Sexual selection and genital evolution

Genitalia are conspicuously variable, even in closely related taxa that are otherwise morphologically very similar. Explaining genital diversity is a longstanding problem that is attracting renewed interest from evolutionary biologists. New studies provide ever more compelling evidence that sexual selection is important in driving genital divergence. Importantly, several studies now link variation in genital morphology directly to male fertilization success, and modern comparative techniques have confirmed predicted associations between genital complexity and mating patterns across species. There is also evidence that male and female genitalia can coevolve antagonistically. Determining mechanisms of genital evolution is an important challenge if we are to resolve current debate concerning the relative significance of mate choice benefits and sexual conflict in sexual selection.     

Sexual selection and the evolution of obligatory sex

Background  

Among the long-standing conundrums of evolutionary theory, obligatory sex is one of the hardest. Current theory suggests multiple factors that might explain the benefits of sex when compared with complete asexuality, but no satisfactory explanation for the prevalence of obligatory sex in the face of facultative sexual reproduction.     

Experimental evolution: experimental evolution and evolvability

The suggestion that there are characteristics of living organisms that have evolved because they increase the rate of evolution is controversial and difficult to study. In this review, we examine the role that experimental evolution might play in resolving this issue. We focus on three areas in which experimental evolution has been used previously to examine questions of evolvability; the evolution of mutational supply, the evolution of genetic exchange and the evolution of genetic architecture. In each case, we summarize what studies of experimental evolution have told us so far and speculate on where progress might be made in the future. We show that, while experimental evolution has helped us to begin to understand the evolutionary dynamics of traits that affect evolvability, many interesting questions remain to be answered.     

Sexual selection expedites the evolution of pesticide resistance

The evolution of insecticide resistance by crop pests and disease vectors causes serious problems for agriculture and health. Sexual selection can accelerate or hinder adaptation to abiotic challenges in a variety of ways, but the effect of sexual selection on resistance evolution is little studied. Here, we examine this question using experimental evolution in the pest insect Tribolium castaneum. The experimental removal of sexual selection slowed the evolution of resistance in populations treated with pyrethroid pesticide, and also reduced the rate at which resistance was lost from pesticide‐free populations. These results suggest that selection arising from variance in mating and fertilization success can augment natural selection on pesticide resistance, meaning that sexual selection should be considered when designing strategies to limit the evolution of pesticide resistance.     

Sexual selection effects on the evolution of senescence

Although the basic theories concerning evolution of senescence have been generally accepted for a half-century, interpretation of this paradigm has been constrained by an over-reliance on mortality as both the cause and the measure of senescence. Consideration of both survival and fecundity as components of reproductive value, and integration of sexual selection theory with senescence theory allows reconciliation of long-standing, as well as recent, discrepancies between data and theory. This approach demonstrates that sexual selection on males in polygynous mating systems can have significant effects on the evolution of senescence that could overshadow the selection effects of mortality rates among such animals.     

The role of epistatic gene interactions in the response to selection and the evolution of evolvability

It has been argued that the architecture of the genotype-phenotype map determines evolvability, but few studies have attempted to quantify these effects. In this article we use the multilinear epistatic model to study the effects of different forms of epistasis on the response to directional selection. We derive an analytical prediction for the change in the additive genetic variance, and use individual-based simulations to understand the dynamics of evolvability and the evolution of genetic architecture. This shows that the major determinant for the evolution of the additive variance, and thus the evolvability, is directional epistasis. Positive directional epistasis leads to an acceleration of evolvability, while negative directional epistasis leads to canalization. In contrast, pure non-directional epistasis has little effect on the response to selection. One consequence of this is that the classical epistatic variance components, which do not distinguish directional and non-directional effects, are useless as predictors of evolutionary dynamics. The build-up of linkage disequilibrium also has negligible effects. We argue that directional epistasis is likely to have major effects on evolutionary dynamics and should be the focus of empirical studies of epistasis.     

