THE EFFECTS OF SELECTION AND GENETIC DRIFT ON THE GENOMIC DISTRIBUTION OF SEXUALLY ANTAGONISTIC ALLELES

Sexual antagonism (SA) occurs when an allele that is beneficial to one sex, is detrimental to the other. This conflict can result in balancing, directional, or disruptive selection acting on SA alleles. A body of theory predicts the conditions under which sexually antagonistic mutants will invade and be maintained in stable polymorphism under balancing selection. There remains, however, considerable debate over the distribution of SA genetic variation across autosomes and sex chromosomes, with contradictory evidence coming from data and theory. In this article, we investigate how the interplay between selection and genetic drift will affect the genomic distribution of sexually antagonistic alleles. The effective population sizes can differ between the autosomes and the sex chromosomes due to a number of ecological factors and, consequently, the distribution of SA genetic variation in genomes. In general, we predict the interplay of SA selection and genetic drift should lead to the accumulation of SA alleles on the X in male heterogametic (XY) species and, on the autosomes in female heterogametic (ZW) species, especially when sexual competition is strong among males.     

THE EVOLUTION OF XY RECOMBINATION: SEXUALLY ANTAGONISTIC SELECTION VERSUS DELETERIOUS MUTATION LOAD

Recombination arrest between X and Y chromosomes, driven by sexually antagonistic genes, is expected to induce their progressive differentiation. However, in contrast to birds and mammals (which display the predicted pattern), most cold‐blooded vertebrates have homomorphic sex chromosomes. Two main hypotheses have been proposed to account for this, namely high turnover rates of sex‐determining systems and occasional XY recombination. Using individual‐based simulations, we formalize the evolution of XY recombination (here mediated by sex reversal; the “fountain‐of‐youth” model) under the contrasting forces of sexually antagonistic selection and deleterious mutations. The shift between the domains of elimination and accumulation occurs at much lower selection coefficients for the Y than for the X. In the absence of dosage compensation, mildly deleterious mutations accumulating on the Y depress male fitness, thereby providing incentives for XY recombination. Under our settings, this occurs via “demasculinization” of the Y, allowing recombination in XY (sex‐reversed) females. As we also show, this generates a conflict with the X, which coevolves to oppose sex reversal. The resulting rare events of XY sex reversal are enough to purge the Y from its load of deleterious mutations. Our results support the “fountain of youth” as a plausible mechanism to account for the maintenance of sex‐chromosome homomorphy.     

THE INTERPLAY BETWEEN LOCAL ECOLOGY,DIVERGENT SELECTION,AND GENETIC DRIFT IN POPULATION DIVERGENCE OF A SEXUALLY ANTAGONISTIC FEMALE TRAIT

Genetically polymorphic species offer the possibility to study maintenance of genetic variation and the potential role for genetic drift in population divergence. Indirect inference of the selection regimes operating on polymorphic traits can be achieved by comparing population divergence in neutral genetic markers with population divergence in trait frequencies. Such an approach could further be combined with ecological data to better understand agents of selection. Here, we infer the selective regimes acting on a polymorphic mating trait in an insect group; the dorsal structures (either rough or smooth) of female diving beetles. Our recent work suggests that the rough structures have a sexually antagonistic function in reducing male mating attempts. For two species (Dytiscus lapponicus and Graphoderus zonatus), we could not reject genetic drift as an explanation for population divergence in morph frequencies, whereas for the third (Hygrotus impressopunctatus) we found that divergent selection pulls morph frequencies apart across populations. Furthermore, population morph frequencies in H. impressopunctatus were significantly related to local bioclimatic factors, providing an additional line of evidence for local adaptation in this species. These data, therefore, suggest that local ecological factors and sexual conflict interact over larger spatial scales to shape population divergence in the polymorphism.     

PERSPECTIVE: CHASE-AWAY SEXUAL SELECTION: ANTAGONISTIC SEDUCTION VERSUS RESISTANCE

A model of sexual selection that leads to the evolution of exaggerated male display characters that is based on antagonistic coevolution between the sexes is described. The model is motivated by three lines of research: intersexual conflict with respect to mating, sensory exploitation, and the evolution of female resistance, as opposed to preference, for male display traits. The model generates unique predictions that permit its operation to be distinguished from other established models of sexual selection. One striking prediction is that females will frequently win the coevolutionary arms race with males, leaving them encumbered with costly ornaments that have little value except that their absence understimulates females. Examples from the literature suggest that the model may have broad application in nature. The chase-away model is a special case of the more general phenomenon of Interlocus Contest Evolution (ICE).     

