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.     

Direct fitness benefits explain mate preference,but not choice,for similarity in heterozygosity levels

Under sexual selection, mate preferences can evolve for traits advertising fitness benefits. Observed mating patterns (mate choice) are often assumed to represent preference, even though they result from the interaction between preference, sampling strategy and environmental factors. Correlating fitness with mate choice instead of preference will therefore lead to confounded conclusions about the role of preference in sexual selection. Here we show that direct fitness benefits underlie mate preferences for genetic characteristics in a unique experiment on wild great tits. In repeated mate preference tests, both sexes preferred mates that had similar heterozygosity levels to themselves, and not those with which they would optimise offspring heterozygosity. In a subsequent field experiment where we cross fostered offspring, foster parents with more similar heterozygosity levels had higher reproductive success, despite the absence of assortative mating patterns. These results support the idea that selection for preference persists despite constraints on mate choice.     

Sexual and reproductive behaviour of Drosophila melanogaster from a microclimatically interslope differentiated population of "Evolution Canyon" (Mount Carmel, Israel).

The strong microscale interslope environmental differences in "Evolution Canyon" provide an excellent natural model for sympatric speciation. Our previous studies revealed significant slope-specific differences for a fitness complex of Drosophila. This complex involved either adaptation traits (tolerance to high temperature, different viability and longevity pattern) or behavioural differentiation, manifested in habitat choice and non-random mating. This remarkable differentiation has evolved despite a very small interslope distance (a few hundred metres only). Our hypothesis is that strong interslope microclimatic contrast caused differential selection for fitness-related traits accompanied by behavioural differentiation and reinforced by some sexual isolation, which started incipient speciation. Here we describe the results of a systematic analysis of sexual behaviour in a non-choice situation and several reproductive parameters of D. melanogaster populations from the opposite slopes of "Evolution Canyon". The evidence indicates that: (i) mate choice derives from differences in mating propensity and discrimination; (ii) females from the milder north-facing slope discriminate strongly against males of the opposite slope; (iii) both sexes of the south-facing slope display distinct reproductive and behavioural patterns with females showing increased fecundity, shorter time before remating and relatively higher receptivity, and males showing higher mating propensity. These patterns represent adaptive life strategies contributing to higher fitness.     

The evolution of wing color: male mate choice opposes adaptive wing color divergence in Colias butterflies

Abstract Correlated evolution of mate signals and mate preference may be constrained if selection pressures acting on mate preference differ from those acting on mate signals. In particular, opposing selection pressures may act on mate preference and signals when traits have sexual as well as nonsexual functions. In the butterfly Colias philodice eriphyle , divergent selection on wing color across an elevational gradient in response to the thermal environment has led to increasing wing melanization at higher elevations. Wing color is also a long-range signal used by males in mate searching. We conducted experiments to test whether sexual selection on wing melanization via male mate choice acts in the same direction as natural selection on mate signals due to the thermal environment. We performed controlled mate choice experiments in the field over an elevational range of 1500 meters using decoy butterflies with different melanization levels. Also, we obtained a more direct estimate of the relation between wing color and sexual selection by measuring mating success in wild-caught females. Both our experiments showed that wing melanization is an important determinant of female mating success in C. p. eriphyle . However, a lack of elevational variation in male mate preference prevents coevolution of mate signals and mate preference, as males at all elevations prefer less-melanized females. We suggest that this apparently maladaptive mate choice may be maintained by differences in detectability between the morphs or by preservation of species recognition.     

