The evolution of male preferences and of female ornaments in species with traditional sex roles (i.e., polygyny) have been highlighted as areas in need of more active research by an accumulation of recent ﬁndings. The theoretical literature on these topics is relatively small and has centered on the evolution of male choice. Mathematical models have emphasized that, under polygyny, the evolution of male preferences faces much greater competition costs than does the evolution of fe- male preferences. We discuss ways in which costly male choice can nonetheless evolve, via (1) dir- ect selection that favors preferences, primarily through mating with highly fecund females, (2) mechanisms that rely on indirect selection, which weakly counters competitive costs of male preferences, and (3) genetic constraints, primarily in the form of pleiotropy of male and female preferences and traits. We also review a variety of mathematical models that have elucidated how costs to male preferences can be avoided. Finally, we turn our attention to the relatively scant the- oretical literature on the effects of male mate choice on the evolution of female traits. We empha- size the ﬁnding that the presence of male preferences cannot be assumed to lead to the evolution of female ornaments during polygyny, and point out situations where models have elucidated ways in which female ornaments can nevertheless evolve. Key words: female ornaments, male mate preferences, mathematical models Introduction (Andersson 1994; Shuster and Wade 2003; Arnqvist and Rowe The phenomena of ornamentation in male animals and choosiness 2005; Rosenthal 2017). in female animals have received substantial attention from biologists In contrast, a literature on the evolution of male mate choice and since a burst of interest on the topic in the 1970s and 1980s. They female ornamentation has only been accumulating in recent decades. are now commonly understood within the context of sexual selec- The early research on male mate choice and female ornamentation tion; that is, female choice and male ornamentation often coexist in focused primarily on species with sex role reversal, in which context species where males with flashier ornaments that exploit female the phenomena can be generally understood as the inverse of the choice can increase their relative fitness. Although some questions traditional sexual selection scenario (e.g., Gwynne 1993; Jones et al. remain about the evolution of male ornaments and female choice 2000). However, reports from empiricists now indicate that male (e.g., whether good genes in males can maintain mate preferences in mate choice and female ornamentation among species with trad- females; see e.g., Adkins-Regan et al. 2013), a hefty body of itional sex roles are not nearly as rare as once believed (Amundsen both empirical and theoretical literature has now accumulated 2000; Bonduriansky 2001; Edward and Chapman 2011). [Note, we V C The Author(s) (2018). Published by Oxford University Press. 323 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 firstname.lastname@example.org Downloaded from https://academic.oup.com/cz/article-abstract/64/3/323/4975622 by Ed 'DeepDyve' Gillespie user on 21 June 2018 324 Current Zoology, 2018, Vol. 64, No. 3 use the term “traditional sex roles” to describe those species that, polygnous males. Male choice, when it occurs, is most often based while not always strictly polygynous, are not sex role reversed. on traits that correlate with high fertility in females (e.g., LeBas We recognize that this term carries some unfortunate colloquial con- et al. 2003; Griggio et al. 2005; Pizzolon et al. 2008), such as large notations (Ah-King and Ahnesjo ¨ 2013), but we opt to use it rather body size (e.g., Olsson 1993; Verrell 1995; Ptacek and Travis 1997; than introduce new and unfamiliar terminology.] Choosiness in Arntzen 1999; Werner and Lotem 2003; Wong and Jennions 2003; males and sexual signals in females have been reported in many taxa Herdman et al. 2004; Saeki et al. 2005; Byrne and Rice 2006; (e.g., insects, Hopkins et al. 2015; fishes, Amundsen and Forsgren Me ´ ndez-Janovitz and Macı ´as Garcia 2017; for reviews, see 2001; Massironi et al. 2005; Me ´ ndez-Janovitz and Macı ´as Garcia Andersson 1994, table 6A; Bonduriansky 2001). Male choice has 2017; lizards, Weiss 2006; Weiss et al. 2009; crustaceans, Baldwin also been found for other characteristics that represent a direct bene- and Johnsen 2012; primates, Huchard et al. 2009; Fitzpatrick et al. fit to the male, such as readiness to mate (e.g., Rowland et al. 2002), 2015). lack of infection (e.g., Gourbal and Gabrion 2004; Wittman and Furthermore, many of these empirical examples are of traits that Fedorka 2014), virginity (e.g., Bateman and Ferguson 2004; Carazo are female-specific [see Nordeide et al. (2013) for a review of mutu- et al. 2004; Gaskett et al. 2004; Martel et al. 2008; MacLeod and ally ornamented species]. That is, the ornaments that females of Andrade 2014), or other indicators of reproductive potential (e.g., many species exhibit are not simply muted versions of traits that are Craig et al. 2002; Orrell and Jenssen 2002; Ojanguren and found in conspecific males (although this also does occur, see Magurran 2004; Siefferman and Hill 2005; Simcox et al. 2005; below). The prevalence of this female-specific signaling in species Parga 2006; Fitzpatrick et al. 2015; Cole and Endler 2016). with polygynous mating systems is important because it demon- Likewise, the empirical literature suggests that common patterns strates that these ornaments are not explained simply by pleiotropy of female ornamentation differ in generalizable ways from the com- between male and female traits or by genetic correlations mon patterns of male ornamentation. The phrase “male ornament” (e.g., Lande 1980; Amundsen 2000) nor are they explained by sex- usually calls to mind outlandish traits like the peacock’s train, the ual selection under sex role reversal, where polygyny typically does dances of lekking birds, or the bright color patterns of some male not apply. In other words, the known natural history of male mate guppies. By comparison, the traits that have been reported as orna- choice and female ornaments so far suggests that they may arise ments for females—while still bearing the hallmarks of secondary from processes that are fundamentally different in some way from sexual characteristics—tend to be more subtle. For instance, no mat- the processes of sexual selection that give rise to female choice and ter how conspicuous the displays of exaggerated estrous swellings male-specific signals. by females of many species of Old World Monkeys, they pale in Indeed, the recent empirical consensus—that the distribution of comparison to the flamboyant colors displayed by males mandrills male mate choice and female ornamentation