SEXUAL CONFLICT AND SEXUAL SELECTION: MEASURING ANTAGONISTIC COEVOLUTION

Abstract Arnqvist (2004) raises some concerns with several of the points made by Pizzari and Snook (2003) on the study of sexually antagonistic coevolution (SAC) generated by sexual conflict, arguing that: (1) sexual conflict cannot be expressed in terms of average male and female fitness; (2) our criticism of current experimental approaches, particularly interpopulation crosses, is unjustified; and (3) the alternative experimental approach we proposed is problematic. Here we discuss and respond to these criticisms by: (1) clarifying that we can distinguish between SAC and mutualistic sexual coevolution by measuring changes in the average fitness of the reproducing subsamples of males and females of a population across generations, (2) maintaining that testing SAC using interpopulation crosses is undermined by the lack of a priori knowledge of what traits mediate SAC across isolated populations, and (3) reinforcing the advantages of our experimental approach to distinguish between sexually mutualistic and antagonistic selection.     

SEX AND SPECIATION: GENETIC ARCHITECTURE AND EVOLUTIONARY POTENTIAL OF SEXUAL VERSUS NONSEXUAL TRAITS IN THE SIBLING SPECIES OF THE DROSOPHILA MELANOGASTER COMPLEX

Phenotypic divergence in the male reproductive system (genitalia and gonads) between species of the Drosophila melanogaster complex and their hybrids was quantified to decipher the role of these traits in species differentiation and speciation. Internal as well as external, sexual and nonsexual traits were analyzed with respect to genetic variation and trait asymmetry between strains within species, genetic divergence between species, and dominance and asymmetry in species and hybrids. The variation between strains within species was significant among sexual traits, and only external traits were less asymmetric than internal ones, which suggests that sexual traits are not strongly constrained within species. Three main findings show that sexual traits are most divergent between species: (1) testis length and area, and the area of the posterior lobe of the genital arch (sexual traits) showed the highest proportion of variation between species; (2) linear discriminant functions with the highest components associated to sexual traits were better predictors of species membership; and (3) testis length and area revealed a departure from a linear relationship between members of the species group. Examination of interspecific hybrids showed that sexual traits had higher asymmetry in species hybrids than in the parental species and that sexual traits showed additivity or dominance whereas nonsexual traits showed overdominance (with the exception of malpighian tubules length). These results suggest that sexual traits have undergone more genetic changes and, as a result, tend to show higher divergence and stronger hybrid breakdown between species than nonsexual traits. We propose that sexual selection in the broad sense, affecting all aspects of sexuality, may be responsible for the diversified appearance of sexual traits among closely related species and that the genetic architecture underlying sexual traits may be more prone to disruption during the early stages of speciation.     

THE EFFECTS OF THE RELATIVE GEOGRAPHIC SCALES OF GENE FLOW AND SELECTION ON MORPH FREQUENCIES IN THE WALKING-STICK TIMEMA CRISTINAE

Gene frequencies in large populations are determined by a balance between selection and gene flow between neighborhoods of different selection regimes. This balance is affected by the area of the patches of a given selection regime relative to the gene-flow distance. If patches are small relative to gene-flow distance, similarity in the total area occupied by different patch types is a crucial condition for the stability of polymorphisms. However, if patches are larger than the gene-flow distance, then the relative area of different patch types is less important because of reduced gene flow resulting from isolation by distance. Two morphs (striped and unstriped) of the walking-stick Timema cristinae were each strongly associated with patches of distinct species of food plants on which they are most cryptic. The frequency of a morph was high on the plant on which it is most cryptic when either: (1) the area occupied by the food plant (patch) was very large; (2) the patch was completely isolated from other patches; or (3) the patch was larger than adjacent patches. Results (1) and (2) are consistent with isolation-by-distance models, and result (3) is consistent with Levene's multiple-niche polymorphism model.     