Populations with elevated mutation load do not benefit from the operation of sexual selection

Theory predicts that if most mutations are deleterious to both overall fitness and condition-dependent traits affecting mating success, sexual selection will purge mutation load and increase nonsexual fitness. We explored this possibility with populations of mutagenized Drosophila melanogaster exhibiting elevated levels of deleterious variation and evolving in the presence or absence of male-male competition and female choice. After 60 generations of experimental evolution, monogamous populations exhibited higher total reproductive output than polygamous populations. Parental environment also affected fitness measures - flies that evolved in the presence of sexual conflict showed reduced nonsexual fitness when their parents experienced a polygamous environment, indicating trans-generational effects of male harassment and highlighting the importance of a common garden design. This cost of parental promiscuity was nearly absent in monogamous lines, providing evidence for the evolution of reduced sexual antagonism. There was no overall difference in egg-to-adult viability between selection regimes. If mutation load was reduced by the action of sexual selection in this experiment, the resultant gain in fitness was not sufficient to overcome the costs of sexual antagonism.     

Sexual selection's impacts on ecological specialization: an experimental test

In many species, individuals specialize on different resources, thereby reducing competition. Such ecological specialization can promote the evolution of alternative ecomorphs—distinct phenotypes adapted for particular resources. Elucidating whether and how this process is influenced by sexual selection is crucial for understanding how ecological specialization promotes the evolution of novel traits and, potentially, speciation between ecomorphs. We evaluated the population-level effects of sexual selection (as mediated by mate choice) on ecological specialization in spadefoot toad tadpoles that express alternative ecomorphs. We manipulated whether sexual selection was present or reversed by mating females to their preferred versus non-preferred males, respectively. We then exposed their tadpoles to resource competition in experimental mesocosms. The resulting distribution of ecomorphs was similar between treatments, but sexual selection generated poorer trait integration in, and lower fitness of, the more specialized carnivore morph. Moreover, disruptive and directional natural selection were weaker in the sexual selection present treatment. Nevertheless, this effect on disruptive selection was smaller than previously documented effects of ecological opportunity and competitor density. Thus, sexual selection can inhibit adaptation to resource competition and thereby hinder ecological specialization, particularly when females obtain fitness benefits from mate choice that offset the cost of producing competitively inferior offspring.     

Sexual selection is influenced by both developmental and adult environments

Sexual selection is often assumed to be strong and consistent, yet increasing research shows it can fluctuate over space and time. Few experimental studies have examined changes in sexual selection in response to natural environmental variation. Here, we use a difference in resource quality to test for the influence of past environmental conditions and current environmental conditions on male and female mate choice and resulting selection gradients for leaf‐footed cactus bugs, Narnia femorata. We raised juveniles on natural high‐ and low‐quality diets, cactus pads with and without ripe cactus fruits. New adults were again assigned a cactus pad with or without fruit, paired with a potential mate, and observed for mating behaviors. We found developmental and adult encounter environments affected mating decisions and the resulting patterns of sexual selection for both males and females. Males were not choosy in the low‐quality encounter environment, cactus without fruit, but they avoided mating with small females in the high‐quality encounter environment. Females were choosy in both encounter environments, avoiding mating with small males. However, they were the choosiest when they were in the low‐quality encounter environment. Female mate choice was also context dependent by male developmental environment. Females were more likely to mate with males that had developed on cactus with fruit when they were currently in the cactus with fruit environment. This pattern disappeared when females were in the cactus without fruit environment. Altogether, these results experimentally demonstrate context‐dependent mate choice by both males and females. Furthermore, we demonstrate that simple, seasonal changes in resources can lead to fluctuations in sexual selection.     