in polygynous species (Figure 1A). Likewise, female two-spotted gobies display an orange across the tree of life is not as limited as once thought—has spurred colored belly when they are receptive (Amundsen and Forsgren a developing body of theoretical literature as well, which we review 2001), but this coloration is muted relative to the flashy sexual sig- here. The bulk of this new theoretical work dissects the processes by nals commonly displayed by males of some fishes, like guppies which male choosiness might evolve under polygyny and tries to (Brooks et al. 2001)(Figure 1B). Finally, female-spotted plateau liz- understand the ways in which the constraints upon male mate choice ards display orange throat patches during the breeding season might differ from its female mate choice counterpart. A small num- (Weiss 2002, 2006), but are still drab overall when compared with ber of theoretical models have been developed that examine the evo- the bright colorations in males of many species (Figure 1C). Female lution of female ornamentation as well. Indeed, one way to organize traits also tend to by “dynamic.” In other words, they tend to appear our thinking on the topic is as follows. Most of the male mate choice only around breeding time and then disappear. Although this kind literature examines male mate choice as an outcome of selection; of dynamic intra-individual variation in expression is observed in these models investigate the evolutionary processes that produce males of many species with visual sexual signal (e.g., birds with and constrain the evolution of such a behavior among males. A few breeding plumage, seasonal antler growth in deer), it is also very models investigate male mate choice as a mechanism of selection; common for males to display their extravagance year round (the these models examine the potential for male mate choice to exert se- many species of birds, fishes, and lizards that maintain bright color- lection pressure on female traits. This distinction provides some- ation). In contrast, this dynamic pattern has been reported in almost thing of a scaffold for the present review. Note that although all species in which females display ornaments or visual sexual sig- “ornaments” might be viewed as a subset of “traits” (e.g., those that nals [but see bluethroats (Amundsen et al. 1997)]. These general pat- are more exaggerated and/or costly), for the purposes of our review, terns hold for fishes (Amundsen and Forsgren 2001; Massironi et al. the distinction is not necessary. Therefore, we use the terms “female 2005), lizards (LeBas and Marshall 2000; Weiss 2006; Calisi et al. ornament” and “female trait” interchangeably throughout. We turn 2008; Weiss et al. 2009), crabs (Takahashi and Watanabe 2011; first to a brief summary of the patterns that have been reported by Baldwin and Johnsen 2012), and primates (Huchard et al. 2009; the empirical and natural history literature. Fitzpatrick et al. 2014)(Figure 1). Natural History of Male Mate Choice and Direct Selection against the Evolution of Male Female Ornamentation Mate Choice A survey of the empirical literature reveals different patterns be- The empirical patterns of male mate choice summarized above tween male mate choice and female choice. While females in pol- (i.e., polygynous males rarely display preferences for traits that seem ygynous species commonly choose males on the basis of what to be “arbitrary”) are consistent with insights about the evolution- appear to be “arbitrary” traits (e.g., plumage characteristics or ary processes resulting in male mate choice derived from theoretical songs that bear no obvious relationship to the “quality” of the male; studies. Mathematical models demonstrate that, under polygyny, see Andersson 1994), this appears to be less predominant among direct selection will often emerge against male mate choice, such Downloaded from https://academic.oup.com/cz/article-abstract/64/3/323/4975622 by Ed 'DeepDyve' Gillespie user on 21 June 2018 Fitzpatrick and Servedio Male mate choice and female ornamentation 325 Figure 1. Comparison of some of the most extreme secondary sexual characters for males (left column) and females (right column) in 3 different taxa. (A)In primates, male mandrills have evolved dramatic coloration in their faces and haunches and some empirical research in a semi-natural population indicates that females prefer the more brightly colored males. In comparison, females in many species of cercopithecine primates (including the savannah baboons, pictured) have evolved exag- gerated estrous swellings that appear around the time of ovulation and then disappear, coming and going each time the female experiences a sexual cycle(Nunn 1999; Fitzpatrick 2014). (B) Many species of ﬁshes have evolved highly exaggerated coloration and courtship behavior, like the male guppy pictured here (Endler 1983). By comparison, the orange bellies that are displayed by female two-spotted gobies are more subdued and are only visible when the female is receptive (Amundsen and Forsgren 2001). (C) Finally, males in many species of lizards (e.g., collared lizards) display ornate color patterns. In those species in which females have evolved sexual signals (e.g., striped plateau lizards) the signals are muted, relative to the extreme colors seen in males of some species, and they only appear during the breeding season. Photocredits: (A) Male mandrill Mandrillus sphinx; Wikimedia commons (user: NicBar): female baboon Papio cynocephalus;CL Fitzpatrick. (B) Male guppy Poecilia wingei; Wikimedia commons (user Emilio17): female two-spotted goby Gobiusculus ﬂavescens; Trond Amundsen. (C) Male col- lared lizard Crotaphytus collaris; Wikimedia commons (user: L. Dakota): female striped plateau lizard Sceloporus virgatus; Stacey Weiss. that—all else being equal—it will be unlikely to evolve. A “null However, in the case of the more ornamented female, that mating model” (sensu, Prum 2010) of the evolution of male mate choice opportunity also exists within a more intense competitive environ- that presents this phenomenon in detail was developed by Servedio ment than the mating opportunity represented by the unornamented and Lande (2006). In that paper, a series of population genetic mod- female. This difference in the intensity of competition associated els examined the fate of an allele for male mate choice, expressed as with each female emerges because ornamented females will dispro- biased courtship toward one type of female over another. The most portionally receive courtship from other males in the population basic of these models examined the case where the female trait was with choice alleles, while still being courted proportional to their arbitrary, male preferences determined which females the male frequency by the males that mate at random; ornamented females thus end up receiving