The evolution of reproductive character displacement conflicts with how sexual selection operates within a species

Processes that affect the evolution of female preferences or male display traits involved in mating decisions in different geographic areas have the potential to result in within-species divergence. This could occur via reinforcement of mate recognition in species using the same traits for species recognition and sexual selection. Sympatric individuals experience reinforcement of female preferences and male display traits, whereas allopatric individuals do not, creating the potential for divergent sexual selection in sympatric and allopatric populations. Sexual selection operates on the cuticular hydrocarbons (CHCs) of Drosophila serrata, and reinforcement on the CHCs of populations sympatric with D. birchii. Here, we manipulate sexual selection in D. serrata populations generated by hybridizing natural sympatric and allopatric populations. Under the influence of sexual selection, male CHCs evolved from an intermediate phenotype to resemble an allopatric phenotype, which was driven by female choice. Additionally, female choice resulted in evolution of an allopatric female preference, so that allopatric males were preferred to sympatric males. Allopatric CHCs and preferences represent a sexual selection optimum via female choice. Sympatric populations display suboptimal phenotypes relative to their allopatric conspecifics. The combination of reinforcement and sexual selection can therefore generate divergence in female preferences and male display traits.     

Female discrimination thresholds frequently exceed local male display variation: implications for mate choice dynamics and sexual selection

Among the factors that can influence female mate choice decisions is the degree to which females differentiate among similar displays: as differences decrease, females are expected to eventually stop discriminating. This discrimination threshold, in conjunction with the magnitude of male trait variation females regularly encounter while making mate choice decisions, may have important consequences for sexual selection. If local display variation is above the discrimination threshold, female preferences should translate into higher mating success for the more attractive male. But if display variation is frequently below the threshold, the resulting increased pattern of random mating may obscure the existence of female mate choice. I investigated the interplay between female discrimination and male display variation in green treefrogs (Hyla cinerea) and found that call trait differences between nearest neighbour males were frequently smaller than what females are expected to discriminate. This finding has two important consequences for our understanding of sexual selection in the wild: first, low display variation should weaken the strength of selection on male display traits, but the direction of selection should mirror the one predicted from females choice trials. Second, caution is needed when interpreting data on realized mating success in the wild: a pattern of random mating with respect to male display traits does not always mean that female preferences are weak or that conditions are too challenging for females to express their preferences. Rather, insufficient display variation can generate the same pattern.     

Sexual selection drives rapid divergence in bowerbird display traits

Abstract.— Sexual selection driving display trait divergence has been suggested as a cause of rapid speciation, but there is limited supporting evidence for this from natural populations. Where speciation by sexual selection has occurred in newly diverged populations, we expect that there will be significant differences in female preferences and corresponding male display traits in the absence of substantial genetic and other morphological differentiation. Two allopatric populations of the Vogelkop bowerbird, Amblyornis inornatus , show large, qualitative differences in a suite of display traits including bower structure and decorations. We experimentally demonstrate distinct male decoration color preferences within each population, provide direct evidence of female preferences for divergent decoration and bower traits in the population with more elaborate display, and show that there is minimal genetic differentiation between these populations. These results support the speciation by sexual selection hypothesis and are most consistent with the hypothesis that changes in male display have been driven by divergent female choice.     

Acoustic preference functions and sexual selection on the male calling song in the grasshopper Chorthippus biguttulus

Male courtship songs have two functions in species recognition and intraspecific mate choice. Female preference might thus exert different types of selection pressure on male song traits. We used a combination of acoustic mate choice experiments and statistical analyses to examine how traits of the calling songs of male nightingale grasshoppers,Chorthippus biguttulus , are influenced by different sexual selection pressures. We recorded calling songs of males and tested their attractiveness to females in acoustic mate choice experiments. The attractiveness values were a good estimate of the potential male mating success. In experiments with a pair of males, females copulated significantly more often with the male that had the higher attractiveness value. To detect directional, stabilizing, disruptive or correlative selection acting on male song properties we used linear and nonlinear regressions between male song traits and female response behaviour. Three signal traits were revealed to be under directional selection: song loudness, pause to syllable ratio and the mean duration of gaps within syllables. A nonlinear regression testing for correlative selection showed that a fourth song trait, rhythm, in combination with mean gap duration was also important for female mate choice. With these traits and trait combinations we were able to explain 42% of the variance in attractiveness between males. Since we found no evidence for stabilizing selection, but ample evidence for directional selection, we conclude that selection on the traits examined is related to mate choice mainly in the context of intraspecific sexual selection and probably less so in species recognition. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Intraspecific evidence from guppies for correlated patterns of male and female genital trait diversification

