The role of mating preferences in shaping interspecific divergence in mating signals in vertebrates

Vertebrates represent one of the best-studied groups in terms of the role that mating preferences have played in the evolution of exaggerated secondary sexual characters and mating behaviours within species. Vertebrate species however, also exhibit enormous interspecific diversity in features of mating signals that has potentially led to reproductive isolation and speciation in many groups. The role that sexual selection has played in interspecific divergence in mating signals has been less fully explored. This review summarizes our current knowledge of how mating preferences within species have shaped interspecific divergence in mate recognition signals among the major vertebrate groups. Certain signal modalities appear to characterize mating signal diversification among different vertebrate taxa. Acoustic signals play an important role in mating decisions in anuran amphibians and birds. Here, different properties of the signal may convey information regarding individual, neighbor and species recognition. Mating preferences for particular features of the acoustic signal have led to interspecific divergence in calls and songs. Divergence in morphological traits such as colouration or ornamentation appears to be important in interspecific diversity in certain groups of fishes and birds. Pheromonal signals serve as the primary basis for species-specific mating cues in many salamander species, most mammals and even some fishes. The evolution of interspecific divergence in elaborate courtship displays may have played an important role in speciation of lizards, and particular groups of fishes, salamanders, birds and mammals. While much research has focused on the importance of mating preferences in shaping the evolution of these types of mating signals within species, the link between intraspecific preferences and interspecific divergence and speciation remains to be more fully tested. Future studies should focus on identifying how variation in mating preferences within a species shapes interspecific diversity in features of mating signals in order to better understand how sexual selection may have led to speciation in vertebrates.     

Sex chromosomes and male ornaments: a comparative evaluation in ray-finned fishes

Theory predicts that the mechanism of genetic sex determination can substantially influence the evolution of sexually selected traits. For example, female heterogamety (ZZ/ZW) can favour the evolution of extreme male traits under Fisher's runaway model of sexual selection. We empirically test whether the genetic system of sex determination has played a role in the evolution of exaggerated male ornaments in actinopterygiian fishes, a clade in which both female-heterogametic and male-heterogametic systems of sex determination have evolved multiple times. Using comparative methods both uncorrected and corrected for phylogenetic non-independence, we detected no significant correlation between sex-chromosome systems and sexually selected traits in males. Results suggest that sex-determination mechanism is at best a relatively minor factor affecting the outcomes of sexual selection in ray-finned fishes.     

The turn of the sword: length increases male swimming costs in swordtails

Sexual selection via female mate choice can result in the evolution of elaborate male traits that incur substantial costs for males. Despite increased interest in how female mating preferences contribute to the evolution of male traits, few studies have directly quantified the locomotor costs of such traits. A sexually selected trait that could affect movement costs is the sword exhibited by male swordtail fishes: while longer swords may increase male mating success, they could negatively affect the hydrodynamic aspects of swimming activities. Here, we examine the energetic costs of the sword in Xiphophorus montezumae by experimentally manipulating sword length and measuring male aerobic metabolism during two types of activity, routine swimming and courtship swimming. Direct measurements of oxygen consumption indicate that males with longer swords expend more energy than males with shortened swords during both types of swimming. In addition, the sword increases the cost of male courtship. Thus, while sexual selection via female choice favours long swords, males with longer swords experience higher metabolic costs during swimming, suggesting that sexual and natural selection have opposing effects on sword evolution. This study demonstrates a hydrodynamic cost of a sexually selected trait. In addition, this study discriminates between the cost of a sexually selected trait used in courtship and other courtship costs.     