more courtship overall. The key point is this: would court, and females chose from among courting males. Servedio and Lande (2006) found that in this case, the allele for during strict polygyny, each female has equal mating success, re- male choice was always lost. gardless of her ornamentation. Thus, competition is greater for the This failure to maintain the male mate choice allele under these mating opportunity that the ornamented female represents, versus circumstances can be explained as follows: Imagine that 2 males, the equivalent mating opportunity that the unornamented female one with a “preference” allele and one with an allele for “no prefer- represents. This increased competition surrounding ornamented ence,” encounter both an ornamented and an unornamented female females creates direct selection against the preference allele because (Figure 2). Both females represent exactly 1 mating opportunity. males with the “preference” allele are overrepresented in the high Downloaded from https://academic.oup.com/cz/article-abstract/64/3/323/4975622 by Ed 'DeepDyve' Gillespie user on 21 June 2018 326 Current Zoology, 2018, Vol. 64, No. 3 Figure 2. Direct selection against a male choice allele emerges under polygyny in a “null model.” A male with a “preference” allele and a male with a “no prefer- ence” allele are faced with an ornamented and an unornamented female (center of each circle). Both males are assumed to have the same amount of energy to devote to courtship (denoted in the ﬁgure by 6 males, representing courting males, for males with both the “no preference,” “N,” and the “preference,” “P” alleles). The male with the “no preference” allele will distribute his courtship (the “N”s) randomly between the females. The male with the “preference” allele, however, will direct more courtship (the “P”s) to the ornamented female. The male with the “no preference” allele is overrepresented in courting the non-orna- mented female, and is most likely to obtain a mating there (3 Ns out of 4 courting males in the ﬁgure). The male with the “preference” allele is overrepresented in courting the ornamented female (5 Ps out of 8 courting males), but not to the same extent as the “no preference” male was in courting the plain female (3/ 4 ¼ 0.75> 5/8 ¼ 0.625). The male with the “preference” allele is thus at a competitive disadvantage due to his biased courtship, leading to direct selection against the “preference” allele. This may help to explain why highly ornamented females, such as the one in the ﬁgure, are rarely seen in nature. competition situation (the ornamented female), while males with the review models that make assumptions which preclude competition “no-preference” allele are overrepresented in the low competition costs of male preferences from emerging in the first place. Finally, situation (the unornamented female) (Figure 2). In this null model, a we discuss theoretical findings regarding the potential for male pref- erences to place sexual selection on female traits. male with the preference allele thus has a reduced chance of mating at all. In addition to the competition cost that emerges naturally from How Can Male Preferences Evolve If There Is the assumption of polygyny in the null model above, obstacles to the Direct Selection against Them? evolution of male preferences can arise from other causes. Several models simply assign competition costs (e.g., Fawcett and Johnstone Direct selection against male preferences that emerges from 2003; Courtiol et al. 2016, see additional discussion of these and increased competition, or other costs, can be countered in several other models directly including costs below). Other models suggest ways. The most effective of these possible foils for direct selection that male mate preferences are even less likely to evolve if males are against male preferences is opposing direct selection which favors faced with multiple mating opportunities sequentially, rather than male preferences. Male preference evolution due to such direct selec- simultaneously (e.g., Barry and Kokko 2010). This result is consist- tion is investigated by many models, as we discuss below. Less ef- ent with what has been established about sequential choice using a fective are processes that apply indirect selection which favors male model of female (rather than male) choice (Kokko and Ots 2006). preferences; in these scenarios, male preference alleles are statistical- That is, under sequential mate choice scenarios, a choosy individual ly correlated with alleles at other loci so that changes at loci other rejects a mating opportunity without knowing if another mate will than the preference locus increase the frequency of the preference al- be encountered. As a consequence of this feature of sequential lele as a correlated response. It is well known that indirect selection choice, the evolution of male preferences can be difficult even in sit- tends to be weaker than direct selection because it is mediated by the strength of imperfect genetic correlations (e.g., Kirkpatrick and uations where such preferences would otherwise be favored. In Barton 1997). Nevertheless, several proposals for how male choice Barry and Kokko’s (2010) model, for example, males could poten- tially avoid the very high costs of female cannibalism through exert- might evolve rely on such indirect selection. We conclude this sec- tion by a consideration of the effects of genetic constraints, mainly ing mate choice, yet in their sequential choice model such a due to pleiotropy between the sexes at trait and preference loci. preference does not always evolve. Whenever there is direct selection against male preference, the question arises of whether male preferences are able to evolve des- Opposing direct selection can favor male preferences pite this cost. Below, we first address 3 mechanisms, opposing direct By far the most common form of direct selection favoring male pref- selection, opposing indirect selection, and genetic constraint, that erences in mathematical models is fecundity selection. Because fe- can lead to the evolution of male preferences despite costs that arise cundity selection acts upon a mated pair, instead of upon one sex or either from the emergent competition in the null model or from the other, a male preference for females with high fecundity other forms of direct selection against male preferences. We then will lead to fecundity selection favoring the male preference. This Downloaded from https://academic.oup.com/cz/article-abstract/64/3/323/4975622 by Ed 'DeepDyve' Gillespie user on 21 June 2018 Fitzpatrick and Servedio Male mate choice and female ornamentation 327 selection happens because the male preference will cause high fe- and can thus provide a direct-selection counterweight to direct selec- cundity females to be disproportionately paired with males