The role of sexual selection in fuelling genital evolution is becoming increasingly apparent from comparative studies revealing interspecific divergence in male genitalia and evolutionary associations between male and female genital traits. Despite this, we know little about intraspecific variance in male genital morphology, or how male and female reproductive traits covary among divergent populations. Here we address both topics using natural populations of the guppy, Poecilia reticulata, a livebearing fish that exhibits divergent patterns of male sexual behaviour among populations. Initially, we performed a series of mating trials on a single population to examine the relationship between the morphology of the male's copulatory organ (the gonopodium) and the success of forced matings. Using a combination of linear measurements and geometric morphometrics, we found that variation in the length and shape of the gonopodium predicted the success of forced matings in terms of the rate of genital contacts and insemination success, respectively. We then looked for geographical divergence in these traits, since the relative frequency of forced matings tends to be greater in high-predation populations. We found consistent patterns of variation in male genital size and shape in relation to the level of predation, and corresponding patterns of (co)variation in female genital morphology. Together, these data enable us to draw tentative conclusions about the underlying selective pressures causing correlated patterns of divergence in male and female genital traits, which point to a role for sexually antagonistic selection.     

Role of sexual selection in speciation in Drosophila

The power of sexual selection to drive changes in the mate recognition system through divergence in sexually selected traits gives it the potential to be a potent force in speciation. To know how sexual selection can bring such type of divergence in the genus Drosophila, comparative studies based on intra- and inter-sexual selection are documented in this review. The studies provide evidence that both mate choice and male–male competition can cause selection of trait and preference which thereby leads to divergence among species. In the case of intrasexual selection, various kinds of signals play significant role in affecting the species mate recognition system and hence causing divergence between the species. However, intrasexual selection can bring the intraspecific divergence at the level of pre- and post-copulatory stage. This has been better explained through Hawaiian Drosophila which has been suggested a wonderful model system in explaining the events of speciation via sexual selection. This is due to their elaborate mating displays and some kind of ethological isolation persisting among them. Similarly, the genetic basis of sexually selected variations can provide yet another path in understanding the speciation genetics via sexual selection more closely.     

Sexual selection accelerates signal evolution during speciation in birds

Sexual selection is proposed to be an important driver of diversification in animal systems, yet previous tests of this hypothesis have produced mixed results and the mechanisms involved remain unclear. Here, we use a novel phylogenetic approach to assess the influence of sexual selection on patterns of evolutionary change during 84 recent speciation events across 23 passerine bird families. We show that elevated levels of sexual selection are associated with more rapid phenotypic divergence between related lineages, and that this effect is restricted to male plumage traits proposed to function in mate choice and species recognition. Conversely, we found no evidence that sexual selection promoted divergence in female plumage traits, or in male traits related to foraging and locomotion. These results provide strong evidence that female choice and male–male competition are dominant mechanisms driving divergence during speciation in birds, potentially linking sexual selection to the accelerated evolution of pre-mating reproductive isolation.     

A review of the potential of surface flow constructed wetlands to enhance macroinvertebrate diversity in agricultural landscapes with particular reference to Integrated Constructed Wetlands (ICWs)

Discriminating female mate preferences enhance the variance in reproductive success among males of a population and create a potential for sexual selection, which can account for trait evolution and diversification. Fish color patterns are among the prime targets of mate choice-driven sexual selection. Populations of the cichlid Tropheus from Lake Tanganyika display remarkable geographic color pattern variation, but the role of female choice in their rapid and rich phenotypic diversification is unclear. Males and females establish a pair bond prior to spawning monogamously, but as brood care is strictly maternal, female investment in reproduction is high and the operational sex ratio is male-biased. Therefore, variance in male reproductive success can accrue if individual males succeed repeatedly in securing a mate. To test this prediction in the red colored Tropheus moorii “Chimba”, four pairs of males were presented to a series of females and female mate preferences were inferred from pairwise interactions. There was a significant difference in mating success between the males of each pair (P < 0.001 over all trials), as—with one exception—females shared preferences for the same males. Male courtship activity was strongly correlated with female choice. Our experiment suggests that female choice contributes to the variance in male reproductive success in the tested population.     