Quantitative Genetic Analyses of Male Color Pattern and Female Mate Choice in a Pair of Cichlid Fishes of Lake Malawi,East Africa

The traits involved in sexual selection, such as male secondary sexual characteristics and female mate choice, often co-evolve which can promote population differentiation. However, the genetic architecture of these phenotypes can influence their evolvability and thereby affect the divergence of species. The extraordinary diversity of East African cichlid fishes is often attributed to strong sexual selection and thus this system provides an excellent model to test predictions regarding the genetic architecture of sexually selected traits that contribute to reproductive isolation. In particular, theory predicts that rapid speciation is facilitated when male sexual traits and female mating preferences are controlled by a limited number of linked genes. However, few studies have examined the genetic basis of male secondary sexual traits and female mating preferences in cichlids and none have investigated the genetic architecture of both jointly. In this study, we artificially hybridized a pair of behaviorally isolated cichlid fishes from Lake Malawi and quantified both melanistic color pattern and female mate choice. We investigated the genetic architecture of both phenotypes using quantitative genetic analyses. Our results suggest that 1) many non-additively acting genetic factors influence melanistic color patterns, 2) female mate choice may be controlled by a minimum of 1–2 non-additive genetic factors, and 3) F₂ female mate choice is not influenced by male courting effort. Furthermore, a joint analysis of color pattern and female mate choice indicates that the genes underlying these two traits are unlikely to be physically linked. These results suggest that reproductive isolation may evolve rapidly owing to the few genetic factors underlying female mate choice. Hence, female mate choice likely played an important role in the unparalleled speciation of East African cichlid fish.     

Effects of female preference intensity on the permissiveness of sexual trait polymorphisms

Recent developments in sexual selection theory suggest that on their own, mate preferences can promote the maintenance of sexual trait diversity. However, how mate preferences constrain the permissiveness of sexual trait diversity in different environmental regimes remains an open question. Here, we examine how a range of mate choice parameters affect the permissiveness of sexual trait polymorphism under several selection regimes. We use the null model of sexual selection and show that environments with strong assortative mating significantly increase the permissiveness of sexual trait polymorphism. We show that for a given change in mate choice parameters, the permissiveness of polymorphism changes more in environments with strong natural selection on sexual traits than in environments with weak selection. Sets of nearly stable polymorphic populations with weak assortative mating are more likely to show accidental divergence in sexual traits than sets of populations with strong assortative mating. The permissiveness of sexual trait polymorphism critically depends upon particular combinations of natural selection and mate choice parameters.     

The genetic basis of traits regulating sperm competition and polyandry: can selection favour the evolution of good- and sexy-sperm?

The good-sperm and sexy-sperm (GS-SS) hypotheses predict that female multiple mating (polyandry) can fuel sexual selection for heritable male traits that promote success in sperm competition. A major prediction generated by these models, therefore, is that polyandry will benefit females indirectly via their sons' enhanced fertilization success. Furthermore, like classic 'good genes' and 'sexy son' models for the evolution of female preferences, GS-SS processes predict a genetic correlation between genes for female mating frequency (analogous to the female preference) and those for traits influencing fertilization success (the sexually selected traits). We examine the premise for these predictions by exploring the genetic basis of traits thought to influence fertilization success and female mating frequency. We also highlight recent debates that stress the possible genetic constraints to evolution of traits influencing fertilization success via GS-SS processes, including sex-linked inheritance, nonadditive effects, interacting parental genotypes, and trade-offs between integrated ejaculate components. Despite these possible constraints, the available data suggest that male traits involved in sperm competition typically exhibit substantial additive genetic variance and rapid evolutionary responses to selection. Nevertheless, the limited data on the genetic variation in female mating frequency implicate strong genetic maternal effects, including X-linkage, which is inconsistent with GS-SS processes. Although the relative paucity of studies on the genetic basis of polyandry does not allow us to draw firm conclusions about the evolutionary origins of this trait, the emerging pattern of sex linkage in genes for polyandry is more consistent with an evolutionary history of antagonistic selection over mating frequency. We advocate further development of GS-SS theory to take account of the complex evolutionary dynamics imposed by sexual conflict over mating frequency.     