The mutation matrix and the evolution of evolvability

Evolvability is a key characteristic of any evolving system, and the concept of evolvability serves as a unifying theme in a wide range of disciplines related to evolutionary theory. The field of quantitative genetics provides a framework for the exploration of evolvability with the promise to produce insights of global importance. With respect to the quantitative genetics of biological systems, the parameters most relevant to evolvability are the G-matrix, which describes the standing additive genetic variances and covariances for a suite of traits, and the M-matrix, which describes the effects of new mutations on genetic variances and covariances. A population's immediate response to selection is governed by the G-matrix. However, evolvability is also concerned with the ability of mutational processes to produce adaptive variants, and consequently the M-matrix is a crucial quantitative genetic parameter. Here, we explore the evolution of evolvability by using analytical theory and simulation-based models to examine the evolution of the mutational correlation, r(mu), the key parameter determining the nature of genetic constraints imposed by M. The model uses a diploid, sexually reproducing population of finite size experiencing stabilizing selection on a two-trait phenotype. We assume that the mutational correlation is a third quantitative trait determined by multiple additive loci. An individual's value of the mutational correlation trait determines the correlation between pleiotropic effects of new alleles when they arise in that individual. Our results show that the mutational correlation, despite the fact that it is not involved directly in the specification of an individual's fitness, does evolve in response to selection on the bivariate phenotype. The mutational variance exhibits a weak tendency to evolve to produce alignment of the M-matrix with the adaptive landscape, but is prone to erratic fluctuations as a consequence of genetic drift. The interpretation of this result is that the evolvability of the population is capable of a response to selection, and whether this response results in an increase or decrease in evolvability depends on the way in which the bivariate phenotypic optimum is expected to move. Interestingly, both analytical and simulation results show that the mutational correlation experiences disruptive selection, with local fitness maxima at -1 and +1. Genetic drift counteracts the tendency for the mutational correlation to persist at these extreme values, however. Our results also show that an evolving M-matrix tends to increase stability of the G-matrix under most circumstances. Previous studies of G-matrix stability, which assume nonevolving M-matrices, consequently may overestimate the level of instability of G relative to what might be expected in natural systems. Overall, our results indicate that evolvability can evolve in natural systems in a way that tends to result in alignment of the G-matrix, the M-matrix, and the adaptive landscape, and that such evolution tends to stabilize the G-matrix over evolutionary time.     

Sexual selection and the adaptive evolution of mammalian ejaculate proteins

An elevated rate of substitution characterizes the molecular evolution of reproductive proteins from a wide range of taxa. Although the selective pressures explaining this rapid evolution are yet to be resolved, recent evidence implicates sexual selection as a potentially important explanatory factor. To investigate this hypothesis, we sought evidence of a high rate of adaptive gene evolution linked to postcopulatory sexual selection in muroid rodents, a model vertebrate group displaying a broad range of mating systems. Specifically, we sequenced 7 genes from diverse rodents that are expressed in the testes, prostate, or seminal vesicles, products of which have the potential to act in sperm competition. We inferred positive Darwinian selection in these genes by estimation of the ratio of nonsynonymous (d(N), amino acid changing) to synonymous (d(S), amino acid retaining) substitution rates (omega = d(N)/d(S)). Next, we tested whether variation in this ratio among lineages could be attributed to interspecific variation in mating systems, as inferred from the variation in these rodents' relative testis sizes (RTS). Four of the 7 genes examined (Prm1, Sva, Acrv1, and Svs2, but not Svp2, Msmb, or Spink3) exhibit unambiguous evidence of positive selection. One of these, the seminal vesicle-derived protein Svs2, also shows some evidence for a concentration of positive selection in those lineages in which sperm competition is common. However, this was not a general trend among all the rodent genes we examined. Using the same methods, we then reanalyzed previously published data on 2 primate genes, SEMG1 and SEMG2. Although SEMG2 also shows evidence of positive selection concentrated in lineages subject to high levels of sperm competition, no such trend was found for SEMG1. Overall, despite a high rate of positive selection being a feature of many ejaculate proteins, these results indicate that the action of sexual selection potentially responsible for elevated evolutionary rates may be difficult to detect on a gene-by-gene basis. Although the extreme diversity of reproductive phenotypes exhibited in nature attests to the power of sexual selection, the extent to which this force predominates in driving the rapid molecular evolution of reproductive genes therefore remains to be determined.     

