggest that hybridization occurs between M. tonkeana males and M. maura females (Evans et al. 2001). Unidirectional introgression of mtDNA, Competitive asymmetry and directional hybridization autosomal loci, and/or phenotypic traits can be explained by sexual Competitive asymmetry can lead to asymmetric introgression,in selection, either due to the competitive dominance of 1 species, or to which loci and traits that confer a reproductive advantage and are inherited from a competitively superior parental species progress mate choice favoring 1 species. It can also be found between females into the hybrid zone farther than background neutral loci (Barton of a rare species and males of a common species in sympatry (Wirtz 1979; Pia ´ lek and Barton 1997). For example, an asymmetry in 1999). Patterns suggesting unidirectional hybridization can addi- male–male competition between 2 lineages of common wall lizards tionally be explained by the reduction in fitness from 1 cross type Podarcis muralis may be promoting directional hybridization due to deleterious epistatic interactions—so-called “Darwin’s (While et al. 2015). The lineages are divergent in competitive Corollary to Haldane’s Rule (Turelli and Moyle 2007). Studies test- morphology—males of the northern Italian subspecies Podarcis ing whether pre-mating behaviors can explain patterns of asymmet- muralis nigriventris have larger heads, stronger bite force, and ric introgression should also consider alternative, but not necessarily greater testes mass compared with the Western Europe subspecies mutually exclusive hypotheses of post-mating and postzygotic repro- Podarcis muralis brogniardii. Podarcis muralis nigriventris males ductive isolation (e.g., Carling and Brumfield 2008). For example, are more aggressive and dominant to P.m. brogniardii males in terri- unidirectional hybridization between 2 sunfish species Lepomis torial interactions, which allows them to monopolize high-quality macrochirus and Lepomis gibbosus was explained by both asym- territories and courtship of both conspecific and heterospecific metric conspecific sperm precedence and hybrid inviability of 1 cross females (MacGregor et al. 2017). Sexual traits associated with P.m. (Immler et al. 2011). nigriventris males, including head size and dorsal and ventral colora- Asymmetric introgression can also lead to a moving hybrid zone. tion, are introgressing into the hybrid zone (While et al. 2015). Moving hybrids zones can occur between sympatric species with Directional hybridization can occur particularly when male– asymmetric competitive interactions that result in the geographic male competition is a stronger determinant of mating than female and/or genetic displacement of the inferior competitor via hybridiza- mate preferences (e.g., Reichard et al. 2005). For example, in experi- tion. Especially when an aggressive phenotype is linked with greater mental secondary contact among Tropheus cichlid fish of different dispersal (Duckworth and Badyaev 2007; Canestrelli et al. 2016), color morphs, dominance of the red male morph interfered with range expansion of the superior competitor can cause a hybrid zone positive assortative mating preferences by females and promoted to move over time. In the Setophaga hybrid zone between hermit asymmetric hybridization (Sefc et al. 2015). When males of a domi- Setophaga occidentalis and Townsend’s S. townsendi warblers, nant lineage displace lower-ranked males of the subordinate lineage S. occidentalis are superior competitors over breeding territories and from breeding territories, their conspecific females are left with no mates, and hybrids are intermediate to parentals in aggression choice but to join the territory of a heterospecific in order to repro- (Pearson 2000; Owen-Ashley and Butler 2004). While hybridization duce (Wirtz 1999). However, particularly when hybridization is is restricted to narrow zones, S. townsendi mtDNA is found in a maladaptive, females could still exercise choice for conspecifics phenotypically pure S. occidentalis population (Krosby and Rohwer through extra-pair mating with nearby conspecific males. This hap- 2009), and a resampling of hybrid zone sites 10–20 years later indi- pens, for example, in fur seals that pursue extra-territory insemina- cated they have become more townsendi-like over time (Krosby and tions when their phenotype did not match that of territorial mates Rohwer 2010). This geographic replacement of the competitively (Goldsworthy et al. 1999). The outcomes of interspecific male–male inferior S. occidentalis (Krosby and Rohwer 2010) could ultimately competition for hybridization in the Podarcis wall lizards may be result in its extinction. Hybridization between species with asym- influenced by weak female preference as well as by male mate choice metric competitive abilities can have important conservation for conspecifics (Heathcote et al. 2016). Although P.m. nigriventris implications—resulting in the extirpation of the less competitive lin- males outcompete P.m. brogniardii males for mating opportunities eage through genetic or demographic swamping, but also facilitating in the hybrid zone, P.m. nigriventris males prefer to mate guard the genetic rescue (reviewed in Allendorf et al. 2001; Mooney and largest females, which are typically also P.m. nigriventris, thereby Cleland 2001; Todesco et al. 2016; vonHoldt et al. 2017). Female promoting assortative mating and reducing gene flow between the 2 choice in conjunction with male–male competition can also facilitate lineages (Heathcote et al. 2016). These examples demonstrate some hybrid zone movement. For example, females of both black-capped of the ways competition and mate choice can interact to promote (Poecile atricapillus) and Carolina (Poecile carolinensis) chickadees similar or opposing outcomes for hybridization. When possible, display mate choice for dominant males, which are typically P. caro- empirical studies on the behavioral mechanisms of hybridization linensis (Bronson et al. 2003). The dominance of P. carolinensis should investigate the contributions of both male and female behav- males over territories and mates can explain its northward range ior separately, to understand the interactions between competition expansion and the northern movement of the hybrid zone, but cli- and mate choice (Wong and Candolin 2005). mate change can also explain this movement (Taylor et al. 2014). Unidirectional hybridization resulting from competitive asymme- Because hybrid zone movement can be explained by many other tries can yield increased prevalence of 1 heterospecific cross—for drivers including mate choice, postzygotic genetic incompatibilities, example, mating between females of 1 species with males of the and environmental change (Buggs 2007), hypotheses for competi- competitively dominant species, but the reciprocal cross is rare. A tion as a driver of asymmetric introgression and hybrid zone move- pattern of mitochondrial