with the tion against male preferences. For instance, Kokko and Heubel (2011) preference allele, leading directly to increased reproductive success present a model that investigates the evolution of male preferences in for males carrying such a preference. Although fecundity selection an environment where males face the risk of being sexually parasi- thus applies only direct selection to male preferences, the distinction tized. This model is based on the Amazon molly system (Poecilia for- between direct and indirect selection in this context can be subtle; it mosa), in which females reproduce through gynogenesis; that is, depends on the association between the ornamented (high-fecundity) copulation with related species is required to trigger reproduction, but females and males with preferences (created by non-random mat- offspring are all female clones of their mothers because copulating ing), and we are trained to think of benefits arising from associations males do not contribute their genetic material to the zygotes (Hubbs between traits and preferences as indirect selection. In this case, the and Hubbs 1932; Schlupp 2010). Such males, therefore, experience a benefit to the preference allele does depend on non-random mating significant fitness cost as a result of mating with an Amazon molly with the trait that is an honest indicator of high fecundity (note that (but see Schlupp et al. 1994). Using individual-based simulations, the the indicator must be honest), and this does form a genetic correl- authors examine the likelihood that male preferences will evolve as a ation between the trait and preference in the mated pair, upon which function of the density of Amazon mollies. Not surprisingly, they find the benefit conferred to the preference allele rests. However, an indi- that male preferences are more likely to evolve when the density of vidual male obtains the fecundity benefit as a consequence of the ex- sexual parasites is high. The male preference evolution in this case can pression of his own preference, not due to the fact that he is likely to perhaps be framed as an exaggerated fecundity selection; indeed, the carry the preference allele because of the expression of the prefer- males who mate with Amazon mollies receive zero fecundity benefits. ence and trait in his parents. Another model in which direct fecundity-like benefits counterbalance Fecundity selection can thus be quite a strong direct force coun- the direct costs of male preferences is presented by Courtiol et al. tering direct selection against male preferences. However, a male (2016), using a game theoretical framework. In this case, the benefits preference for fecundity-indicator traits will only evolve when the are determined strictly by the environment and thus any possibility of fecundity advantage is high enough to compensate for the direct se- indirect benefits is eliminated. They find that the costs of prefer- lection against male preferences emerging from the null model or ences—modeled as a decrease in mating rate—can be counterbalanced other forms of costs. Indeed, critical parameters representing the by direct benefits under many conditions. strength of this fecundity advantage arise in many different models An interesting set of game-theoretical models examines not only of various scenarios of male choice; as such, fecundity selection is the effects of differences in female fecundity or reproductive matur- mentioned often throughout the remainder of this review. A simple ity on the evolution of male mate preferences, but also the effects of demonstration of the way in which fecundity selection can counter variation in male quality (Fawcett and Johnstone 2003; Ha ¨ rdling direct selection against male preferences was illustrated by Servedio et al. 2004; Ha ¨ rdling and Kokko 2005; Ha ¨ rdling et al., 2008; and Lande (2006), who added fecundity selection to the “null mod- Venner et al. 2010). Male quality in these sequential-choice models el” described above by assuming that the trait preferred by males is generally manifested as a male’s direct competitive ability in con- was an honest indicator of female fecundity. They determined a tests with other males to guard females [Fawcett and Johnstone threshold fecundity advantage above which male preferences would 2003; Ha ¨ rdling et al. 2004; Ha ¨ rdling and Kokko 2005; Venner et al. evolve, and below which the direct selection on preferences resulting 2010; although see Ha ¨ rdling et al. (2008) for a model where quality from fecundity selection was still too weak to counter the direct se- affects how quickly males can replenish sperm reserves]. These mod- lection against male preferences due to increased competition for els consider a situation with limited mating opportunities; males preferred females. Nakahashi (2008) expanded upon these ideas pair, are challenged, and potentially displaced during a period of using a quantitative genetic model very parallel to the null model of competition, gaining benefits from mating with whichever female Servedio and Lande (2006). He showed that when fitness due to fe- they are paired with after the competition phase ends. They find cundity was normally distributed around an optimum trait value, that choice can evolve in either high-quality males, low-quality the effects of fecundity selection on male preferences depend on the males, or both, depending on exact conditions. All of these models preference function. This preference function can take a much wider find some parameter ranges where both low- and high-quality males variety of forms when preferences are assumed to be continuous, as prefer more fecund females, as is expected because of the direct in the quantitative genetic framework, versus when they are discrete. benefit that such a preference can incur. Some models produce the Specifically, Nakahashi (2008) found (in his Model 2) that male similarly intuitive outcome in which only high-quality males express preferences for more fecund females can evolve when such preferen- a preference (or express a stronger preference; e.g., Fawcett and ces are unimodal (“absolute” or “relative,” see Lande 1981); they Johnstone 2003; Ha ¨ rdling and Kokko 2005). However, some sur- will then evolve to be proportional to female fertility (e.g., will be prising results also emerge, including a case in which only low-qual- centered around the mean of the female trait). They cannot evolve, ity males have a preference (e.g., Ha ¨ rdling et al. 2004; Ha ¨ rdling and however, if they are open-ended (or “psychophysical”), such that Kokko 2005), for example, when encounters are scarce and low- males prefer more extreme female traits which cannot match well quality males easily lose guarded mates at a high cost to themselves with the normally distributed fecundity benefits. Nakahashi (2008) (Ha ¨ rdling and Kokko 