Sexual selection and the evolution of beauty: two views

This is a review of Ryan’s A Taste for the Beautiful and Prum’s The Evolution of Beauty, two books that show how sexual selection by female choice can favor the evolution of beauty.     

Sexual selection and the evolution of sperm morphology in sharks

Post‐copulatory sexual selection, and sperm competition in particular, is a powerful selective force shaping the evolution of sperm morphology. Although mounting evidence suggests that post‐copulatory sexual selection influences the evolution of sperm morphology among species, recent evidence also suggests that sperm competition influences variation in sperm morphology at the intraspecific level. However, contradictory empirical results and limited taxonomic scope have led to difficulty in assessing the generality of sperm morphological responses to variation in the strength of sperm competition. Here, we use phylogenetically controlled analyses to explore the effects of sperm competition on sperm morphology and variance in sharks, a basal vertebrate group characterized by wide variation in rates of multiple mating by females, and consequently sperm competition risk. Our analyses reveal that shark species experiencing greater levels of sperm competition produce sperm with longer flagella and that sperm flagellum length is less variable in species under higher sperm competition risk. In contrast, neither the length of the sperm head and midpiece nor variation in sperm head and midpiece length was associated with sperm competition risk. Our findings demonstrate that selection influences both the inter‐ and intraspecific variation in sperm morphology and suggest that the flagellum is an important target of sexual selection in sharks. These findings provide important insight into patterns of selection on the ejaculate in a basal vertebrate lineage.     

Mosaic evolution,preadaptation, and the evolution of evolvability in apes

A major goal in postsynthesis evolutionary biology has been to better understand how complex interactions between traits drive movement along and facilitate the formation of distinct evolutionary pathways. I present analyses of a character matrix sampled across the haplorrhine skeleton that revealed several modules of characters displaying distinct patterns in macroevolutionary disparity. Comparison of these patterns to those in neurological development showed that early ape evolution was characterized by an intense regime of evolutionary and developmental flexibility. Shifting and reduced constraint in apes was met with episodic bursts in phenotypic innovation that built a wide array of functional diversity over a foundation of shared developmental and anatomical structure. Shifts in modularity drove dramatic evolutionary changes across the ape body plan in two distinct ways: (1) an episode of relaxed integration early in hominoid evolution coincided with bursts in evolutionary rate across multiple character suites; (2) the formation of two new trait modules along the branch leading to chimps and humans preceded rapid and dramatic evolutionary shifts in the carpus and pelvis. Changes to the structure of evolutionary mosaicism may correspond to enhanced evolvability that has a “preadaptive” effect by catalyzing later episodes of dramatic morphological remodeling.     

Sexual selection and the evolution of exclusive paternal care in arthropods

Internal fertilization and anisogamy are thought to impede the evolution of exclusive paternal care by reducing paternity assurance and increasing male promiscuity. The potential role of sexual selection in easing these constraints is currently being examined in vertebrates but has not been seriously studied in most arthropods. To distinguish the effects of sexual from natural selection on the evolution of arthropod paternal care, I tested predictions of the state of several life history and behavioural traits under both forms of selection across all known taxa with exclusive paternal care. The results suggest parallels between prezygotic nuptial gifts and exclusive postzygotic paternal care and support the hypothesis that, in arthropods, male behaviours that enhance female reproductive success either directly by releasing females from the fecundity constraints of maternal care (enhanced fecundity hypothesis) or indirectly by identifying mates with superior genes (handicap principle) are traits on which sexual selection has acted. Under such conditions males willing to guard young become preferred mates for gravid females and enjoy greater promiscuity than males unable or unwilling to guard. Females use nest construction or the act of guarding another female's eggs as honest signals of paternal intent and quality. Copyright 2000 The Association for the Study of Animal Behaviour.     