DNA (mtDNA) of only 1 parental species ment should be explicitly tested, for example by comparing found in hybrids can suggest unidirectional hybridization. For exam- aggression to simulated territorial intrusion (e.g., Billerman and ple in hybridizing macaques, the Tonkean macaque (Macaca ton- keana) has more intense male–male competition for mates, and may Carling 2017; Lipshutz 2017). These are not mutually exclusive be outcompeting the Moor macaque (M. maura) for M. maura processes, however, as the presence of competitive asymmetries is a Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 82 Current Zoology, 2018, Vol. 64, No. 1 necessary but not sufficient demonstration that competition is a key hybridization—phenotypic hybrids only had J. spinosa mtDNA hap- driver of hybrid zone movement. lotypes, suggesting predominant crosses between J. spinosa females When mate choice is based on an evaluation of traits also and J. jacana males (Miller et al. 2014). Unidirectional introgression involved in competitive interactions, it can be difficult to disentangle of J. spinosa mtDNA across the hybrid zone may be explained by the effects of reproductive competition from mate choice on hybrid- interspecific female–female competition for mates, whereby ization (e.g., Mennill et al. 2002). In the golden-collared Manacus the larger body size, spur length, and higher aggression of female candei and white-collared Manacus vitellinus manakin hybrid zone, J. spinosa allow them to exclude female J. jacana from obtaining ter- male–male competition may be driving asymmetric introgression of ritories in mixed-species populations (Lipshutz 2017). While inter- gold plumage across the hybrid zone, as M. candei males are more specific female–female competition over territories and mates may aggressive than M. vitellinus males and plumage color is associated be more likely to influence hybridization outcomes in species with with aggression (Mcdonald et al. 2001). However, this pattern may polyandrous mating systems, to what extent does female–female also be driven by female preference for M. candei males in mixed competition impact the likelihood of hybridization in other mating leks (Brumfield et al. 2001; Stein and Uy 2006). As with identifying systems? the drivers hybrid zone movement and distinguishing between ACD and RCD, we should test alternative hypothesis for competition ver- Adaptive introgression of competitive traits sus mate choice in driving asymmetric introgression, for example Heterospecific mating is often considered an accidental byproduct with experimental tests of interspecific competition (While et al. of incomplete species recognition, which reduces fitness due to 2015) and mate choice (Heathcote et al. 2016) in the same system. wasted time, energy, and gametes. However, hybridization can also be adaptive (Willis 2013). While this review has thus far examined Female–female competitive asymmetry how competition influences the likelihood for hybridization, hetero- Could competitive asymmetries between females of sympatric spe- typic mating can also increase competitive ability. For example, cies promote hybridization, in a similar fashion to males? Within a hybrid tadpoles between S. bombifrons and S. multiplicata develop species, competitive phenotypes in females can influence mating suc- more rapidly and are more likely to achieve metamorphosis than S. cess. In the social lizard Egernia whitii, more aggressive females bombifrons tadpoles, which can facilitate survival in ephemeral have more extra-pair offspring (While et al. 2009). Between species, ponds. Spea bombifrons females become more likely to hybridize female–female competition for mating opportunities is less under- with S. multiplicata males when water levels are low (Pfennig et al. stood. Interspecific female–female competition for male sperm has 2002; Pfennig and Rice 2007), suggesting that unidirectional hybrid- been documented between mollies Poecilia latipinna and a unisexual ization is adaptive in certain environments. Inheritance of competi- species of hybrid origin Poecilia formosa from crossings of P. lati- tive traits from the dominant parental lineage could also provide pinna and P. mexicana (Riesch et al. 2008). In order to trigger hybrids with a selective advantage over the competitively inferior embryogenesis, hybrid female P. formosa require sperm from either lineage. parental species, known as sexual parasitism (Schlupp 2009). While Heterosis, or hybrid vigor, occurs when hybrids are competi- P. formosa was more aggressive toward P. latipinna than vice versa, tively superior to their parental species (Birchler 2003), and can also it is unknown what role interspecific female competition plays in result in reduction or extinction of parental species. A pattern of maintaining the Poecilia species complex (Makowicz and Schlupp hybrids outcompeting their parental taxa is particularly associated 2015). That aggressive females are more promiscuous could influ- with invasive species (Py sek et al. 2003; Suehs et al. 2004). Hybrids ence their likelihood of mating with a heterospecific. Costs of heter- between 2 morphs of invasive Thiarid snail Melanoides tuberculata ospecific mating may be higher in females because of gametic and are produced sexually, but the hybrid morphs reproduce asexually parental investment (Wirtz 1999), but these costs may be lowered if via apomictic parthenogenesis (Samadi et al. 1999). Hybrid morphs females mate with multiple males. For example, one experimental are superior competitors to their parental taxa in natural habitats by study of Gryllus crickets demonstrated that mating barriers between having greater colonization ability and larger bodied offspring hybridizing species were weakest among females of the more poly- (Facon et al. 2005, 2008), and are mostly female (B. Facon, personal androus species (Veen et al. 2011). Females of the more polyandrous communication). There are several other examples where hybrids species, Gryllus bimaculatus discriminated less and mated more are superior competitors to parentals, for example in several crosses with heterospecific males. Therefore, we might expect females in of Darwin’s finches (Geospiza sp.) where hybrids have higher breed- polyandrous systems, especially those that compete for mates, to ing success (Grant and Grant 1992), and in hybrid gulls between Larus occidentalis and Larus glaucescens because of the combina- mate less discriminately than females in monogamous mating systems. tion of adaptive traits from parentals in an intermediate environ- Interspecific female–female competition in polyandrous mating ment (Good et al. 2000). Heterosis can also be a mechanism of systems, in which females compete for access to male mates, may be speciation if hybrids are reproductively isolated from their parental analogous to interspecific male–male competition. Because polyan- species. This can occur due to an inversion (Lowry and Willis 2010) drous