Beauty and the beast: mechanisms of sexual selection in humans

Literature in evolutionary psychology suggests that mate choice has been the primary mechanism of sexual selection in humans, but this conclusion conforms neither to theoretical predictions nor available evidence. Contests override other mechanisms of sexual selection; that is, when individuals can exclude their competitors by force or threat of force, mate choice, sperm competition, and other mechanisms are impossible. Mates are easier to monopolize in two dimensional mating environments, such as land, than in three-dimensional environments, such as air, water, and trees. Thus, two-dimensional mating environments may tend to favor the evolution of contests. The two-dimensionality of the human mating environment, along with phylogeny, the spatial and temporal clustering of mates and competitors, and anatomical considerations, predict that contest competition should have been the primary mechanism of sexual selection in men. A functional analysis supports this prediction. Men's traits are better designed for contest competition than for other sexual selection mechanisms; size, muscularity, strength, aggression, and the manufacture and use of weapons probably helped ancestral males win contests directly, and deep voices and facial hair signal dominance more effectively than they increase attractiveness. However, male monopolization of females was imperfect, and female mate choice, sperm competition, and sexual coercion also likely shaped men's traits. In contrast, male mate choice was probably central in women's mating competition because ancestral females could not constrain the choices of larger and more aggressive males through force, and attractive women could obtain greater male investment. Neotenous female features and body fat deposition on the breasts and hips appear to have been shaped by male mate choice.     

Nonlinear effects of female mate choice in wild threespine sticklebacks

Sexual selection by mate choice represents a very important selective pressure in many animal species and might have evolutionary impacts beyond exaggeration of secondary sexual traits. Describing the shape and strength of the relationships linking mating success and nonsexual traits in natural conditions represents a challenging step in our understanding of adaptive evolution. We studied the effect of behavioral (nest site choice), immunological (trematode level of infection), genetic diversity (measured by mean d2) and morphological (standard length and pectoral fin size) traits on male mating success in a natural population of threespine sticklebacks Gasterosteaus aculeatus. Male mating success was measured by microsatellite genotyping of embryos used to infer female genotypes. First, we analyzed all territorial males (full analysis) but also considered independently only males with a nonzero mating success (reduced analysis) because some of the males with no eggs could have been part of a later breeding cycle. Multiple linear regressions identified a significant negative effect of parasite load in the full analysis, whereas no linear effect was found in the reduced analysis. The quadratic analyses revealed that nest location and parasite load were significantly related to mating success by positive (concave selection) and negative (convex selection) quadratic coefficients respectively, resulting in a saddle-shaped fitness surface. Moreover, there were significant interactions between nest location, mean d2 and parasite load in the reduced analysis. The subsequent canonical rotation of the matrix of quadratic and cross-product terms identified two major axes of the response surface: a vector representing mostly nest site choice and a vector representing parasite load. These results imply that there exists more than one way for a male threespine stickleback to maximize its mating success and that such nonlinear relationships between male mating success induced by female mate choice and male characteristics might have been overlooked in many studies.     

A Paradox of Genetic Variance in Epigamic Traits: Beyond “Good Genes” View of Sexual Selection

Maintenance of genetic variance in secondary sexual traits, including bizarre ornaments and elaborated courtship displays, is a central problem of sexual selection theory. Despite theoretical arguments predicting that strong sexual selection leads to a depletion of additive genetic variance, traits associated with mating success show relatively high heritability. Here we argue that because of trade-offs associated with the production of costly epigamic traits, sexual selection is likely to lead to an increase, rather than a depletion, of genetic variance in those traits. Such trade-offs can also be expected to contribute to the maintenance of genetic variation in ecologically relevant traits with important implications for evolutionary processes, e.g. adaptation to novel environments or ecological speciation. However, if trade-offs are an important source of genetic variation in sexual traits, the magnitude of genetic variation may have little relevance for the possible genetic benefits of mate choice.     

Post-copulatory sexual selection and female fitness in Scathophaga stercoraria

Whether sexual selection increases or decreases female fitness is determined by the occurrence and relative importance of sexual-conflict processes and the ability of females to choose high-quality males. Experimentally enforced polyandry and monogamy have previously been shown to cause rapid evolution in the yellow dung fly Scathophaga stercoraria. Flies from polyandrous lines invested more in reproductive tissue, and this investment influenced paternity in sperm competition, but came at a cost to immune function. While some fitness consequences of enforced polyandry or monogamy have been examined when flies mate multiply, the consequences for female fitness when singly copulated remain unexplored. Under a good-genes scenario females from polyandrous lines should be of higher general quality and should outperform females from monogamous lines even with a single copulation. Under sexual conflict, costly adaptations will afford no advantages when females are allowed to mate only once. We investigate the lifetime reproductive success and longevity of females evolving under enforced monogamy or polyandry when mating once with males from these selection regimes. Females from polyandrous lines were found to have lower fitness than their monogamous counterparts when mating once. They died earlier and produced significantly fewer eggs and offspring. These results suggest that sexual conflict probably drove evolution under enforced polyandry as female fitness did not increase overall as expected with purely good-genes effects.     