Response to selection and evolvability of invasive populations

While natural selection might in some cases facilitate invasions into novel habitats, few direct measurements of selection response exist for invasive populations. This study examined selection response to changes in salinity using the copepod Eurytemora affinis. This copepod has invaded fresh water from saline habitats multiple times independently throughout the Northern Hemisphere. Selection response to a constant intermediate salinity (5 PSU) was measured in the laboratory for saline source and freshwater invading populations from the St. Lawrence drainage (North America). These populations were reared under three conditions: (1) native salinities (0 or 15 PSU) for at least two generations, (2) 5 PSU for two generations, and (3) 5 PSU for six generations. Full-sib clutches taken from populations reared under these three conditions were split across four salinities (0, 5, 15, and 25 PSU) to determine reaction norms for survival and development time. Contrasts in survival and development time across the three rearing conditions were treated as the selection response. Selection at 5 PSU resulted in a significant decline in freshwater (0 PSU) tolerance for both the saline and freshwater populations. Yet, evolutionary differences in freshwater tolerance persisted between the saline and freshwater populations. The saline and freshwater populations converged in their high-salinity (25 PSU) tolerance, with an increase in the freshwater population and decline in the saline population. Development time did not shift greatly in response to selection at 5 PSU. For all three rearing conditions, the freshwater population exhibited retarded larval development and accelerated juvenile development relative to the saline population. Results from this study indicate that both the saline and freshwater populations exhibit significant responses to selection for a fitness-related trait critical for invasions into a novel habitat. For the Symposium on “Evolvability and Adaptation of Invasive Species,” Society for the Study of Evolution 2004.     

Sexual selection drives the evolution of antiaphrodisiac pheromones in butterflies

Competition for mates has resulted in sophisticated mechanisms of male control over female reproduction. Antiaphrodisiacs are pheromones transferred from males to females during mating that reduce attractiveness of females to subsequent courting males. Antiaphrodisiacs generally help unreceptive females reduce male harassment. However, lack of control over pheromone release by females and male control over the amount transferred provides males an opportunity to use antiaphrodisiacs to delay remating by females that have returned to a receptive state. We propose a model for the evolution of antiaphrodisiacs under the influence of intrasexual selection, and determine whether changes in this signal in 11 species of Heliconius butterflies are consistent with two predictions of the model. First, we find that as predicted, male-contributed chemical mixtures are complex and highly variable across species, with limited phylogenetic signal. Second, differences in rates of evolution in pheromone composition between two major clades of Heliconius are as expected: the clade with a greater potential for male-male competition (polyandrous) shows a faster rate of divergence than the one with typically monoandrous mating system. Taken together, our results provide evidence that for females, antiaphrodisiacs can be both honest signals of receptivity (helping reduce harassment) and chastity belts (a male-imposed reduction in remating).     

Sexual selection and the evolution of secondary sexual traits: sex comb evolution in Drosophila

Sexual selection can drive rapid evolutionary change in reproductive behaviour, morphology and physiology. This often leads to the evolution of sexual dimorphism, and continued exaggerated expression of dimorphic sexual characteristics, although a variety of other alternative selection scenarios exist. Here, we examined the evolutionary significance of a rapidly evolving, sexually dimorphic trait, sex comb tooth number, in two Drosophila species. The presence of the sex comb in both D. melanogaster and D. pseudoobscura is known to be positively related to mating success, although little is yet known about the sexually selected benefits of sex comb structure. In this study, we used experimental evolution to test the idea that enhancing or eliminating sexual selection would lead to variation in sex comb tooth number. However, the results showed no effect of either enforced monogamy or elevated promiscuity on this trait. We discuss several hypotheses to explain the lack of divergence, focussing on sexually antagonistic coevolution, stabilizing selection via species recognition and nonlinear selection. We discuss how these are important, but relatively ignored, alternatives in understanding the evolution of rapidly evolving sexually dimorphic traits.     