females have multiple opportunities to breed, they may face or allopolyploidy (Comai 2005; Van de Peer et al. 2017), which is lower costs of heterospecific mating (Arnqvist et al. 2000). One more common for plants (Abbott et al. 2016) but also documented example is a hybrid zone between 2 polyandrous sex-role reversed in animals (Mable et al. 2011). Heterosis can also be associated with bird species, the wattled jacana Jacana jacana and the Northern a hybrid swarm because of the production of highly fit recombinant jacana Jacana spinosa (Miller et al. 2014; Figure 2). Female jacanas genotypes that erode parental genetic boundaries, for example in the of both species control access to mates by competing for territories copepod Tigriopus californicus (Hwang et al. 2011). In a hybrid encompassing a harem of males. Females are under stronger selec- swarm between Pecos pupfish (Cyprinodon pecosensis) and sheeps- tion for increased aggression and larger body size and spur weap- head minnow (C. variegatus), male–male competition is asymmetric onry, while males provide parental care (Jenni and Collier 1972; (Rosenfield and Kodric-Brown 2003). Male C. variegatus as well as Emlen and Wrege 2004a, 2004b). There is an asymmetry of F1 hybrids outcompeted male C. pecosensis for mates, suggesting Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Lipshutz  Female competition and speciation 83 hybrid vigor can promote extensive hybridization via competition. When females compete, is the evolution of competitive signals The adaptiveness of hybridization is based on the fitness of hybrids and recognition in females predicted to have similar outcomes for hybridization as those found in males? For species in which both relative to parental species, and this can be challenging to quantify males and females defend territories, we might expect the sexes to but useful for understanding how and why hybridization occurs. For have similar patterns of agonistic signal evolution. This can depend species in which hybridization is maladaptive, introgression of traits on whether the agonistic signals are also used in mate choice deci- that increase a hybrid individual’s competitive advantage may be sions for either sex (Wong and Candolin 2005). If male signals are undermined by lower survival due to incompatibilities for other loci. under selection in both choice and competition contexts, but female signals are not, then we might predict fewer constraints on the direc- Convergence in agonistic signals tion of evolution of female signals. In a scenario where convergence Although studies of interspecific competition typically focus on the in agonistic signals facilitates interspecific territorial interactions, evolution of trait divergence, competition over shared mating female agonistic signals may be more likely to converge in secondary resources can actually drive convergence in signals and signal recog- contact, whereas male signals may be expected to be more divergent nition involved in territorial defense to facilitate aggressive interac- to facilitate species recognition. However, if males use female ago- tions between heterospecifics (Cody 1969; Tobias and Seddon 2009; nistic signals to select a mate, then we should see similar patterns of Vokurkova ´ et al. 2013). Convergence in competitive signals has convergence in the agonistic signals of both sexes. In a sympatric been found within an avian radiation of ovenbirds (Furnariidae), species pair of Neotropical antbirds, Hypocnemis peruviana and H. whereby species coexistence predicted convergence in male song subflava, both males and females sing to defend territories, and (Tobias et al. 2013). Agonistic signal convergence could evolve due interspecific aggression is intense (Tobias and Seddon 2009). Both to direct interactions in competing over shared ecological or mating male and female songs converged in sympatry, likely due to social resources (Grether et al. 2009; Dufour et al. 2015; Laiolo 2017), or selection, which includes competition for ecological resources in because of acoustic adaptation to a shared environment (e.g., addition to mate acquisition (West-Eberhard 1983; Tobias et al. Cardoso and Price 2010). Convergence in competitive signals can 2012). Interestingly, female songs showed greater similarity in also occur due to hybridization (Grant et al. 2004; Secondi et al. acoustic structure in sympatry than male songs, potentially because 2011), either if signals are genetically determined and are intermedi- of selection on male song for females to discriminate between con- ate to parental signals (e.g., de Kort et al. 2002; Gee 2005), or due specifics and heterospecifics and avoid hybridization (Searcy and to learning if offspring imprint on the songs of heterospecifics (e.g., Brenowitz 1988). Although hybridization does not occur between Secondi et al. 2003; Haavie et al. 2004). these species, this study can provide insight for female versus male While signal convergence between sympatric species is expected agonistic signal evolution resulting from interspecific interactions. to facilitate competitor recognition and interspecific territoriality Female territorial signals may be less constrained by conspecific (Grether et al. 2009), it could also increase the probability of hetero- mate recognition than male signals, and can therefore evolve more specific pairing and hybridization, especially in species that use the strongly in response to interspecific competition than male signals. same signals to both defend territories and attract a mate (Berglund Currently, there are no known studies of ACD in female competitive et al. 1996; Wong and Candolin 2005). For example, in sympatric traits and/or species recognition. Are female agonistic signals more Ficedula flycatchers, the pied flycatcher F. hypoleuca song converges likely to converge or diverge in secondary contact with closely with the song of the more dominant collared flycatcher (F. albicollis) related competitors, in comparison to male signals? by incorporating learned parts of its song repertoire (Haavie et al. 2004). This mixed singing leads to heterospecific pairing and increases the likelihood of hybridization (Qvarnstro ¨ m et al. 2006). Conclusions and Next Steps However, the convergence of male song and song discrimination to This review has examined the processes by which reproductive com- facilitate territorial competition is opposed by stricter female choice petition between species in secondary contact promotes reproductive in sympatry (Wheatcroft and Qvarnstro ¨ m 2017). These findings, isolation versus hybridization. When possible, I have compared the that divergence in species recognition can evolve in females along evidence for male–male competition to that of female–female com- with convergence in male sexual signals, provide a more inclusive petition, but thus far both theoretical and empirical studies are rare understanding of reproductive isolation in the flycatcher