2005). One particularly interesting recurrent result from the family of further demonstrated that unimodal preferences can instead evolve to be directional, favoring a female trait value above the current trait game theoretical models described above is the emergence of as- mean, when the female trait in question is acted upon by viability as sortative mating, in which high-quality males prefer high-quality well as fecundity selection (his Model 3; but note the trait will not females, while low-quality males do not just opportunistically pair necessarily be under selection due to this preference. See section on with the remaining females [as in Rowell and Servedio (2009), the relationship between preferences and traits below). described below], but instead actively express a preference for low- Other direct selection forces can arise in models that, while not ex- quality females (Fawcett and Johnstone 2003; Ha ¨ rdling and Kokko plicitly fecundity selection, function in similar ways mathematically 2005; Ha ¨ rdling et al. 2008; Venner et al. 2010). This outcome, Downloaded from https://academic.oup.com/cz/article-abstract/64/3/323/4975622 by Ed 'DeepDyve' Gillespie user on 21 June 2018 328 Current Zoology, 2018, Vol. 64, No. 3 which has been termed “prudent choice” (Ha ¨ rdling and Kokko scenarios, the male preference allele that leads to reproductive isola- 2005) or “reversed male mate choice” (Venner et al. 2010), occurs tion in the focal population becomes correlated with both the trait because it may be too costly for a low-quality male to attempt to locus and the loci that are under selection against hybrids, causing pair with a high-quality female if he is likely to lose her to a high- indirect selection to favor the preference through multiple channels. quality male in a costly encounter (or, similarly, simply end up los- Male preferences were generally able to evolve under such selection, ing her late in a season and remaining unmated). although in some cases not as quickly as female preference would in Finally, another possible direct benefit to male preferences arises a parallel situation [Servedio 2007, see also Servedio and Dukas if females have a preference for males that court them more, pro- (2013) for a description of how within-generational learning would vided that preference is disproportionately large compared with the affect this process]. relative amount with which they are courted by each type of male (South et al. 2012). Returning to Figure 2, such a preference would Genetic constraint mean, for example, that un-ornamented females would be more Finally, it is possible that male preferences may evolve because of than 3/4 times as likely to mate with males without a preference al- genetic constraints that affect loci involved in preferences or traits. lele and, similarly, ornamented females would be more than 5/8 Early observations of female traits, for example, noted that they times as likely to mate with males with a preference. South et al. often seemed to reflect male traits expressed in that same species, (2012) found that male preferences are likely to evolve more easily if but in a more subdued manner (Darwin 1871; Amundsen 2000); females have a fixed strength of preference for a male that courts such an effect could potentially occur if traits were at least partially more and if the preferred female trait were more common. This re- pleiotropic (e.g., Lande 1980). Similarly, female preferences may sult suggests that the biology of the female response to male court- have pleiotropic expressions in males. Using population genetic ship may be an important factor in the evolution of male models, Servedio and Lande (2006) analyzed both of these cases. preferences. They first examined the pleiotropy of both trait and preference ex- pression across the sexes, such that male traits were weakly Opposing indirect selection can sometimes favor expressed in females and female preferences were weakly expressed male preferences in males. They found that male preferences could indeed evolve as a As stated above, indirect selection is expected to be less efficient pleiotropic expression of female preference, although the presence than direct selection at opposing direct competition costs that males of this pleiotropic effect reduced the parameter space in which fe- face if they bias their courtship toward certain females. This can be male preference could occur, indicating that the expression in males seen in the contrast between the version of the “null model” of was generally having an inhibitory effect. In the case in which only Servedio and Lande (2006) that includes fecundity selection, which trait expression was pleiotropic and there were separate loci for is a form of direct selection favoring males preferences (see above), male and female preferences, only slight increases in the frequency and an otherwise identical version that includes instead a direct via- of a male preference were found, and this occurred under restricted bility advantage to females with the trait (Servedio 2007). Viability conditions. While other types of genetic constraints on preferences selection on the trait acts only on females, not on the mated pair, and traits may be envisaged, to date this seems to be a restricted av- and so any advantage to the male preference allele is due to indirect enue for the evolution of male preference. rather than direct selection, as a result of the fact that females with the trait allele tend to also carry the preference allele. Servedio (2007) found that such a viability advantage to the trait is very inef- When Direct Selection against Male Preferences ficient at driving male preference evolution; it was found to move Is Absent the preference only slightly upward in frequency even when viability Perhaps the simplest way to prevent the occurrence of the direct se- selection was of a value to maximize preference evolution (paradox- lection against male preference that arises from the increased compe- ically, stronger viability selection favoring the trait does not always tition emergent in the null model is to violate the assumption of increase the equilibrium frequency of a preference allele, see strict polygyny, whereby in the null model females have equal mat- Servedio 2007). In a parallel quantitative genetic model where males ing success, regardless of their traits. There are several ways in prefer a high-viability female trait, Nakahashi (2008) found that which such an assumption can be violated, and not all of these will unimodal male preferences could not evolve, and while very strong remove direct selection against a male preference allele. open-ended male preferences could evolve the dynamics were quite Females may, for example, have higher mating success if they are unusual and not biologically likely (they were oscillatory with