Sexual selection, natural selection and the evolution of dimorphic coloration and ornamentation in agamid lizards

Both sexual selection and natural selection can influence the form of dimorphism in secondary sexual traits. Here, we used a comparative approach to examine the relative roles of sexual selection and natural selection in the evolution of sexually dimorphic coloration (dichromatism) and ornamentation in agamid lizards. Sexual dimorphism in head and body size were used as indirect indicators of sexual selection, and habitat type (openness) as an index of natural selection. We examined separately the dichromatism of body regions "exposed to" and "concealed from" visual predators, because these body regions are likely to be subject to different selection pressures. Dichromatism of "exposed" body regions was significantly associated with habitat type: males were typically more conspicuously coloured than females in closed habitats. By contrast, dichromatism of "concealed" body regions and ornament dimorphism were positively associated with sexual size dimorphism (SSD). When we examined male and female ornamentation separately, however, both were positively associated with habitat openness in addition to snout-vent length and head SSD. These results suggest that natural selection constrains the evolution of elaborate ornamentation in both sexes as well as sexual dichromatism of body regions exposed to visual predators. By contrast, dichromatism of "concealed" body regions and degree of ornament dimorphism appear to be driven to a greater degree by sexual selection.     

Sexual selection uncouples the evolution of brain and body size in pinnipeds

The size of the vertebrate brain is shaped by a variety of selective forces. Although larger brains (correcting for body size) are thought to confer fitness advantages, energetic limitations of this costly organ may lead to trade-offs, for example as recently suggested between sexual traits and neural tissue. Here, we examine the patterns of selection on male and female brain size in pinnipeds, a group where the strength of sexual selection differs markedly among species and between the sexes. Relative brain size was negatively associated with the intensity of sexual selection in males but not females. However, analyses of the rates of body and brain size evolution showed that this apparent trade-off between sexual selection and brain mass is driven by selection for increasing body mass rather than by an actual reduction in male brain size. Our results suggest that sexual selection has important effects on the allometric relationships of neural development.     

Sexual selection and the evolution of costly female preferences: spatial effects

Abstract.— Models of Fisher's runaway process show that if there is a cost to female preference, no preference or male trait exaggeration will evolve. Surprisingly, this is true no matter how small the cost, which reveals that these models of Fisher's process are structurally unstable (Bulmer 1989). Here a model of Fisher's runaway process is presented to demonstrate that costly female preference evolves very easily when space is explicitly included in the model. The only requirement is that the optimal male phenotype changes across the species' range. The model shows that the spatial average of the female preference and male trait reach an evolutionary equilibrium that is identical to those of nonspatial models, but that the preference and male trait can deviate greatly from these averages at any point in space. For example, if random mating results in the lowest cost to females, then at equilibrium the spatial average preference will be zero. Nevertheless, there will be some locations at which females prefer males with larger ornaments and others where they prefer males with smaller ornaments. Results also show that the structural instability of nonspatial models of Fisher's process is less of a problem in spatial models. In particular, many of the main qualitative features of cost-free spatial models of Fisher's process remain valid even when there are small costs of female preference. Finally, the model shows that abrupt changes in the optimal male phenotype across space can result in an amplification of this pattern when preference has a small cost, but it can also result in a pattern similar to reproductive character displacement. Which of these occurs depends on the magnitude of the cost of female preference. This suggests that some patterns of reproductive character displacement in nature might be explained simply by sexual selection rather than by hybrid dysgenesis and reinforcement.