system. for female competition. Interspecific competition that promotes the This study adds to an emerging understanding that signal discrimi- divergence of sexual traits and/or recognition between species via nation may diverge between the sexes, based on different selective character displacement, as well interspecific interactions that result pressures of mate and competitor recognition. In another example, a in reproductive exclusion, can promote reproductive isolation study of 2 sympatric Hypocnemis antbird species found that females (Figure 1: Conceptual framework). While evidence for ECD, RCD, discriminate between conspecific and heterospecific males in sympa- and ACD includes the involvement of both males and females, try, despite convergence in male song (Seddon and Tobias 2010). reproductive exclusion has only been documented in males. Concerning interspecific communication in secondary contact, the Competition between species in secondary contact can also promote evolution of signal recognition is expected to facilitate competition hybridization, for instance when a dominant species monopolizes over a shared mating resource in males and to avoid maladaptive mating resources, sometimes leading to asymmetric introgression. hybridization in females. Both convergent and divergent character Convergence in sexual traits and recognition due to competition can displacement on the same sexual signals and their recognition can also increase the likelihood for hybridization if the same traits are therefore have opposing outcomes for reproductive isolation in involved in mate choice. Hybridization itself can cause the introgres- males versus females (see Box 2). When this tension exists, the selec- sion of competitive traits, which can facilitate further hybridization. tive pressures resulting divergent RCD dominate those favoring con- Evidence for the involvement of both males and females has been vergent ACD, due to the costs of reproduction outweighing the costs found in all of these processes, though the male examples are strik- of aggression (Okamoto and Grether 2013). ingly more prevalent. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 84 Current Zoology, 2018, Vol. 64, No. 1 Allender CJ, Seehausen O, Knight ME, Turner GF, Maclean N, 2003. Our understanding of how male–male competition influences Divergent selection during speciation of Lake Malawi cichlid fishes inferred hybridization outcomes is solidifying. Still, the predictions for how from parallel radiations in nuptial coloration. Proc Natl Acad Sci USA 100: female choice can reinforce reproductive isolation via selection for 14074–14079. male trait divergence are more clearly developed than the predic- Allendorf FW, Leary RF, Spruell P, Wenburg JK, 2001. The problems with tions for how male–male competition can influence hybridization. hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622. This is paradoxical, because most empirical studies examining Alatalo RV, Gustafsson L, Lundberg A, 1994. Male coloration and species rec- whether sexual trait divergence promotes reproductive isolation are ognition in sympatric flycatchers. Proc R Soc Lond B 256:113–118. carried out by testing male–male interactions and not male–female Ame ´ zquita A, Ho ¨ dl W, Lima AP, Castellanos L, Erdtmann L et al., 2006. interactions, due to logistical challenges (see Box 2: Playback Masking interference and the evolution of the acoustic communication sys- tem in the Amazonian dendrobatid frog Allobates Femoralis. Evolution 60: experiments). Only by testing both competition and mate choice 1874–1887. within the same study systems can we disentangle whether the mat- Anderson CN, Grether GF, 2010a. Character displacement in the fighting col- ing behavior of males and females impedes or promotes the evolu- ours of Hetaerina damselflies. Proc R Soc B Biol Sci 277:3669–3675. tion of reproductive isolation. Anderson CN, Grether GF, 2010b. Interspecific aggression and character dis- Does taking a non-traditional perspective change our under- placement of competitor recognition in Hetaerina damselflies. Proc R Soc B standing of how sexual selection impacts the process of reproductive Biol Sci 277:549–555. isolation? For those systems in which females of different species Andersson M, 1994. Sexual Selection. Princeton: Princeton University Press. compete for shared mating resources, the likelihood for female– Arbuthnott D, Crespi BJ, 2009. Courtship and mate discrimination within and female competition to promote reproductive isolation versus between species of Timema walking-sticks. Anim Behav 78:53–59. Arnqvist G, Edvardsson M, Friberg U, Nilsson T, 2000. Sexual conflict pro- facilitate hybridization depends on the cost of mating with a hetero- motes speciation in insects. Proc Natl Acad Sci USA 97:10460–10464. specific. Mating behavior is just one component of species interac- Arnqvist G, Rowe L, 2002. Antagonistic coevolution between the sexes in a tions that influences the potential for hybridization between lineages group of insects. Nature 415:787–789. in secondary contact, and the evolutionary context of interacting lin- Arnqvist G, Rowe L, 2005. Sexual Conflict. Princeton: Princeton University eages is important to consider. The outcomes for reproductive isola- Press. tion depend not only on interspecific competition and mate choice, Baker MC, 2001. Bird song research: the past 100 years. Bird Behav 14:3–50. but also the fitness costs to hybridization, which can be related to Baldassarre D, Webster M, 2013. Experimental evidence that extra-pair mat- the age of divergence between the interacting lineages and accumu- ing drives asymmetrical introgression of a sexual trait. Proc R Soc B Biol Sci 280:1–7. lation of genetic incompatibilities (Pfennig 1998; Ord et al. 2011; Barton NH, 1979. The dynamics of hybrid zones. Heredity 43:341–359. Drury et al. 2015). For instance, the accumulation of intrinsic Bateman AJ, 1948. Intra-sexual selection in Drosophila. Heredity 2:349–368. genetic incompatibility over time is likely to select for species recog- Beall E, Moran P, Pendas A, Izquierdo J, Garcia Vazquez E, 1997. nition traits to avoid heterospecific mating. As females typically Hybridization in natural populations of salmonids in South-West Europe have higher gametic and parental investment and fewer opportuni- and in an experimental channel. Bull Fr Peche Piscic 344:271–285. ties for multiple mating attempts, one prediction is that male compe- Berglund A, Bisazza A, Pilastro A, 1996. Armaments and ornaments: an evolu- tition is more likely to result in hybridization than female tionary explanation of traits of dual utility. Biol J Linn Soc 58:385–399. competition. Future empirical and theoretical work should explicitly Bergman TJ, Beehner JC, 2003. Hybrid zones and sexual selection: insights test this prediction on the outcome of intraspecific competition for from the Awash baboon hybrid zone (Papio hamadryas Anubis P. h. ham- adryas). In: Jones C, editor. Sexual Selection and Primates: New Insights hybridization in males versus females, in the context of the strength and Directions. Norman: American Society of Primatologists, 500–537. of intrinsic incompatibilities between sympatric lineages. Billerman SM, Carling MD, 2017. Differences in aggressive responses do not contribute to shifts in a sapsucker hybrid zone. Auk 134:202–214. Birchler JA, 2003. In search of the molecular basis of heterosis. Plant Cell Acknowledgments Online 15:2236–2239. Thanks to Ole Seehausen and his group at EAWAG and the Bonduriansky R, 2001. The evolution of male mate choice in insects: a synthe- University of Bern, including Ayana De Brito Martins, Joana Meier, sis of ideas and evidence. Biol Rev Camb Philos Soc 76: Florian Moser, Marcel Hasler, as well as K. Okamoto, Erik Enbody, S1464793101005693. Elizabeth Derryberry, special editor Robin Tinghitella, and three Brennan PLR, Clark CJ, Prum RO, 2010. Explosive eversion and functional morphology of the duck penis supports sexual conflict in waterfowl genita- anonymous reviewers for comments on the manuscript. lia. Proc R Soc B 277:1309–1314. Bronson CL, Grubb TC, Sattler GD, Braun MJ, 2003. Mate preference: a pos- sible causal mechanism for a moving hybrid zone. Anim Behav 65:489–500. Funding Brown W, Wilson EO, 1956. Character displacement. Syst Zool 5:49–64. S.E.L. was supported by a National Science Foundation (NSF) Graduate Brumfield RT, Jernigan RW, McDonald DB, 2001. Evolutionary implications Research Opportunities Worldwide (GROW) Fellowship in Switzerland and of divergent clines in an avian (Manacus: Aves) hybrid zone. Evolution 55: NSF Graduate Research Fellowship under Grant No. 1154145. Any opinion, 2070–2087. findings, and conclusions or recommendations expressed in this material are Buggs RJA, 2007. Empirical study of hybrid zone movement. Heredity 99: those of the author and do not necessarily reflect the views of the NSF. 301–312. Burdfield-Steel ER, Shuker DM, 2011. Reproductive interference. Curr Biol 21:R450–R451. References Cain KE, Ketterson ED, 2012. Competitive females are successful females; Abbott RJ, Barton NH, Good JM, 2016. Genomics of hybridization and its phenotype, mechanism and selection in a common songbird. Behav Ecol evolutionary consequences. Mol Ecol 25:2325–2332. Sociobiol 66:241–252. Albert AYK, Millar NP, Schluter D, 2007. Character displacement of male Canestrelli D, Porretta D, Lowe WH, Bisconti R, Carere C et al., 2016. The nuptial colour in threespine sticklebacks Gasterosteus aculeatus. Biol J Linn tangled evolutionary legacies of range expansion and hybridization. Trends Soc 91:37–48. Ecol Evol 31:677–688. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Lipshutz  Female competition and speciation 85 Carling MD, Brumfield RT, 2008. Haldane’s rule in an avian system: using Gause F, 1934. The struggle for existence. Yale J Biol Med 7:609. cline theory and divergence population genetics to test for differential intro- Gavrilets S, 2014. Is sexual conflict an “engine of speciation”? Cold Spring gression of mitochondrial, autosomal, and sex-linked loci across the Harb Perspect Biol 6:1–14. Passerina bunting hybrid zone. Evolution 62:2600–2615. Gee JM, 2005. No species barrier by call in an avian hybrid zone between Cardoso GC, TD Price, 2010. Community convergence in bird song. Evol California and Gambel’s quail Callipepla californica and C. gambelii. Biol J Ecol 24:447–461. Linn Soc 86:253–264. Clutton-Brock T, 2007. Sexual selection in males and females. Science 318: Gering EJ, 2017. Male-mimicking females increase male–male interactions, 1882–1885. and decrease male survival and condition in a female-polymorphic damsel- Cody L, 1969. Convergent characteristics in sympatric species: a possible rela- fly. Evolution 71:1390–1396. tion to interspecific competition and aggression. Condor 71:222–239. Gill SA, Alfson ED, Hau M, 2007. Context matters: female aggression and tes- Comai L, 2005. The advantages and disadvantages of being polyploid. Nat tosterone in a year-round territorial neotropical songbird Thryothorus leu- Rev Genet 6:836–846. cotis. Proc R Soc B 274:2187–2194. Cooney CR, Tobias JA, Weir JT, Botero CA, Seddon N, 2017. Sexual selec- Goldsworthy S, Boness D, Fleischer R, 1999. Mate choice among sympatric tion, speciation and constraints on geographical range overlap in birds. Ecol fur seals: female preference for conphenotypic males. Behav Ecol Sociobiol Lett 20:863–871. 45:253–267. Coyne JA, Orr AH, 2004. Speciation. Sunderland (MA): Sinauer Associates. Good TP, Ellis JC, Annett CA, Pierotti R, 2000. Bounded hybrid superiority in Coyne JA, Orr HA, 1989. Patterns of speciation in Drosophila. Evolution 43: an avian hybrid zone: effects of mate, diet, and habitat choice. Evolution 54: 362–381. 1774–1783. Darwin C, 1871. The Descent of Man and Selection in Relation to Sex. Grant PR, 1972. Convergent and divergent character displacement. Biol J London: Murray. Linn Soc 4:39–68. Desjardins JK, Hazelden MR, Van Der Kraak GJ, Balshine S, 2006. Male and Grant PR, Grant BR, 1992. Hybridization of bird species. Science 256: female cooperatively breeding fish provide support for the “Challenge 193–197. Hypothesis.” Behav Ecol 17:149–154. Grant PR, Grant BR, 1997. Genetics and the origin of bird species. Proc Natl Dijkstra PD, Van Dijk S, Groothuis TGG, Pierotti MER, Seehausen O, 2009. Acad Sci USA 94:7768–7775. Behavioral dominance between female color morphs of a Lake Victoria Grant PR, Grant BR, Markert JA, Keller LF, Petren K, 2004. Convergent evo- cichlid fish. Behav Ecol 20:593–600. lution of Darwin’s finches caused by introgressive hybridization and selec- Dijkstra PD, Seehausen O, Pierotti MER, Groothuis TGG, 2007. Male–male tion. Evolution 58:1588–1599. competition and speciation: aggression bias towards differently coloured Grether GF, Anderson CN, Drury JP, Kirschel ANG, Losin N et al., 2013. The rivals varies between stages of speciation in a Lake Victoria cichlid species evolutionary consequences of interspecific aggression. Ann N Y Acad Sci complex. J Evol Biol 20:496–502. 1289:48–68. Doorn GSV, Dieckmann U, Weissing FJ, 2004. Sympatric speciation by sexual Grether GF, Losin N, Anderson CN, Okamoto K, 2009. The role of interspe- selection: a critical reevaluation. Am Nat 163:709–725. cific interference competition in character displacement and the evolution of Drury J, Clavel J, Manceau M, Morlon H, 2016. Estimating the effect of com- competitor recognition. Biol Rev 84:617–635. petition on trait evolution using maximum likelihood inference. Syst Biol Gro ¨ ning J, Hochkirch A, 2008. Reproductive interference between animal spe- 65:700–710. cies. Q Rev Biol 83:257–282. Drury JP, Grether GF, 2014. Interspecific aggression, not interspecific mating, Haavie J, Borge T, Bures S, Garamszegi LZ, Lampe HM et al., 2004. drives character displacement in the wing coloration of male rubyspot dam- Flycatcher song in allopatry and sympatry: convergence, divergence and selflies Hetaerina. Proc R Soc B 281:20141737. reinforcement. J Evol Biol 17:227–237. Drury JP, Okamoto KW, Anderson CN, Grether GF, 2015. Reproductive Hankison SJ, Morris MR, 2003. Avoiding a compromise between sexual selec- interference explains persistence of aggression between species. Proc R Soc tion and species recognition: female swordtail fish assess multiple B 282:20142256. species-specific cues. Behav Ecol 14:282–287. Duckworth RA, 2008. Adaptive dispersal strategies and the dynamics of a Hardin G, 1960. The competitive exclusion principle. Science 131: range expansion. Am Nat 172:S4–S17. 