The role of maternal and paternal effects in the evolution of parental quality by sexual selection

Genetic models of maternal effects and models of mate choice have focused on the evolutionary effects of variation in parental quality. There have been, however, few attempts to combine these into a single model for the evolution of sexually selected traits. We present a quantitative genetic model that considers how male and female parental quality (together or separately) affect the expression of a sexually selected offspring trait. We allow female choice of males based on this parentally affected trait and examine the evolution of mate choice, parental quality and the indicator trait. Our model reveals a number of consequences of maternal and paternal effects. (1) The force of sexual selection owing to adaptive mate choice can displace parental quality from its natural selection optimum. (2) The force of sexual selection can displace female parental quality from its natural selection optimum even when nonadaptive mate choice occurs (e.g. runaway sexual selection), because females of higher parental quality produce more attractive sons and these sons counterbalance the loss in fitness owing to over-investment in each offspring. (3) Maternal and paternal effects can provide a source of genetic variation for offspring traits, allowing evolution by sexual selection even when those traits do not show direct genetic variation (i.e. are not heritable). (4) The correlation between paternal investment and the offspring trait influenced by the parental effects can result in adaptive mate choice and lead to the elaboration of both female preference and the male sexually selected trait. When parental effects exist, sexual selection can drive the evolution of parental quality when investment increases the attractiveness of offspring, leading to the elaboration of indicator traits and higher than expected levels of parental investment.     

Female mating preferences and male coloration covary with water transparency in a Lake Victoria cichlid fish

Rapid speciation in Lake Victoria cichlid fish of the genus Pundamilia may be facilitated by sexual selection: female mate choice exerts sexual selection on male nuptial coloration within species and maintains reproductive isolation between species. However, declining water transparency coincides with increasingly dull coloration and increasing hybridization. In the present study, we investigated the mechanism underlying this pattern in Pundamilia nyererei, a species that interbreeds with a sister species in turbid but not in clear water. We compared measures of intraspecific sexual selection between two populations from locations that differ in water transparency. First, in laboratory mate‐choice experiments, conducted in clear water and under broad‐spectrum illumination, we found that females originating from turbid water have significantly weaker preferences for male coloration than females originating from clear water. Second, both the hue and body coverage of male coloration differ between populations, which is consistent with adaptation to different photic habitats. These findings suggest that the observed relationship between male coloration and water transparency is not mediated by environmental variation alone. Rather, female mating preferences are indicated to have changed in response to this variation, constituting the first evidence for intraspecific preference‐trait co‐evolution in cichlid fish. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 398–406.     

EVOLUTION OF DIVERGENT FEMALE MATING PREFERENCE IN RESPONSE TO EXPERIMENTAL SEXUAL SELECTION

Sexual selection is predicted to drive the coevolution of mating signals and preferences (mating traits) within populations, and could play a role in speciation if sexual isolation arises due to mating trait divergence between populations. However, few studies have demonstrated that differences in mating traits between populations result from sexual selection alone. Experimental evolution is a promising approach to directly examine the action of sexual selection on mating trait divergence among populations. We manipulated the opportunity for sexual selection (low vs. high) in populations of Drosophila pseudoobscura. Previous studies on these experimental populations have shown that sexual selection manipulation resulted in the divergence between sexual selection treatments of several courtship song parameters, including interpulse interval (IPI) which markedly influences male mating success. Here, we measure female preference for IPI using a playback design to test for preference divergence between the sexual selection treatments after 130 generations of experimental sexual selection. The results suggest that female preference has coevolved with male signal, in opposite directions between the sexual selection treatments, providing direct evidence of the ability of sexual selection to drive the divergent coevolution of mating traits between populations. We discuss the implications in the context sexual selection and speciation.     