SEXUAL SELECTION ACCELERATES THE ELIMINATION OF A DELETERIOUS MUTANT IN DROSOPHILA MELANOGASTER

Although theory indicates that indirect genetic benefits through mate choice should be widespread, empirical work has often either failed to detect the operation of such benefits or shown a net cost to the presence of sexual selection. We tested whether sexual selection can increase the speed with which a conditionally deleterious allele is removed from a laboratory population of Drosophila melanogaster. The alcohol dehydrogenase null allele ( Adh –) confers slightly lower viability than wild-type alleles in the absence of ethanol but is lethal in homozygotes when ethanol comprises 6% of the medium. We tracked the frequency of this allele in artificially constructed populations reared at three different levels of ethanol (0%, 2%, and 4%) that either experienced sexual selection or did not. Loss of the deleterious Adh – allele was more rapid when sexual selection was allowed to act, especially in the presence of ethanol. We also quantified the strength of both nonsexual and sexual selection against the Adh – allele using maximum-likelihood estimation. In contrast to recent experiments employing monogamy/polygamy designs, our results demonstrate a fitness benefit to sexual selection. This is consistent with the operation of good-genes female choice.     

Genetic and nutritional effects on male traits and reproductive performance in Tribolium flour beetles

In Tribolium flour beetles and other organisms, individuals migrate between heterogeneous environments where they often encounter markedly different nutritional conditions. Under these circumstances, theory suggests that genotype-by-environment interactions (GEI) may be important in facilitating adaptation to new environments and maintaining genetic variation for male traits subject to directional selection. Here, we used a nested half-sib breeding design with Tribolium castaneum to partition the separate and joint effects of male genotype and nutritional environment on phenotypic variation in a comprehensive suite of life-history traits, reproductive performance measures across three sequential sexual selection episodes, and fitness. When male genotypes were tested across three nutritional environments, considerable phenotypic plasticity was found for male mating and insemination success, longevity and traits related to larval development. Our results also revealed significant additive genetic variation for male mating rate, sperm offence ability (P(2)), longevity and total fitness and for several traits reflecting both larval and adult resource use. In addition, we found evidence supporting GEI for sperm defence ability (P(1)), adult longevity and larval development; thus, no single male genotype outperforms others in every nutritional environment. These results provide insight into the potential roles of phenotypic plasticity and GEI in facilitating Tribolium adaptation to new environments in ecological and evolutionary time.     

Sexual conflict and the evolution of female mate choice and male social dominance

Conflicts between the sexes over control of reproduction are thought to lead to a cost of sexual selection through the evolution of male traits that manipulate female reproductive physiology and behaviour, and female traits that resist this manipulation. Although studies have begun to document negative fitness effects of sexual conflict, studies showing the expected association between sexual conflict and the specific behavioural mechanisms of sexual selection are lacking. Here we experimentally manipulated the opportunity for sexual conflict in the cockroach. Nauphoeta cinerea and showed that, for this species, odour cues in the social environment influence the behavioural strategies and fitness of males and females during sexual selection. Females provided with the opportunity for discriminating between males but not necessarily mating with preferred males produced fewer male offspring than females mated at random. The number of female offspring produced was not affected, nor was the viability of the offspring. Experimental modification of the composition of the males' pheromone showed that the fecundity effects were caused by exposure to the pheromone component that makes males attractive to females but also makes males less likely to be dominant. Female mate choice therefore carries a demographic cost but functions to avoid male manipulation and aggression. Male-male competition appears to function to circumvent mate choice rather than directly manipulating females, as the mate choice can be cryptic. The dynamic struggle between the sexes for control of mating opportunities and outcomes in N. cinerea therefore reveals a unique role for sexual conflict in the evolution of the behavioural components of sexual selection.     