1292–1297. Duckworth RA, Badyaev AV, 2007. Coupling of dispersal and aggression den Hartog PM, Slabbekoorn H, ten Cate C, 2008. Male territorial vocaliza- facilitates the rapid range expansion of a passerine bird. Proc Natl Acad Sci tions and responses are decoupled in an avian hybrid zone. Philos Trans R USA 104:15017–15022. Soc B 363:2879–2889. Dufour CMS, Meynard C, Watson J, Rioux C, Benhamou S et al., 2015. Space Heathcote RJP, While GM, Macgregor HEA, Sciberras J, Leroy C et al., 2016. use variation in co-occurring sister species: response to environmental varia- Male behaviour drives assortative reproduction during the initial stage of tion or competition? PLoS ONE 10:1–15. secondary contact. J Evol Biol 29:1003–1015. Edward DA, Chapman T, 2011. The evolution and significance of male mate Hebets E, Papaj DR, 2005. Complex signal function: developing a framework choice. Trends Ecol Evol 26:647–654. of testable hypotheses complex signal function: developing a framework of Emlen ST, Oring LW, 1977. Ecology, sexual selection, and evolution of mat- testable hypotheses. Behav Ecol Sociobiol 57:197–214. ing systems. Science 197:215–223. Hochkirch A, Gro ¨ning J, Bu ¨ cker A, 2007. Sympatry with the devil: reproduc- Emlen ST, Wrege PH, 2004a. Division of labour in parental care behaviour of tive interference could hamper species coexistence. J Anim Ecol 76: a sex-role-reversed shorebird, the wattled jacana. Anim Behav 68:847–855. 633–642. Emlen ST, Wrege PH, 2004b. Size dimorphism, intrasexual competition, and Hosken D, Stockley P, 2004. Sexual selection and genital evolution. Trends sexual selection in wattled jacana Jacana jacana, a sex-role-reversed shore- Ecol Evol 19:87–93. bird in Panama. Auk 121:391–403. Huber SK, Leon LFD, Hendry AP, Bermingham E, Podos J, 2007. Evans BJ, Supriatna J, Melnick DJ, 2001. Hybridization and population genet- Reproductive isolation of sympatric morphs in a population of Darwin’s ics of two macaque species in Sulawesi, Indonesia. Evolution 55: 1686–1702. finches. Proc R Soc B 274:1709–1714. Facon B, Jarne P, Pointier JP, David P, 2005. Hybridization and invasiveness Huber SK, Podos J, 2006. Beak morphology and song features covary in a pop- ulation of Darwin’s finches Geospiza fortis. Biol J Linn Soc 88:489–498. in the freshwater snail Melanoides tuberculata: hybrid vigour is more impor- Hudson EJ, Price TD, 2014. Pervasive reinforcement and the role of sexual tant than increase in genetic variance. J Evol Biol 18:524–535. Facon B, Pointier JP, Jarne P, Sarda V, David P, 2008. High genetic variance in selection in biological speciation. J Hered 105:821–833. life-history strategies within invasive populations by way of multiple intro- Hwang AS, Northrup SL, Alexander JK, Vo KT, Edmands S, 2011. Long-term ductions. Curr Biol 18:363–367. experimental hybrid swarms between moderately incompatible Tigriopus Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 86 Current Zoology, 2018, Vol. 64, No. 1 californicus populations: hybrid inferiority in early generations yields to Mckinney F, Derrickson SR, Mineau P, 1983. Forced copulation in waterfowl. hybrid superiority in later generations. Conserv Genet 12:895–909. Behaviour 86:250–293. Immler S, Hamilton MB, Poslusny NJ, Birkhead TR, Epifanio JM, 2011. Mennill DJ, Ratcliffe LM, Boag PT, 2002. Female eavesdropping on male Post-mating reproductive barriers in two unidirectionally hybridizing sun- song contests in songbirds. Science 296:873. fish (Centrarchidae: Lepomis). J Evol Biol 24:111–120. Miller MJ, Lipshutz SE, Smith NG, Bermingham E, 2014. Genetic and pheno- Irwin DE, Price TD, 1999. Sexual imprinting, learning and speciation. typic characterization of a hybrid zone between polyandrous Northern and Heredity 82:347–354. Wattled Jacanas in Western Panama. BMC Evol Biol 14:14. Jenni DA, Collier G, 1972. Polyandry in the American Jac¸ana. Auk 89: Mooney HA, Cleland EE, 2001. The evolutionary impact of invasive species. 743–765. Proc Natl Acad Sci USA 98:5446–5451. Kirschel ANG, Blumstein DT, Smith TB, 2009. Character displacement of Moore WS, 1987. Random mating in the Northern Flicker hybrid zone: impli- song and morphology in African tinkerbirds. Proc Natl Acad Sci USA 106: cations for the evolution of bright and contrasting plumage patterns in birds. 8256–8261. Evolution 41:539–546. Kishi S, Nishida T, Tsubaki Y, 2009. Reproductive interference determines per- Nandy B, Joshi A, Ali ZS, Sen S, Prasad NG, 2012. Degree of adaptive male mate sistence and exclusion in species interactions. J Anim Ecol 78:1043–1049. choice is positively correlated with female quality variance. Sci Rep 2:1–8. de Kort SR, den Hartog PM, ten Cate C, 2002. Diverge or merge? The effect of Nielsen MG, Watt WB, 2000. Interference competition and sexual selection sympatric occurrence on the territorial vocalizations of the vinaceous dove promote polymorphism in Colias (Lepidoptera, Pieridae). Funct Ecol 14: Streptopelia vinacea and the ring-necked dove S. capicola. J Avian Biol 33: 718–730. 150–158. Okamoto KW, Grether GF, 2013. The evolution of species recognition in com- Kozak GM, Reisland M, Boughmann JW, 2009. Sex differences in mate recog- petitive and mating contexts: the relative efficacy of alternative mechanisms nition and conspecific preference in species with mutual mate choice. of character displacement. Ecol Lett 16:670–678. Evolution 63:353–365. Ord TJ, King L, Young AR, 2011. Contrasting theory with the empirical data Kraaijeveld K, Kraaijeveld-Smit FJL, Komdeur J, 2007. The evolution of of species recognition. Evolution 65:2572–2591. mutual ornamentation. Anim Behav 74:657–677. Owen-Ashley NT, Butler LK, 2004. Androgens, interspecific competition and Krosby M, Rohwer S, 2009. A 2000 km genetic wake yields evidence for species replacement in hybridizing warblers. Proc R Soc B 271:S498–S500. northern glacial refugia and hybrid zone movement in a pair of songbirds. Panhuis TM, Butlin R, Zuk M, Tregenza T, 2001. Sexual selection and specia- Proc R Soc B 276:615–621. tion. Trends Ecol Evol 16:364–371. Krosby M, Rohwer S, 2010. Ongoing movement of the hermit warbler X Parker GA, Partridge L, 1998. Sexual conflict and speciation. Philos Trans R Townsend’s warbler hybrid zone. PLoS ONE 5:e14164. Soc B 353:261–274. Krosby M, Wilsey CB, McGuire JL, Duggan JM, Nogeire TM et al., 2015. Pearson SF, 2000. Behavioral