SEX LINKAGE,SEX‐SPECIFIC SELECTION,AND THE ROLE OF RECOMBINATION IN THE EVOLUTION OF SEXUALLY DIMORPHIC GENE EXPRESSION

Sex‐biased genes—genes that are differentially expressed within males and females—are nonrandomly distributed across animal genomes, with sex chromosomes and autosomes often carrying markedly different concentrations of male‐ and female‐biased genes. These linkage patterns are often gene‐ and lineage‐dependent, differing between functional genetic categories and between species. Although sex‐specific selection is often hypothesized to shape the evolution of sex‐linked and autosomal gene content, population genetics theory has yet to account for many of the gene‐ and lineage‐specific idiosyncrasies emerging from the empirical literature. With the goal of improving the connection between evolutionary theory and a rapidly growing body of genome‐wide empirical studies, we extend previous population genetics theory of sex‐specific selection by developing and analyzing a biologically informed model that incorporates sex linkage, pleiotropy, recombination, and epistasis, factors that are likely to vary between genes and between species. Our results demonstrate that sex‐specific selection and sex‐specific recombination rates can generate, and are compatible with, the gene‐ and species‐specific linkage patterns reported in the genomics literature. The theory suggests that sexual selection may strongly influence the architectures of animal genomes, as well as the chromosomal distribution of fixed substitutions underlying sexually dimorphic traits.     

THE GENOMIC LOCATION OF SEXUALLY ANTAGONISTIC VARIATION: SOME CAUTIONARY COMMENTS

Sexually antagonistic polymorphisms are polymorphisms in which the allele that is advantageous in one sex is deleterious in the other sex. In an influential 1984 paper, W. Rice hypothesized that such polymorphisms should be relatively common on the X chromosome (or on the W in female‐heterogametic species) but relatively rare on the autosomes. Here, I show that there are plausible assumptions under which the reverse is expected to be true, and point out recent studies that give evidence for sexually antagonistic variation on the autosomes. Although more work is needed to resolve the issue, it is premature to conclude that the X chromosome is a “hot spot” for the accumulation of sexually antagonistic variation.     

THE GENOMIC ARCHITECTURE OF SEXUAL DIMORPHISM IN THE DIOECIOUS PLANT SILENE LATIFOLIA

Evaluating the genetic architecture of sexual dimorphism can aid our understanding of the extent to which shared genetic control of trait variation versus sex‐specific control impacts the evolutionary dynamics of phenotypic change within each sex. We performed a QTL analysis on Silene latifolia to evaluate the contribution of sex‐specific QTL to phenotypic variation in 46 traits, whether traits involved in trade‐offs had colocalized QTL, and whether the distribution of sex‐specific loci can explain differences between the sexes in their variance/covariance matrices. We used a backcross generation derived from two artificial‐selection lines. We found that sex‐specific QTL explained a significantly greater percent of the variation in sexually dimorphic traits than loci expressed in both sexes. Genetically correlated traits often had colocalized QTL, whose signs were in the expected direction. Lastly, traits with different genetic correlations within the sexes displayed a disproportionately high number of sex‐specific QTL, and more QTL co‐occurred in males than females, suggesting greater trait integration. These results show that sex differences in QTL patterns are congruent with theory on the resolution of sexual conflict and differences based on G ‐matrix results. They also suggest that trade‐offs and trait integration are likely to affect males more than females.     

GENETIC DIVERSITY IN THE MATRILINEAL WHALES: MODELS OF CULTURAL HITCHHIKING AND GROUP-SPECIFIC NON-HERITABLE DEMOGRAPHIC VARIATION

Cultural hitchhiking is the process by which cultural selection reduces the diversity of genes that are being transmitted in parallel to selective cultural traits. I use simulation models to investigate cultural hitchhiking in geographically unstructured populations of culturally homogeneous tribes. Substantial reduction of genetic diversity required: a reasonably low mutation rate; that tribes split fairly frequently when they constitute a substantial part of the population; a fairly low migration rate (<∼10 migrants per tribe per generation); only a low rate of cultural evolution (mean culturally determined fitness change >∼0.005%/ generation); and that cultural assimilation from other tribes change the fitness of a tribe less than cultural innovation within it. Cultural hitchhiking tends to increase mean tribe size. Measures of genetic and cultural variation among tribes poorly indicate past cultural hitchhiking. Demographic effects, in which tribal fitness varies but is not heritable, can also reduce a population's genetic diversity if the fitness varies very considerably, or tribal extirpation is added. In such cases populations frequently become extinct. Four species of matrilineal whales have remarkably low mitochondrial DNA diversity. Knowledge of the population and social structure of these species is consistent with the conditions for cultural hitchhiking. However, there remain important information gaps.     