Ecology, sexual selection and speciation

The spectacular diversity in sexually selected traits among animal taxa has inspired the hypothesis that divergent sexual selection can drive speciation. Unfortunately, speciation biologists often consider sexual selection in isolation from natural selection, even though sexually selected traits evolve in an ecological context: both preferences and traits are often subject to natural selection. Conversely, while behavioural ecologists may address ecological effects on sexual communication, they rarely measure the consequences for population divergence. Herein, we review the empirical literature addressing the mechanisms by which natural selection and sexual selection can interact during speciation. We find that convincing evidence for any of these scenarios is thin. However, the available data strongly support various diversifying effects that emerge from interactions between sexual selection and environmental heterogeneity. We suggest that evaluating the evolutionary consequences of these effects requires a better integration of behavioural, ecological and evolutionary research.     

The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes

The question of how genetic variation translates into organismal diversity has puzzled biologists for decades. Despite recent advances in evolutionary and developmental genetics, the mechanisms that underlie adaptation, diversification and evolutionary innovation remain largely unknown. The exceptionally diverse species flocks of cichlid fishes are textbook examples of adaptive radiation and explosive speciation and emerge as powerful model systems to study the genetic basis of animal diversification. East Africa's hundreds of endemic cichlid species are akin to a natural mutagenesis screen and differ greatly not only in ecologically relevant (hence naturally selected) characters such as mouth morphology and body shape, but also in sexually selected traits such as coloration. One of the most fascinating aspects of cichlid evolution is the frequent occurrence of evolutionary parallelisms, which has led to the question whether selection alone is sufficient to produce these parallel morphologies, or whether a developmental or genetic bias has influenced the direction of diversification. Here, I review fitness-relevant traits that could be responsible for the cichlids' evolutionary success and assess whether these were shaped by sexual or natural selection. I then focus on the interaction and the relative importance of sexual vs. natural selection in cichlid evolution. Finally, I discuss what is currently known about the genes underlying the morphogenesis of adaptively relevant traits and highlight the importance of the forthcoming cichlid genomes in the quest of the genetic basis of diversification in this group.     

Variance in reproductive success and the opportunity for selection in a serially monogamous species: simulations of the mating system of <Emphasis Type="Italic">Tropheus</Emphasis> (Teleostei: Cichlidae)

Sexual selection is believed to play a major role in speciation processes of cichlid fishes in the East African Great Lakes, in particular Lakes Malawi and Victoria, by driving diversification in male nuptial coloration. In Lake Tanganyika, a high rate of color pattern diversification is found in the genus Tropheus, where more than 100, mostly allopatric, color morphs have been described. Whether color pattern differentiation in Tropheus could follow from sexual selection as well, has not yet been conclusively shown. Unlike typical sexually selected species, Tropheus are sexually monomorphic, establish temporary pair bonds and spawn monogamously. Variance in mating success among individuals would still allow for sexual selection, but due to their high population census sizes, parentage data from natural populations are difficult to obtain. Simulations designed according to existing data on mating behavior in Tropheus suggested that variance in male reproductive success can be substantial and lead to levels of opportunity for selection, which are similar to values estimated, for example, from natural populations of sexually dimorphic songbirds. Variance in male success was mostly affected by the way females perceived and reacted to differences between males, and to a lesser extent by the duration of components of the reproductive cycles of males and females. These results indicate that future work on the importance of sexual selection in Tropheus should concentrate on mate choice cues and female mate choice behavior, but does not depend critically on the acquisition of more detailed life history data.     

Is sexual selection driving diversification of the bioluminescent ponyfishes (Teleostei: Leiognathidae)?

