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 email@example.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. 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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. 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