Fluctuating mate preferences in a marine fish

According to theory, directional female choice for male sexual ornaments is expected to erode underlying genetic variation. Considerable attention, in this regard, has been given to understanding the ubiquity of heritable genetic variation in both female choice and male sexual traits. One intriguing possibility emerging from this work is that persistent genetic variation could be maintained, over time, by variation in female mate preferences. Here, we report the results of a four-year study showing significant year-to-year fluctuations in mate preferences in a small marine fish, the sand goby, Pomatoschistus minutus. Although the average size of mature fish varied across years, we were unable to find direct evidence linking this variation to differences in female preferences among years. Our results, nevertheless, underscore the importance of temporal fluctuations in female mate preferences, as these can have important consequences for understanding variation in sexual traits and the intensity of sexual selection.     

The search for causal traits of speciation: Divergent female mate preferences target male courtship song,not pheromones,in Drosophila athabasca species complex

Understanding speciation requires the identification of traits that cause reproductive isolation. This remains a major challenge since it is difficult to determine which of the many divergent traits actually caused speciation. To overcome this difficulty, we studied the sexual cue traits and behaviors associated with rapid speciation between EA and WN sympatric behavioral races of Drosophila athabasca that diverged only 16,000–20,000 years ago. First, we found that sexual isolation was essentially complete and driven primarily by divergent female mating preferences. To determine the target of female mate choice, we found that, unlike cuticular hydrocarbons (CHCs), male courtship song is highly divergent between EA and WN in both allopatry and sympatry and is not affected by latitudinal variation. We then used pheromone rub‐off experiments to show no effect of CHCs on divergent female mate choice. In contrast, both male song differences and male mating success in hybrids exhibited a large X‐effect and playback song experiments confirmed that male courtship song is indeed the target of sexual isolation. These results show that a single secondary sexual trait is a major driver of speciation and suggest that we may be overestimating the number of traits involved in speciation when we study older taxa.     

Runaway sexual selection without genetic correlations: social environments and flexible mate choice initiate and enhance the fisher process

Female mating preferences are often flexible, reflecting the social environment in which they are expressed. Associated indirect genetic effects (IGEs) can affect the rate and direction of evolutionary change, but sexual selection models do not capture these dynamics. We incorporate IGEs into quantitative genetic models to explore how variation in social environments and mate choice flexibility influence Fisherian sexual selection. The importance of IGEs is that runaway sexual selection can occur in the absence of a genetic correlation between male traits and female preferences. Social influences can facilitate the initiation of the runaway process and increase the rate of trait elaboration. Incorporating costs to choice do not alter the main findings. Our model provides testable predictions: (1) genetic covariances between male traits and female preferences may not exist, (2) social flexibility in female choice will be common in populations experiencing strong sexual selection, (3) variation in social environments should be associated with rapid sexual trait divergence, and (4) secondary sexual traits will be more elaborate than previously predicted. Allowing feedback from the social environment resolves discrepancies between theoretical predictions and empirical data, such as why indirect selection on female preferences, theoretically weak, might be sufficient for preferences to become elaborated.     

Does divergence in female mate choice affect male size distributions in two cave fish populations?

Sexual selection by female choice can maintain male traits that are counter selected by natural selection. Alteration of the potential for sexual selection can thus lead to shifts in the expression of male traits. We investigated female mate choice for large male body size in a fish (Poecilia mexicana) that, besides surface streams, also inhabits two caves. All four populations investigated, exhibited an ancestral visual preference for large males. However, only one of the cave populations also expressed this female preference in darkness. Hence, the lack of expression of female preference in darkness in the other cave population leads to relaxation of sexual selection for large male body size. While P. mexicana populations with size-specific female mate choice are characterized by a pronounced male size variation, the absence of female choice in one cave coincides with the absence of large bodied males in that population. Our results suggest that population differences in the potential for sexual selection may affect male trait variation.     

Divergence in coloration and ecological speciation in the Anolis marmoratus species complex