asymmetries in a moving hybrid zone. Behav Climate-induced range overlap among closely related species. Nat Clim Ecol 11:84–92. Chang 5:883–886. Van de Peer Y, Mizrachi E, Marchal K, 2017. The evolutionary significance of Kuno E, 1992. Competitive exclusion through reproductive interference. Res polyploidy. Nat Rev Genet 8:206–216. Popul Ecol 34:275–284. Peiman KS, Robinson BW, 2010. Ecology and evolution of resource-related Laiolo P, 2017. Phenotypic similarity in sympatric crow species: evidence of heterospecific aggression. Q Rev Biol 85:133–158. social convergence? Evolution 71:1051–1060. Pfennig D, Murphy P, 2003. A test of alternative hypotheses for character Lande R, 1981. Models of speciation by sexual selection on polygenic traits. divergence between coexisting species. Ecology 84:1288–1297. Proc Natl Acad Sci USA 78:3721–3725. Pfennig DW, Pfennig KS, 2012. Evolution’s Wedge: Competition and the Levin DA, Francisco-Ortega J, Jansen RK, 1996. Hybridization and the extinc- Origins of Diversity. Oakland (CA): University of California Press. tion of rare plant species. Conserv Biol 10:10–16. Pfennig DW, Rice AM, 2007. An experimental test of character displacement’s Lipshutz SE, 2017. Divergent competitive phenotypes between females of two role in promoting postmating isolation between conspecific populations in sex-role reversed species. Behav Ecol Sociobiol 71:106. contrasting competitive environments. Evolution 61:2433–2443. Lipshutz SE, Overcast IA, Hickerson MJ, Brumfield RT, Derryberry EP, 2017. Pfennig KS, 1998. The evolution of mate choice and the potential for conflict Behavioral response to song and genetic divergence in two subspecies ofwhi- between species and mate-quality recognition. Proc R Soc B 265: te-crowned sparrows Zonotrichia leucophrys. Mol Ecol 26:3011–3027. 1743–1748. Losos JB, Creer D, Glossip D, Goellner R, Hampton A et al., 2000. Pfennig KS, Pfennig DW, 2009. Character displacement: ecological and repro- Evolutionary implications of phenotypic plasticity in the hindlimb of the liz- ductive responses to a common evolutionary problem. Q Rev Biol 84: ard Anolis sagrei. Evolution 54:301–305. 253–276. Lowry DB, Willis JH, 2010. A widespread chromosomal inversion polymor- Pfennig KS, Simovich MA, Merila ¨ J, 2002. Differential selection to avoid phism contributes to a major life-history transition, local adaptation, and hybridization in two toad species. Evolution 56:1840–1848. reproductive isolation. PLoS Biol 8:e1000500. Pia ´ lek J, Barton NH, 1997. The spread of an advantageous allele across a bar- Mable BK, Alexandrou MA, Taylor MI, 2011. Genome duplication in rier: the effects of random drift and selection against heterozygotes. amphibians and fish: an extended synthesis. J Zool 284:151–182. Genetics 145:493–504. MacGregor HEA, While GM, Barrett J, Pe ´ rez I de Lanuza G, Carazo P et al., Podos J, 2010. Acoustic discrimination of sympatric morphs in Darwin’s 2017. Experimental contact zones reveal causes and targets of sexual selec- finches: a behavioural mechanism for assortative mating? Philos Trans R tion in hybridizing lizards. Funct Ecol 31:742–752. Soc B 365:1031–1039. Makowicz AM, Schlupp I, 2015. Effects of female–female aggression in a sex- Price TD, 2008. Speciation in Birds. Greenwood Village: Roberts and ual/unisexual species complex. Ethology 121:903–914. Company Publishers. Mallet J, 2005. Hybridization as an invasion of the genome. Trends Ecol Evol Ptacek M, 2000. The role of mating preferences in shaping interspecific diver- 20:229–237. gence in mating signals in vertebrates. Behav Process 51:111–134. Martin OY, Hosken DJ, 2003. The evolution of reproductive isolation Py sek P, Brock JH, Bı´mova ´ K, Manda ´ k B, Jaro sı´k V et al., 2003. Vegetative through sexual conflict. Nature 423:979–982. Martin PR, Freshwater C, Ghalambor CK, 2017. The outcomes of most regeneration in invasive Reynoutria (Polygonaceae) taxa: the determinant of invasibility at the genotype level. Am J Bot 90:1487–1495. aggressive interactions among closely related bird species are asymmetric. Qvarnstro ¨ m A, Haavie J, Saether S, Eriksson D, Pa ¨ rt T, 2006. Song similarity PeerJ 5:e2847. Mcdonald DB, Clay RP, Brumfield RT, Braun MJ, 2001. Sexual selection on predicts hybridization in flycatchers. J Evol Biol 19:1202–1209. plumage and behavior in an avian hybrid zone: experimental tests of Qvarnstro ¨ m A, Vallin N, Rudh A, 2012. The role of male contest competition male–male interactions. Evolution 55:1443–1451. over mates in speciation. Curr Zool 58:493–509. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Lipshutz  Female competition and speciation 87 Randler C, 2002. Avian hybridization, mixed pairing and female choice. Anim Seddon N, Tobias JA, 2010. Character displacement from the receiver’s per- Behav 63:103–119. spective: species and mate recognition despite convergent signals in subo- scine birds. Proc R Soc B 277:2475–2483. Randler C, 2005. Do forced extrapair copulations and interspecific brood Seehausen O, Van Alphen JJM, Lande R, 1999. Color polymorphism and sex amalgamation facilitate natural hybridisation in wildfowl? Behaviour 142: ratio distortion in a cichlid fish as an incipient stage in sympatric speciation 477–488. Reedy AM, Pope BD, Kiriazis NM, Giordano CL, Sams CL et al., 2017. by sexual selection. Ecol Lett 2:367–378. Seehausen O, Schluter D, 2004. Male–male competition and nuptial-colour Female anoles display less but attack more quickly than males in response to displacement as a diversifying force in Lake Victoria cichlid fishes. Proc R territorial intrusions. Behav Ecol 28:1323–1328. Soc B 271:1345–1353. Reichard M, Bryja J, Ondra ckova´M, Da ´ vidova ´ M, Kaniewska P et al., 2005. Sefc KM, Hermann CM, Steinwender B, Brindl H, Zimmermann H et al., Sexual selection for male dominance reduces opportunities for female mate 2015. Asymmetric dominance and asymmetric mate choice oppose premat- choice in the European bitterling Rhodeus sericeus. Mol Ecol 14:1533–1542. ing isolation after allopatric divergence. Ecol Evol 5:1549–1562. Rhymer JM, Simberloff D, 1996. Extinction by hybridization and introgres- Servedio M, Saether S, Saetre G, 2009. Reinforcement and learning. Evol Ecol sion. Annu Rev Ecol Syst 27:83–109. 23:109–123. Ribeiro JM, Spielman A, 1986. The satyr effect: a model predicting parapatry Servedio MR, 2007. Male versus female mate choice: sexual selection and the and species extinction. Am Nat 128:513–528. evolution of species recognition via reinforcement. Evolution 61: Rice AM, Pfennig DW, 2007. Character displacement: in situ evolution of 2772–2789. novel phenotypes or sorting of pre-existing variation? J Evol Biol 20: Servedio MR, Noor MAF, 2003. The role of reinforcement in speciation: 448–459. theory and data. Annu Rev Ecol Evol Syst 34:339–364. Rice AM, Pfennig DW, 2010. Does character displacement initiate speciation? Slabbekoorn H, Smith TB, 2002. Bird song, ecology and speciation. Philos Evidence of reduced gene flow between populations experiencing divergent Trans R Soc B 357:493–503. selection. J Evol Biol 23:854–865. Stein AC, Uy JAC, 2006. Unidirectional introgression of a sexually selected Riesch R, Schlupp I, Plath M, 2008. Female sperm limitation in natural popu- trait across an avian hybrid zone: a role for female choice? Evolution 60: lations of a sexual/asexual mating complex (Poecilia latipinna, Poecilia for- 1476–1485. mosa). Biol Lett 4:266–269. Stockley P, Campbell A, 2013. Female competition and aggression: interdisci- Ritchie MG, 2007. Sexual selection and speciation. Annu Rev Ecol Evol Syst plinary perspectives. Philos Trans R Soc B 368:20130073. 