Sexual selection may facilitate genetic isolation among populations and result in increased rates of diversification. As a mechanism driving diversification, sexual selection has been invoked and upheld in numerous empirical studies across disparate taxa, including birds, plants and spiders. In this study, we investigate the potential impact of sexual selection on the tempo and mode of ponyfish evolution. Ponyfishes (Leiognathidae) are bioluminescent marine fishes that exhibit sexually dimorphic features of their unique light-organ system (LOS). Although sexual selection is widely considered to be the driving force behind ponyfish speciation, this hypothesis has never been formally tested. Given that some leiognathid species have a sexually dimorphic LOS, whereas others do not, this family provides an excellent system within which to study the potential role of sexual selection in diversification and morphological differentiation. In this study, we estimate the phylogenetic relationships and divergence times for Leiognathidae, investigate the tempo and mode of ponyfish diversification, and explore morphological shape disparity among leiognathid clades. We recover strong support for a monophyletic Leiognathidae and estimate that all major ponyfish lineages evolved during the Paleogene. Our studies of ponyfish diversification demonstrate that there is no conclusive evidence that sexually dimorphic clades are significantly more species rich than nonsexually dimorphic lineages and that evidence is lacking to support any significant diversification rate increases within ponyfishes. Further, we detected a lineage-through-time signal indicating that ponyfishes have continuously diversified through time, which is in contrast to many recent diversification studies that identify lineage-through-time patterns that support mechanisms of density-dependent speciation. Additionally, there is no evidence of sexual selection hindering morphological diversity, as sexually dimorphic taxa are shown to be more disparate in overall shape morphology than nonsexually dimorphic taxa. Our results suggest that if sexual selection is occurring in ponyfish evolution, it is likely acting only as a genetic isolating mechanism that has allowed ponyfishes to continuously diversify over time, with no overall impact on increases in diversification rate or morphological disparity.     

The evolution of reproductive and genomic diversity in ray-finned fishes: insights from phylogeny and comparative analysis

Collectively, ray-finned fishes (Actinopterygii) display far more diversity in many reproductive and genomic features than any other major vertebrate group. Recent large-scale comparative phylogenetic analyses have begun to reveal the evolutionary patterns and putative causes for much of this diversity. Several such recent studies have offered clues to how different reproductive syndromes evolved in these fishes, as well as possible physiological and genomic triggers. In many cases, repeated independent origins of complex reproductive strategies have been uncovered, probably reflecting convergent selection operating on common suites of underlying genes and hormonal controls. For example, phylogenetic analyses have uncovered multiple origins and predominant transitional pathways in the evolution of alternative male reproductive tactics, modes of parental care and mechanisms of sex determination. They have also shown that sexual selection in these fishes is repeatedly associated with particular reproductive strategies. Collectively, studies on reproductive and genomic diversity across the Actinopterygii illustrate both the strengths and the limitations of comparative phylogenetic approaches on large taxonomic scales.     

An evolutionary limit to male mating success

The well-known phenotypic diversity of male sexual displays, and the high levels of genetic variation reported for individual display traits have generated the expectation that male display traits, and consequently male mating success, are highly evolvable. It has not been shown however that selection for male mating success, exerted by female preferences in an unmanipulated population, results in evolutionary change. Here, we tested the expectation that male mating success is highly evolvable in Drosophila bunnanda using an experimental evolution approach. Female D. bunnanda exhibit a strong, consistent preference for a specific combination of male cuticular hydrocarbons (CHCs). We used female preference to select for male mating success by propagating replicate populations from either attractive or unattractive males over 10 generations. Neither the combination of CHCs under sexual selection (the sexual signal) nor male mating success itself evolved. The lack of a response to selection was consistent with previous quantitative genetic experiments in D. bunnanda that demonstrated the virtual absence of genetic variance in the combination of CHCs under sexual selection. Persistent directional selection, such as applied by female mate choice, may erode genetic variance, resulting in multitrait evolutionary limits.     

GOOD GENES AND DIRECT SELECTION IN THE EVOLUTION OF MATING PREFERENCES

A model is used to study quantitatively the impact of a good genes process and direct natural selection on the evolution of a mating preference. The expression of a male display trait is proportional to genetic quality, which is determined by the number of deleterious mutations a male carries throughout his genome. Genetic variances and covariances, including the covariance between the preference and male trait that drives the good genes process, are allowed to evolve under an infinitesimal model. Results suggest that the good genes process generates only weak indirect selection on preferences, with an effective selection intensity of a few percent or less. If preferences are subject to direct natural selection of the intensity observed for other characters, the good genes process alone is not expected to exaggerate the male trait by more than a few phenotypic standard deviations, contrary to what is observed in highly sexually selected species. Good genes can, however, cause substantial exaggeration if preference genes are nearly selectively neutral. Alternatively, direct selection on preference genes, acting on mating behavior itself or on the genes' pleiotropic effects, can cause mating preferences and male display traits to be exaggerated by any degree. Direct selection of preference genes may therefore play an important role in species that show extreme sexual selection.     