A TEST AND REVIEW OF THE ROLE OF EFFECTIVE POPULATION SIZE ON EXPERIMENTAL SEXUAL SELECTION PATTERNS

Experimental evolution, particularly experimental sexual selection in which sexual selection strength is manipulated by altering the mating system, is an increasingly popular method for testing evolutionary theory. Concerns have arisen regarding genetic diversity variation across experimental treatments: differences in the number and sex ratio of breeders (effective population size; N_e ) and the potential for genetic hitchhiking, both of which may cause different levels of genetic variation between treatments. Such differences may affect the selection response and confound interpretation of results. Here we use both census-based estimators and molecular marker-based estimates to empirically test how experimental evolution of sexual selection in Drosophila pseudoobscura impacts N_e and autosomal genetic diversity. We also consider effects of treatment on X-linked N_e s, which have previously been ignored. Molecular autosomal marker-based estimators indicate that neither N_e nor genetic diversity differs between treatments experiencing different sexual selection intensities; thus observed evolutionary responses reflect selection rather than any confounding effects of experimental design. Given the increasing number of studies on experimental sexual selection, we also review the census N_e s of other experimental systems, calculate X-linked N_e , and compare how different studies have dealt with the issues of inbreeding, genetic drift, and genetic hitchhiking to help inform future designs.     

GEOGRAPHIC VARIATION, FREQUENCY-DEPENDENT SELECTION, AND THE MAINTENANCE OF A FEMALE-LIMITED POLYMORPHISM

A central problem in evolutionary biology is to understand how spatial and temporal variation in selection maintain genetic variation within and among populations. Brown anole lizards ( Anolis sagrei ) exhibit a dorsal pattern polymorphism that is expressed only in females, which occur in diamond,bar, and intermediate diamond-bar morphs. To understand the inheritance of this polymorphism, we conducted a captive breeding study that refuted several single-locus models and supported a two-locus mode of inheritance. To describe geographic variation in morph frequencies, we surveyed 13 populations from two major islands in The Bahamas. Morph frequencies differed substantially between major islands but were highly congruent within each island. Finally, we measured viability selection on each island to test two hypotheses regarding the maintenance of the polymorphism: (1) that spatial variation in selection maintains variation in morph frequencies between islands, and (2) that temporal variation in selection across years maintains variation within islands. Although bar females had relatively lower survival where they were rare, our data do not otherwise suggest that selection varies spatially between islands. However, diamond-bar females were subject to positive frequency-dependent selection across years, and the relative fitness of bar and diamond females alternated across years. We propose that this polymorphism is maintained by temporal variation in selection coupled with the sheltering of alleles via a two-locus inheritance pattern and sex-limited expression.     

MAINTENANCE OR LOSS OF GENETIC VARIATION UNDER SEXUAL AND PARENTAL ANTAGONISM AT A SEX-LINKED LOCUS

An intralocus genetic conflict occurs when a locus is selected in opposing directions in different subsets of a population. Populations with two sexes have the potential to host a pair of distinct intralocus conflicts: sexual antagonism and parental antagonism. In this article, we examine the population genetic consequences of these conflicts for X-linked genes. Both conflicts are capable of maintaining genetic variation in a population, but to different degrees. For weak sexual antagonism, the X chromosome has a higher opportunity for polymorphism than the autosomes. For parental antagonism, there is a very limited opportunity for polymorphism on the X chromosome relative to autosomes or to sexual antagonism. X-linkage introduces an asymmetry in the inheritance and expression of sexually and parentally antagonistic genes that leads to a biased fixation of alleles with certain effects. We find little support for the commonly held intuition that the X chromosome should be biased toward fixing female-beneficial alleles. Contrary to this intuition, we find that the X chromosome is biased toward fixation of male-beneficial alleles for much of the range of dominance. Additionally, we find that the X chromosome is more favorable to the fixation of alleles that are beneficial when maternally derived.     