ever- courted more. If the greater mating success of preferred females is a increasing absolute values; his Model 1). function of the extra courtship that they receive, this can counter, or One situation in which indirect selection in favor of male prefer- in extreme cases remove, the competitive mating disadvantage that ences can be extremely strong is when female traits indicate species males with a preference are subjected to in the null model shown in identity. This was assessed in a model of the process of Figure 2. Nakahashi (2008), for example, directly considers the pos- reinforcement—the evolution of premating isolation due to selection sibility that females that are not courted by enough males can be against hybrids—by Servedio (2007). In this model, the female trait childless (his Model 4, note that preferred females also, independ- is locally adapted and 2 separate loci determine whether individuals ently, have higher fecundity in this model). This probability ranges are “purebreds” or hybrids, and hence selected against. Two types from all females mating to the chance of going unmated being pro- of male preferences were considered, one in which there are separate portional to the degree to which that type of female is preferred (his male preference loci and female trait loci (a “preference/trait” R ¼ 1, at which point male preferences have no cost). He finds that model), and the other which examines the evolution of an allele that causes a male to prefer a female that shares whatever trait he himself the evolution of strong male preferences can occur, but it requires a carries (a “matching” model; for a review of the difference between large chance of a female not mating. In some cases, when a female’s these types of mating models, see Kopp et al. 2018). In both of these chances of going unmated are relatively high, a runaway process can Downloaded from https://academic.oup.com/cz/article-abstract/64/3/323/4975622 by Ed 'DeepDyve' Gillespie user on 21 June 2018 Fitzpatrick and Servedio Male mate choice and female ornamentation 329 even occur, especially if males are of high quality (non-genetic qual- preference. This extra overall courtship of males with a preference ity is included in Nakahashi’s Model 5). Only when there is such a could, for example, allow them to compete equally for matings from runaway can the female trait evolve to be exaggerated beyond its fe- unornamented females while still being over-represented in their cundity optimum. If the mating success of a female is not propor- courtship toward ornamented females (e.g., Servedio and Lande tional to the courtship that she receives, but is instead a fixed benefit 2006); they are thus not at a competitive disadvantage with either of having the preferred trait, this is simply a biological reinterpret- type of female. To our knowledge, there are no empirical explora- ation of the same mathematical relationship that underlies preferen- tions of whether courtship would be expected to be equivalent in males with versus without a preference, although one could imagine ces for more fecund females. In this case the male competition cost is that a relationship between preferences and courtship ability or still present, but is simply countered by the direct selective benefit of resources for courtship might be realistic. Indeed, preferences have mating with a female that has a trait that indicates higher mating been shown to evolve in males with more resources or higher quality success (Servedio and Lande, 2006; the threshold fecundity benefit in several models (Ihara and Aoki 1999; Fawcett and Johnstone described above can be interpreted as a threshold of higher mating 2003; Ha ¨ rdling et al. 2004, 2008; Ha ¨ rdling and Kokko 2005; success in this scenario). Another extreme departure from strict polygyny is the case of Venner et al. 2010). Ihara and Aoki (1999), for example, consider monogamy, where both males and females have equal mating suc- male choice under polygyny when the ability of males to mate with cess. Logically, if monogamy occurs with an equal sex ratio at the the maximum number of females depends on whether the males time of mating, and all mates are of equal quality in terms of direct themselves are “resource rich” or “resource poor,” and resources af- fecundity benefits, there will be neither sexual selection nor fecund- fect the fecundity of the mated pair. They find that if resources are ity selection on either males or females. Models of this scenario that paternally inherited (their Model 4), resources become positively have explicitly considered male choice have, however, generally correlated with male preferences for an attractive but costly female included fecundity differences in either the male or female, as well as trait. This correlation provides indirect selection favoring a male other forms of selection. These models have found that male prefer- preference allele, as resource poor males who sometimes obtain no mate are likely to have no preference. ences can evolve relatively easily in portions of the parameter space Finally, males themselves may be behaviorally capable of elimi- (e.g., Ihara and Aoki 1999, models 1 and 2; Stern and Servedio nating the costs of high competition on preference alleles that 2017; see also the model of post-pairing male choice by Lyu et al. emerge in the null model above if they are aware of the competitive 2017). landscape and direct their courtship in a way to avoid high competi- However, it should be noted that in contrast to the case of mon- tion situations. Rowell and Servedio (2009) considered this situation ogamy with equal sex ratios, if there are more males than females by assuming that males can distribute their courtship following an some males will go without a mate and therefore direct selection ideal-free distribution where females are the limiting resource. They against male preferences will still emerge during monogamous mat- found that when males are capable of moving out of a high competi- ing. A similar effect can also occur when encounter rates between tion situation some degree of assortment generally results. Males the sexes are low, and choosy males risk not mating at all. Male that do not have preferences will tend to be the first to move out of choice can still evolve in such models, even with added competition situations of high competition, leaving ornamented females to males costs, but fecundity selection or another direct benefit of such a pref- with the preference and thus tending themselves to court unorna- erence is again generally required (e.g., see mate guarding models of mented females. This movement and assortment has the conse- “serial monogamy,” Fawcett and Johnstone 2003; Ha ¨ rdling et al. quence of removing the competitive disadvantage of males with the 2004, 2008; Ha ¨ rdling and Kokko 2005). Presumably, such