38:79–102. Suehs CM, Affre L, Me ´ dail F, 2004. Invasion dynamics of two alien Roberts NS, Mendelson TC, 2017. Male mate choice contributes to behaviou- Carpobrotus (Aizoaceae) taxa on a Mediterranean island: II. Reproductive ral isolation in sexually dimorphic fish with traditional sex roles. Anim strategies. Heredity 92:550–556. Behav 130:1–7. Supriatna J, 1991. Hybridization between Macaca maurus and M. tonkeana:a Rohwer S, Harris RB, Walsh HE, 2014. Rape and the prevalence of hybrids in test of species status using behavioral and morphogenetic analyses [Ph.D. broadly sympatric species: a case study using albatrosses. PeerJ 2:e409. dissertation]. Department of Anthropology, University of New Mexico. Rosenfield JA, Kodric-Brown A, 2003. Sexual selection promotes hybridiza- Svensson EI, Abbott JK, Gosden TP, Coreau A, 2009. Female polymorphisms, tion between Pecos pupfish, Cyprinodon pecosensis and sheepshead min- sexual conflict and limits to speciation processes in animals. Evol Ecol 23: now, C. variegatus. J Evol Biol 16:595–606. 93–108. Rosvall KA, 2011. Intrasexual competition in females: evidence for sexual Taylor SA, White TA, Hochachka WM, Ferretti V, Curry RL et al., 2014. selection? Behav Ecol 22:1131–1140. Climate-mediated movement of an avian hybrid zone. Curr Biol 24: Ryan MJ, Rand AS, 1993. Sexual selection and signal evolution: the ghost of 671–676. biases past. Philos Trans Biol Sci 340:187–195. Tobias JA, Cornwallis CK, Derryberry EP, Claramunt S, Brumfield RT et al., Sætre G-P, Kral M, Bicik V, 1993. Experimental evidence for interspecific 2013. Species coexistence and the dynamics of phenotypic evolution in female mimicry in sympatric Ficedula flycatchers. Evolution 47:939–945. adaptive radiation. Nature 506:359–363. Sætre G-P, Moum T, Bures S, Kral M, Adamjan M et al., 1997. A sexually Tobias JA, Montgomerie R, Lyon BE, 2012. The evolution of female orna- selected character displacement in flycatchers reinforces premating isola- ments and weaponry: social selection, sexual selection and ecological com- tion. Nature 387:589–592. petition. Philos Trans R Soc B 367:2274–2293. Sæther SA, Sætre G-P, Borge T, Wiley C, Svedin N et al., 2007. Sex chromoso- Tobias JA, Seddon N, 2009. Signal design and perception in hypocnemis ant- me-linked species recognition and evolution of reproductive isolation in fly- birds: evidence for convergent evolution via social selection. Evolution 63: catchers. Science 318:95–97. 3168–3189. Samadi S, Mava ´ rez J, Pointier JP, Delay B, Jarne P, 1999. Microsatellite and Todesco M, Pascual MA, Owens GL, Ostevik KL, Moyers BT et al., 2016. morphological analysis of population structure in the parthenogenetic fresh- Hybridization and extinction. Evol Appl 9:892–908. water snail Melanoides tuberculata: insights into the creation of clonal vari- Turelli M, Moyle LC, 2007. Asymmetric postmating isolation: Darwin’s cor- ability. Mol Ecol 8:1141–1153. ollary to Haldane’s rule. Genetics 176:1059–1088. Schlupp I, 2009. Chapter 5 Behavior of Fishes in the Sexual/Unisexual Mating Veen T, Faulks J, Rodrı´guez-Munoz ~ R, Tregenza T, 2011. Premating repro- System of the Amazon Molly Poecilia formosa. Advances in the Study of ductive barriers between hybridising cricket species differing in their degree Behavior 39:153–183. of polyandry. PLoS ONE 6:e19531. Schluter D, 2001. Ecology and the origin of species. Trends Ecol Evol 16: Vokurkova ´ J, Petruskova ´ T, Reifova ´ R, Kozman A, Mo rkovsk y L et al., 2013. 372–380. The causes and evolutionary consequences of mixed singing in two hybridiz- Searcy WA, Brenowitz EA, 1988. Sexual differences in species recognition of ing songbird species (Luscinia spp.). PLoS ONE 8:e60172. avian song. Nature 332:152–154. vonHoldt BM, Brzeski KE, Wilcove DS, Rutledge L, 2017. Redefining the role Searcy WA, Nowicki S, 2005. The Evolution of Animal Communication: of admixture and genomics in species conservation. Conserv Lett 0:1–16. Reliability and Deception in Signaling Systems. Princeton: Princeton Weber MG, Strauss SY, 2016. Coexistence in close relatives: beyond competi- University Press. tion and reproductive isolation in sister taxa. Annu Rev Ecol Evol Syst 47: Secondi J, Bordas P, Hipsley CA, Bensch S, 2011. Bilateral song convergence 359–381. in a passerine hybrid zone: Genetics contribute in one species only. Evol West-Eberhard MJ, 1983. Sexual selection, social competition, and speciation. Biol 38:441–452. Q Rev Biol 58:155–183. Secondi J, Bretagnolle V, Compagnon C, Faivre B, 2003. Species-specific song Wheatcroft D, Qvarnstro ¨ m A, 2017. Reproductive character displacement of convergence in a moving hybrid zone between two passerines. Biol J Linn female, but not male song discrimination in an avian hybrid zone. Evolution Soc 80:507–517. 71:1776–1786. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018 88 Current Zoology, 2018, Vol. 64, No. 1 While GM, Michaelides S, Heathcote RJP, Macgregor HEA, Zajac N et al., Wolf DE, Takebayashi N, Rieseberg LH, 2001. Predicting the risk of extinc- 2015. Sexual selection drives asymmetric introgression in wall lizards. Ecol tion through hybridization. Conserv Biol 15:1039–1053. Lett 18:1366–1375. Wong BBM, Candolin U, 2005. How is female mate choice affected by male While GM, Sinn DL, Wapstra E, 2009. Female aggression predicts mode of competition? Biol Rev 80:559. paternity acquisition in a social lizard. Proc R Soc B 276:2021–2029. Wong BBM, Fisher HS, Rosenthal GG, 2005. Species recognition by male Willis PM, 2013. Why do animals hybridize? Acta Ethol 16:127–134. swordtails via chemical cues. Behav Ecol 16:818–822. Wirtz P, 1999. Mother species–father species: unidirectional hybridization in Woodley S, Moore M, 1999. Female territorial aggression and steroid hor- animals with female choice. Anim Behav 58:1–12. mones in mountain spiny lizards. Anim Behav 57:1083–1089. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/75/4575131 by Ed 'DeepDyve' Gillespie user on 16 March 2018

Journal

Current ZoologyOxford University Press

Published: Feb 1, 2018

There are no references for this article.

You’re reading a free preview. Subscribe to read the entire article.


DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create lists to
organize your research

Export lists, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off