THE ROLES OF LIFE‐HISTORY SELECTION AND SEXUAL SELECTION IN THE ADAPTIVE EVOLUTION OF MATING BEHAVIOR IN A BEETLE

Although there is continuing debate about whether sexual selection promotes or impedes adaptation to novel environments, the role of mating behavior in such adaptation remains largely unexplored. We investigated the evolution of mating behavior (latency to mating, mating probability and duration) in replicate populations of seed beetles Callosobruchus maculatus subjected to selection on life‐history (“Young” vs. “Old” reproduction) under contrasting regimes of sexual selection (“Monogamy” vs. “Polygamy”). Life‐history selection is predicted to favor delayed mating in “Old” females, but sexual conflict under polygamy can potentially retard adaptive life‐history evolution. We found that life‐history selection yielded the predicted changes in mating behavior, but sexual selection regime had no net effect. In within‐line crosses, populations selected for late reproduction showed equally reduced early‐life mating probability regardless of mating system. In between‐line crosses, however, the effect of life‐history selection on early‐life mating probability was stronger in polygamous lines than in monogamous ones. Thus, although mating system influenced male–female coevolution, removal of sexual selection did not affect the adaptive evolution of mating behavior. Importantly, our study shows that the interaction between sexual selection and life‐history selection can result in either increased or decreased reproductive divergence depending on the ecological context.     

RELATIVE ROLE OF GENETIC DETERMINATION AND PLASTIC RESPONSE DURING ONTOGENY FOR SHELL-SHAPE TRAITS SUBJECTED TO DIVERSIFYING SELECTION

We studied the relative role of genetic determination versus plastic response for traits involved in ecological adaptation of two ecotypes of Littorina saxatilis living at different shore levels. To investigate the magnitude of the plastic response across ontogeny, we compared morphological data from individuals grown in the laboratory and taken from the wild at three developmental stages: shelled embryos, juveniles, and adults. The results indicate that most shell shape variation (72–99%) in adaptive traits (globosity and aperture of the shell) is explained by the ecotype irrespective of the growth environment, suggesting that direct genetic determination is the main factor responsible for the process of adaptation in the wild. There was a tendency for the contribution of plasticity to increase over ontogeny but, in general, the direction of the plastic response did not suggest that this was adaptive.     

THE ACTION OF STABILIZING SELECTION,MUTATION, AND DRIFT ON EPISTATIC QUANTITATIVE TRAITS

For a quantitative trait under stabilizing selection, the effect of epistasis on its genetic architecture and on the changes of genetic variance caused by bottlenecking were investigated using theory and simulation. Assuming empirical estimates of the rate and effects of mutations and the intensity of selection, we assessed the impact of two‐locus epistasis (synergistic/antagonistic) among linked or unlinked loci on the distribution of effects and frequencies of segregating loci in populations at the mutation‐selection‐drift balance. Strong pervasive epistasis did not modify substantially the genetic properties of the trait and, therefore, the most likely explanation for the low amount of variation usually accounted by the loci detected in genome‐wide association analyses is that many causal loci will pass undetected. We investigated the impact of epistasis on the changes in genetic variance components when large populations were subjected to successive bottlenecks of different sizes, considering the action of genetic drift, operating singly (D), or jointly with mutation (MD) and selection (MSD). An initial increase of the different components of the genetic variance, as well as a dramatic acceleration of the between‐line divergence, were always associated with synergistic epistasis but were strongly constrained by selection.     

THE CONTRIBUTION OF MATERNAL EFFECTS TO SELECTION RESPONSE: AN EMPIRICAL TEST OF COMPETING MODELS

Maternal effects can dramatically influence the evolutionary process, in some cases facilitating and in others hindering adaptive evolution. Maternal effects have been incorporated into quantitative genetic models using two theoretical frameworks: the variance‐components approach, which partitions variance into direct and maternal components, and the trait‐based approach, which assumes that maternal effects are mediated by specific maternal traits. Here, we demonstrate parallels between these models and test their ability to predict evolutionary change. First, we show that the two approaches predict equivalent responses to selection in the absence of maternal effects mediated by traits that are themselves maternally influenced. We also introduce a correction factor that may be applied when such cascading maternal effects are present. Second, we use several maternal effect models, as well as the standard breeder's equation, to predict evolution in response to artificial selection on flowering time in American bellflower, Campanulastrum americanum. Models that included maternal effects made much more accurate predictions of selection response than the breeder's equation. Maternal effect models differed somewhat in their fit, with a version of the trait‐based model providing the best fit. We recommend fitting such trait‐based models when possible and appropriate to make the most accurate evolutionary predictions.