benefits preference allele, and preferences can then be maintained poly- of choice would have to be stronger than in the case of equal sex morphically in the population. Preferences generally evolve only to ratios above, although we are not aware of a model that has low frequencies, however, under this mechanism. reported on an explicit comparison of these cases. Under certain specific assumptions, limited access to females can have a diametrically opposite effect to that described in the monog- The Relationship between Male Mate amy models directly above; it can lead to selection for, instead of Preferences and Female Traits against, male preferences. In moths, for example, male preferences for species-specific pheromone blends can determine the ability of Above, we have discussed the various models that provide explana- males to find females at all (Linn et al. 1997; Gould et al. 2010). In tions for the evolution of male preferences in contexts in which they such cases, males without a preference will be directly selected might not otherwise have been expected to evolve. We now turn our against because they do not approach females, and thus are not vis- attention to the handful of models that examine the potential for ible to females at the short range at which females make mating male mate choice to drive the evolution of ornamentation in females decisions. Several researchers recognized that male preferences in in polygynous mating systems. Although there are not very many such a case can be accurately represented mathematically as the theoretical models that investigate this potential evolutionary pro- equivalent of the male trait in a female-choice sexual selection model cess, the few that have been developed are important because, as we (because females are more likely to mate with males with a prefer- detail below, they challenge the conventional wisdom that empirical ence than one without), while female pheromones can likewise be evidence of male mate choice can be interpreted as evidence for se- represented by the female preference in a female-choice model lection on female traits. In fact, theoretical models suggest that al- (Phelan 1992; Butlin and Trickett 1997; Bengtsson and Lofstedt though male preferences may evolve in species with traditional sex 2007; Bergen et al. 2012). Thus, one can conclude that male prefer- roles, the potential for that behavior to function as a mechanism of ences can evolve in this scenario. selection, thereby driving the evolution of female traits, is highly The direct selection due to competition will be lessened, or even constrained. completely countered, if males that have a preference have more en- This point is demonstrated most explicitly by a recent model ergy available to put into courtship than males that have no published by the authors of this review (Fitzpatrick and Servedio Downloaded from https://academic.oup.com/cz/article-abstract/64/3/323/4975622 by Ed 'DeepDyve' Gillespie user on 21 June 2018 330 Current Zoology, 2018, Vol. 64, No. 3 2017), which demonstrates that—in polygynous mating systems— among non-human primates (Pagel 1994; Nakahashi 2016)—per- the potential for male mate choice to drive the evolution of a female haps because the exaggerated estrous swellings (“sexual swellings”) trait is not only limited, but is only possible under very circum- displayed by many species of primates are so commonly cited as an scribed conditions. We develop a population genetic model that, in example of sexual selection on female traits (e.g., see p. 201 in addition to trait and preference loci (expressed in females and males, Davies et al. 2012). Both models use a game theoretical framework. respectively), includes a “quality” locus expressed only in males. Consistent with the conditions necessary for the evolution of male Quality is modeled as a fecundity benefit to the mated pair such that preferences outlined above, both models assume that the female trait a female mated to a high-quality male produces more offspring. This (exaggerated swellings) indicates something that represents a fitness male quality locus allows the model to formalize the hypothesis benefit to males. It is well known that sexual swellings correspond that, even under polygyny, females might experience sexual selection with ovulation, to varying degrees across species (Nunn 1999; as a result of competition for mates of superior quality [see Alberts and Fitzpatrick 2012). Although Pagel (1994) is presented as Fitzpatrick (2015) for a review of the literature that invokes this a model that explains the evolution of exaggerated swellings in pri- common hypothesis]. The central parameter of interest in the model mates, the math of the model is primarily concerned with the evolu- is q, which allows for an interaction between the male quality and tion of preferences among males (see above) and female traits are preference loci so that when q> 1, males who have both high-qual- implicitly assumed to evolve due to the presence of male preferences. ity and the preference allele have higher mating success than they Nakahashi (2016) developed another, more detailed model, also would if the effects of each allele functioned independently. We using game theoretical techniques. However, the feature of female demonstrate that simply the presence of mate preferences among ornamentation represented by this model is a function of time rather males in combination with variation in quality is insufficient to than morphology; that is, the model asks about the conditions that cause the evolution of an allele for a costly female trait. The only favor a strategy in which females signal receptivity for longer than conditions under which the presence of male mate preferences have they are actually fertile (“exaggerated signal”) versus a strategy in a measurable impact on the evolution of the female trait are when: which females signal receptivity for fewer days than they are actual- (1) q> 1, which biases the mate pairings so that ornamented females ly fertile (“concealed ovulation”). The fitness benefit that females mate non-randomly with choosy, high-quality males; (2) orna- can receive under some conditions is modeled as a direct benefit: the mented females have a level of intrinsic fecundity that is large mitigation of infanticide risk by the confusion of paternity that enough to allow male preference evolution, but not so great that it occurs when females are not monopolized by the alpha male and swamps the fecundity benefit that females might experience by mat- can therefore mate with multiple males. Not surprisingly, he finds ing with a high-quality male. These conditions are not only quite cir- that an exaggerated signal in females (which can take 2 different cumscribed, but might or might not be biologically realistic. forms) can evolve when the costs of