Adaptive divergence in coloration is expected to produce reproductive isolation in species that use colourful signals in mate choice and species recognition. Indeed, many adaptive radiations are characterized by differentiation in colourful signals, suggesting that divergent selection acting on coloration may be an important component of speciation. Populations in the Anolis marmoratus species complex from the Caribbean island of Guadeloupe display striking divergence in the colour and pattern of adult males that occurs over small geographic distances, suggesting strong divergent selection. Here we test the hypothesis that divergence in coloration results in reduced gene flow among populations. We quantify variation in adult male coloration across a habitat gradient between mesic and xeric habitats, use a multilocus coalescent approach to infer historical demographic parameters of divergence, and examine gene flow and population structure using microsatellite variation. We find that colour variation evolved without geographic isolation and in the face of gene flow, consistent with strong divergent selection and that both ecological and sexual selection are implicated. However, we find no significant differentiation at microsatellite loci across populations, suggesting little reproductive isolation and high levels of contemporary gene exchange. Strong divergent selection on loci affecting coloration probably maintains clinal phenotypic variation despite high gene flow at neutral loci, supporting the notion of a porous genome in which adaptive portions of the genome remain fixed whereas neutral portions are homogenized by gene flow and recombination. We discuss the impact of these findings for studies of colour evolution and ecological speciation.     

Divergence in Female Duetting Signals in the Enchenopa binotata Species Complex of Treehoppers (Hemiptera: Membracidae)

Sexual communication often involves signal exchanges between the sexes, or duetting, in which mate choice is expressed through response signals. With both sexes acting as signalers and receivers, variation in the signals of males and females may be important for mate choice, reproductive isolation, and divergence. In the Enchenopa binotata species complex – a case study of sympatric speciation in which vibrational duetting may have an important role – male signals are species‐specific, females choose among males on the basis of signal traits that reflect species and individual differences, and female preferences have exerted divergent selection on male signals. Here, we describe variation in female signals in the E. binotata species complex. We report substantial species differences in the spectral and temporal features of female signals, and in their timing relative to male signals. These differences were similar in range to differences in male signals in the E. binotata complex. We consider processes that might contribute to divergence in female signals, and suggest that signal evolution in the E. binotata complex may be influenced by mate choice in both sexes.     

Beyond magic traits: Multimodal mating cues in Heliconius butterflies

Species coexistence involves the evolution of reproductive barriers opposing gene flow. Heliconius butterflies display colorful patterns affecting mate choice and survival through warning signaling and mimicry. These patterns are called “magic traits” for speciation because divergent natural selection may promote mimicry shifts in pattern whose role as mating cue facilitates reproductive isolation. By contrast, between comimetic species, natural selection promotes pattern convergence. We addressed whether visual convergence interferes with reproductive isolation by testing for sexual isolation between two closely related species with similar patterns, H. timareta thelxinoe and H. melpomene amaryllis. Experiments with models confirmed visual attraction based on wing phenotype, leading to indiscriminate approach. Nevertheless, mate choice experiments showed assortative mating. Monitoring male behavior toward live females revealed asymmetry in male preference, H. melpomene males courting both species equally while H. timareta males strongly preferred conspecifics. Experiments with hybrid males suggested an important genetic component for such asymmetry. Behavioral observations support a key role for short‐distance cues in determining male choice in H. timareta. Scents extracts from wings and genitalia revealed interspecific divergence in chemical signatures, and hybrid female scent composition was significantly associated with courtship intensity by H. timareta males, providing candidate chemical mating cues involved in sexual isolation.     

Independent Mating Preferences for Male Body Size and Coloration in Female Trinidadian Guppies

Although females in numerous species generally prefer males with larger, brighter and more elaborate sexual traits, there is nonetheless considerable intra‐ and interpopulation variation in mating preferences amongst females that requires explanation. Such variation exists in the Trinidadian guppy, Poecilia reticulata, an important model organism for the study of sexual selection and mate choice. While female guppies tend to prefer more ornamented males as mates, particularly those with greater amounts of orange coloration, there remains variation both in male traits and female mating preferences within and between populations. Male body size is another trait that is sexually selected through female mate choice in some species, but has not been examined as extensively as body coloration in the guppy despite known intra‐ and interpopulation variation in this trait among adult males and its importance for survivorship in this species. In this study, we used a dichotomous‐choice test to quantify the mating preferences of female guppies, originating from a low‐predation population in Trinidad, for two male traits, body length and area of the body covered with orange and black pigmentation, independently of each other. We expected strong female mating preferences for both male body length and coloration in this population, given relaxation from predation and presumably relatively low cost of choice. Females indeed exhibited a strong preference for larger males as expected, but surprisingly a weaker (but nonetheless significant) preference for orange and black coloration. Interestingly, larger females demonstrated stronger preferences for larger males than did smaller females, which could potentially lead to size‐assortative mating in nature.