Species Recognition Influences Female Mate Preferences in the Common European Grasshopper (Chorthippus biguttulus Linnaeus, 1758)

Species recognition and intraspecific mating preferences constitute two basic aspects of animal communication. Both can be considered as variations in response to signals and it has been suggested that they represent a continuum. Selection on species recognition could therefore influence intraspecific mating preferences. We show that females of the common European grasshopper Chorthippus biguttulus prefer conspecific male signals that can be distinguished more reliably from sympatrically occurring heterospecific signals. This suggests that in C. biguttulus, sexual selection might be influenced by pleiotropic effects from species recognition. The results show how the heterospecific signal environment could have determined why and in which direction specific traits become sexually selected.     

Sexual conflict and the evolution of female preferences for indicators of male quality

Males and females have opposing interests when it comes to the honesty of signals used in mate choice. The existence of this sexual conflict has long been acknowledged, but its consequences have not been fully investigated. By applying adaptive dynamics methods and individual-based computer simulations to a standard model for good-genes sexual selection, we show that sexual conflict over condition-dependent signaling can prevent the handicap process from ever attaining an evolutionary equilibrium. We outline the parameter conditions and properties of the underlying genetics conducive to nonequilibrium behavior and discuss the potential of such behavior to explain the elaboration and frequent phylogenetic loss of sexually selected traits. We also evaluate its consequences for well-established insights of sexual selection theory previously shown to apply when female mating preference and male ornament expression do converge on stable equilibrium levels. Contrary to equilibrium expectation, a continual change of condition-dependent signaling enables the evolution of a costly preference for a pure epistatic indicator and the evolution of preferences for redundant signals or a large number of independent ornaments. We thus conclude that seemingly general results of sexual selection theory, insofar as these are based on equilibrium considerations, do not extend to cases where nonequilibrium behavior occurs.     

Dietary stress increases the total opportunity for sexual selection and modifies selection on condition‐dependent traits

Although it is often expected that adverse environmental conditions depress the expression of condition‐dependent sexually selected traits, the full consequences of environmental change for the action of sexual selection, in terms of the opportunity for total sexual selection and patterns of phenotypic selection, are unknown. Here we show that dietary stress in guppies, Poecilia reticulata, reduces the expression of several sexually selected traits and increases the opportunity for total sexual selection (standardized variance in reproductive success) in males. Furthermore, our results show that dietary stress modulates the relative importance of precopulatory (mating success) and postcopulatory (relative fertilization success) sexual selection, and that the form of multivariate sexual selection (linear vs. nonlinear) depends on dietary regime. Overall, our results are consistent with a pattern of heightened directional selection on condition‐dependent sexually selected traits under environmental stress, and underscore the importance of sexual selection in shaping adaptation in a changing world.     

Comparative phylogenetic analysis of male alternative reproductive tactics in ray-finned fishes

Using comparative phylogenetic analysis, we analyzed the evolution of male alternative reproductive tactics (MARTs) in ray-finned fishes (Actinopterygii). Numerous independent origins for each type of MART (involving sneaker males, female mimics, pirates, and satellite males) indicate that these behaviors have been highly labile across actinopterygiian evolution, consistent with a previous notion that convergent selection in fishes can readily mold the underlying suites of reproductive hormones into similar behaviors. The evolutionary appearance of MARTs was significantly correlated with the presence of sexually selected traits in bourgeois males (P = 0.001) but not with the presence of male parental care. This suggests that MARTs often arise from selection on some males to circumvent bourgeois male investment in mate monopolization, rather than to avoid male brood care per se. We found parsimony evidence for an evolutionary progression of MARTs wherein sneaking is usually the evolutionary precursor to the presumably more complex MARTs of female mimicry and cooperative satellite behavior. Nest piracy appears not to be part of this evolutionary progression, possibly because its late onset in the life cycle of most ray-finned fishes reduces the effects of selection on this reproductive tactic.     