Effects of soil resources on expression of a sexual conflict over timing of stigma receptivity in a mixed‐mating plant

While environmental factors strongly influence plant growth and reproduction, less is known about environmental effects on sexual selection and sexual conflict. In this study on mixed‐mating Collinsia heterophylla we investigated whether soil resource environment affected traits associated with sexual conflict. In C. heterophylla a sexual conflict over timing of stigma receptivity occurs. Early stigma receptivity benefits pollen parents by securing paternity while late stigma receptivity benefits female fitness in terms of increased seed production. We performed hand‐pollinations combining recipients and donors grown either in high or low resource environments and asked whether these treatments influenced sexual conflict traits – recipient‐ and donor‐based influence on timing of stigma receptivity – and conflict costs related to reduced early seed production. We also asked whether resource environment affected eight traits related to general fitness and mating system. Sexual conflict‐associated traits – timing of stigma receptivity and seed production – were generally unaffected by resource environment. While no universal effect of resources was detected, we did observe donor‐specific responses to environment, suggesting that environment can nonetheless contribute to variation in timing of stigma receptivity. Recipients grown under low resources showed pronounced differences among donors for number of seeds per capsule, indicating that recipients favour some donors over others under resource‐low conditions. Moreover, high resources increased number of flowers but reduced pollen germination rate, while other traits were unaffected, indicating variation in the response to resource environment for fitness‐ and mating system‐traits. Our results suggest that even though soil resource environment had a low impact on the sexual conflict traits and related costs in C. heterophylla, it generated variability in pollen donor‐influence on this trait and in recipient sorting among donors. Thus, it is possible that both sexual conflict and sexual selection is affected by environmental factors not only in animals but also in plants.     

Host shifts and signal divergence: mating signals covary with host use in a complex of specialized plant‐feeding insects

A combination of divergent natural and sexual selection is a powerful cause of speciation. This conjunction of evolutionary forces may often occur when divergence is initiated by ecological differences between populations because local adaptation to new resources can lead to changes in sexual selection. The hypothesis that differences in resource use contribute to the evolution of reproductive isolation by altering the nature of sexual selection predicts that: (1) differences in sexual traits, such as signals and preferences, are an important source of reproductive isolation between species using different resources; (2) there are identifiable sources of selection on sexual traits that differ between species using different resources; and (3) signals vary between populations using different resources to a larger extent than between populations using the same resource at different localities. Testing these predictions requires a group of closely‐related species or populations that specialize on different resources and for which the traits involved in mate choice are known. The Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) are host plant specialists in which speciation is associated with shifts to novel host plants. Mating in this complex is preceded by an exchange of vibrational signals transmitted through host plant stems, and the signal traits important for mate choice have been identified. In the E. binotata complex, previous work has supported the first two predictions: (1) signal differences between species are important in mate recognition and (2) host shifts can alter both the trait values favoured by sexual selection and the evolutionary response to that selection. In the present study, we tested the last prediction by conducting a large‐scale study of mating signal variation within and between the 11 species in the complex. We find that differences in host use are strongly associated with differences in signal traits important for mate recognition. This result supports the hypothesis that hosts shifts have led to speciation in this group in part through their influence on divergence in mate communication systems. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 60–72.     