mounting the strategy are Furthermore, even when male preferences in combination with male smaller than the benefits obtained. It is interesting to note, however, quality can influence female trait evolution in this model, the effect that the exaggerated signal only evolves when the benefits only out- is weak. Thus, one conclusion from this model is that direct fecund- weigh the costs by a small amount. ity benefits delivered to females via male preferences are not a likely Female traits that exist in the context of male mate choice may, explanation for female trait evolution. as we have stressed above, often indicate high fecundity. One way in One scenario in which the concept that q> 1, as in Fitzpatrick which this association may occur is if males are attracted to females and Servedio (2017), might be realistic is laid out by Ihara and Aoki that have a trait that indicates that they are better resource competi- (1999). In order to draw this comparison, let us highlight the conse- tors (e.g., the “armament-ornament” hypothesis or a “dual-utility” quence of q> 1 that is important for female trait evolution; the ne- trait, see Berglund et al. 1996; Hunt et al. 2009). This process has cessary feature for male preferences in combination with male been invoked with respect to female ornamentation in a number of quality to drive the evolution of female traits is that females with the empirical studies (e.g., Griggio et al. 2010; Crowhurst et al. 2012) trait must be more likely to mate with the high-quality males. In the and its feasibility was demonstrated for male preferences and female models of sexual selection by male mate choice in human popula- traits in a population genetic model of monogamous populations by tions presented by Ihara and Aoki (1999), preferred female traits Stern and Servedio (2017). It is possible to interpret the assumption can evolve when resource-rich males are able to mate according to of high fecundity in females in polygyny models, such as those dis- their preferences because they pair before resource-poor males do. cussed elsewhere in this review, as due to the ability of the females That is, the model does not assume an association among males be- to gather more resources, and the preferred trait being an honest in- tween preferences and resources per se, but males with more resour- dicator of this ability. However, none of the models above explicitly ces are more able to mate according to their preferences. The model resource competition for a limited resource by females both females with the preferred trait thus end up mating non-randomly with and without a trait. with resource-rich males. These models are presented within the Finally, Lyu et al. (2017) present a model that examines the po- context of both monogamous mating systems and polygynous ones tential for post-mating male mate choice—expressed in the form of (with no discounting of resources per female for multiply-mated re- allocation of paternal care to the brood versus engaging in extra- source-rich males in the latter case). Male preference-mediated non- pair copulations—to shape female traits, envisaged in this model as a post-mating signal (e.g., egg color; Moreno and Osorno 2003; random mating (between resource-rich males and ornamented females) functions in both contexts to drive trait evolution in Soler et al. 2008). This 2 locus population genetic model indicates females. While mating priority is given to resource-rich males in that, provided the female trait elicits enough paternal care, it can many human cultures [which Ihara and Aoki (1999) explicitly mod- evolve despite a fecundity cost; direct fecundity costs of producing el], the extent to which biological analogs are found in non-human the preferred trait in these cases are offset by the fecundity benefit animals is an open empirical question. provided by the males through parental care. Due to tradeoffs that Two models have addressed the potential for male mate choice arise in this model, it can also yield cases of sexual conflict where to drive the evolution of exaggerated female traits specifically male preferences and female traits cycle evolutionarily. Downloaded from https://academic.oup.com/cz/article-abstract/64/3/323/4975622 by Ed 'DeepDyve' Gillespie user on 21 June 2018 Fitzpatrick and Servedio Male mate choice and female ornamentation 331 A central take home message from this review of the literature of specifically, be investigating the potential for “social selection” to be male mate choice and female sexual signals is that, although there is a common explanation for the patterns of female ornaments within a dearth of mathematical models that explicitly examine the poten- and across taxa. Indeed, we anticipate that these questions about so- tial for male mate choice to promote the evolution of sexual signals cial selection and female ornaments will produce an increasingly in females; this relationship is often assumed. Indeed, most models fruitful and vibrant area of future research. that include female traits simply assume that the trait is associated with high fecundity or is an indicator of some aspect of fertility, such that male mate preferences can evolve, but do not otherwise Acknowledgments focus specifically on the effects that these male preferences might We thank Marcella Willett for the artwork in Figure 2. We thank the guest place on female traits. editor, Ingo Schlupp, as well as 3 anonymous reviewers, whose comments on previous versions improved the quality of this manuscript. Summary and Conclusions Although the number of mathematical models that investigate the Funding evolution of male mate choice has grown in recent decades, the lit- erature on this topic remains relatively small. The subset of these This work was supported by the National Institutes of Health award 5T32HD049336-12 [to C.L.F.]. papers investigating how this behavioral trait can drive trait evolu- tion in females is smaller still. Nonetheless, empirical examples of both male preferences and female-specific traits are now well docu- References mented. Thus, one of our conclusions is that many more interesting Adkins-Regan E, Akc¸ay E, Alonzo S, Bailey N, Crawford J et al., 2013. Sexual questions remain and there is more work to be done. selection studies: progress, challenges, and future directions. Final Report As we have discussed, many models have either assumed that from a NESCent Catalyst Meeting Durham NC, 15–17 July 2013. Revision male choice includes explicit costly contests between males, or have 1.1, 11 December 2013. Available at the PeerJ website. concluded that competitive costs emerge from the very nature of Ah-King M, Ahnesjo ¨ I, 2013. 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Current Zoology – Oxford University Press
Published: Apr 18, 2018
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