Origins of female genital diversity: Predation risk and lock‐and‐key explain rapid divergence during an adaptive radiation

The study of male genital diversity has long overshadowed evolutionary inquiry of female genitalia, despite its nontrivial diversity. Here, we identify four nonmutually exclusive mechanisms that could lead to genital divergence in females, and potentially generate patterns of correlated male–female genital evolution: (1) ecological variation alters the context of sexual selection (“ecology hypothesis”), (2) sexually antagonistic selection (“sexual‐conflict hypothesis”), (3) female preferences for male genitalia mediated by female genital traits (“female‐choice hypothesis”), and (4) selection against inter‐population mating (“lock‐and‐key hypothesis”). We performed an empirical investigation of all four hypotheses using the model system of Bahamas mosquitofish inhabiting blue holes that vary in predation risk. We found unequivocal support for the ecology hypothesis, with females exhibiting a smaller genital opening in blue holes containing piscivorous fish. This is consistent with stronger postmating female choice/conflict when predators are present, but greater premating female choice in their absence. Our results additionally supported the lock‐and‐key hypothesis, uncovering a pattern of reproductive character displacement for genital shape. We found no support for the sexual conflict or female choice hypotheses. Our results demonstrate a strong role for ecology in generating female genital diversity, and suggest that lock‐and‐key may provide a viable cause of female genital diversification.     

Rapid courtship evolution in grouse (Tetraonidae): contrasting patterns of acceleration between the Eurasian and North American polygynous clades

Sexual selection is thought to be a powerful diversifying force, based on large ornamental differences between sexually dimorphic species. This assumes that unornamented phenotypes represent evolution without sexual selection. If sexual selection is more powerful than other forms of selection, then two effects would be: rapid divergence of sexually selected traits and a correlation between these divergence rates and variance in mating success in the ornamented sex. I tested for these effects in grouse (Tetraonidae). For three species pairs, within and among polygynous clades, male courtship characters had significantly greater divergence than other characters. This was most pronounced for two species in Tympanuchus. In the Eurasian polygynous clade, relative courtship divergence gradually increased with nucleotide divergence, suggesting a less dramatic acceleration. Increase in relative courtship divergence was associated with mating systems having higher variance in male mating success. These results suggest that sexual selection has accelerated courtship evolution among grouse, although the microevolutionary details appear to vary among clades.     

Fisher's lost model of runaway sexual selection

The bizarre elaboration of sexually selected traits such as the peacock's tail was a puzzle to Charles Darwin and his 19th century followers. Ronald A. Fisher crafted an ingenious solution in the 1930s, positing that female preferences would become genetically correlated with preferred traits due to nonrandom mating. These genetic correlations would translate selection for preferred traits into selection for stronger preferences, leading to a self-reinforcing process of ever-elaborating traits and preferences. It is widely believed that Fisher provided only a verbal model of this “runaway” process. However, in correspondence with Charles Galton Darwin, Fisher also laid out a simple mathematical model that purportedly confirms his verbal prediction of runaway sexual selection. Unfortunately, Fisher's model contains inconsistencies that render his quantitative conclusions inaccurate. Here, we correct Fisher's model and show that it contains all the ingredients of a working runaway process. We derive quantitative predictions of his model using numerical techniques that were unavailable in Fisher's time. Depending on parameter values, mean traits and preferences may increase until genetic variance is depleted by selection, exaggerate exponentially while their variances remain stable, or both means and variances may increase super-exponentially. We thus present the earliest mathematical model of runaway sexual selection.