Female mate preferences for male body size and shape promote sexual isolation in threespine sticklebacks

Female mate preferences for ecologically relevant traits may enhance natural selection, leading to rapid divergence. They may also forge a link between mate choice within species and sexual isolation between species. Here, we examine female mate preference for two ecologically important traits: body size and body shape. We measured female preferences within and between species of benthic, limnetic, and anadromous threespine sticklebacks (Gasterosteus aculeatus species complex). We found that mate preferences differed between species and between contexts (i.e., within vs. between species). Within species, anadromous females preferred males that were deep bodied for their size, benthic females preferred larger males (as measured by centroid size), and limnetic females preferred males that were more limnetic shaped. In heterospecific mating trials between benthics and limnetics, limnetic females continued to prefer males that were more limnetic like in shape when presented with benthic males. Benthic females showed no preferences for size when presented with limnetic males. These results show that females use ecologically relevant traits to select mates in all three species and that female preference has diverged between species. These results suggest that sexual selection may act in concert with natural selection on stickleback size and shape. Further, our results suggest that female preferences may track adaptation to local environments and contribute to sexual isolation between benthic and limnetic sticklebacks.     

Sexual selection fails to promote adaptation to a new environment

Selection can be divided into sexual and nonsexual components. Some work finds that a component of sexual selection, adaptive female selection for good genes, can promote nonsexual fitness. Less studied is the benefit from sexual selection in toto, that is, when intra- and intersexual selection are both present and able to affect females directly and indirectly. Here an upper bound for the net benefit of sexual selection is estimated for Drosophila melanogaster. Replicate populations were allowed to adapt to low-grade thermal stress, with or with out the operation of sexual selection. Because proteins and lipids are highly sensitive to temperature, low-grade thermal stress will select broadly across the genome for alternative alleles. Such broad, directional selection for thermal tolerance should increase the measurable benefits of sexual selection far beyond that available under stabilizing selection. Sexual selection was removed by enforced monogamy without mate choice and retained by enforced polyandry (four males per female). After 36 generations of thermal stress exposure, there was substantial adaptation to the new environment (the net reproductive rate increased six standard deviations relative to thermal controls). However, sexual selection did not affect the rate of adaptation. Therefore, adaptive female selection for thermal tolerance either was insignificant or negated by other aspects of sexual selection, for example, male-induced female harm, which has been shown to diminish under monogamy. This experiment employed two parameters that reduced the opportunity for divergence in such harm: a truncated intersexual interaction period and strong directional selection for thermal tolerance. No divergence in male-induced harm was observed.     

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.     

Genetic variance of sexually selected traits in waxmoths: maintenance by genotype x environment interaction

When traits experience directional selection, such as that imposed by sexual selection, their genetic variance is expected to diminish. Nonetheless, theory and findings from sexual selection predict and demonstrate that male traits favored by female choice retain substantial amounts of additive genetic variance. We explored this dilemma through an ecological genetic approach and focused on the potential contributions of genotype x environment interaction (GEI) to maintenance of additive genetic variance for male signal characters in the lesser waxmoth, Achroia grisella (Lepidoptera: Pyralidae). We artificially selected genetic variants for two male signal characters, signal rate (SR) and peak amplitude (PA), that influence female attraction and then examined the phenotypic plasticity of these variants (high- and low-SR and high- and low-PA lines) under a range of environmental conditions expected in natural populations. Our split-family breeding experiments indicated that two signal characters, SR and PA, and several developmental characters in both high- and low-SR and high- and low-PA lines displayed considerable phenotypic plasticity among the environments tested. Moreover, strong GEIs leading to crossover between high- and low-SR lines were found for SR and developmental period. Therefore, neither high- nor low-SR genetic variants would achieve maximum attractiveness and fitness in every environment, and those variants producing unattractive signals with low SRs under normal conditions may remain in populations provided that gene flow across environments or generation overlap are sufficiently high. We speculate that the phenotypic plasticity for SR and developmental period is adaptive in A. grisella populations experiencing a range of temperature and density conditions. Females mating with attractive (high-SR) males may be assured of obtaining good genes because these males sire offspring that develop more rapidly and a crossover for developmental period may parallel that for SR. Such parallel crossovers may be expected wherever good-genes sexual selection mechanisms operate.