The depletion of genetic variance by sexual selection

Sexually selected traits display substantial genetic variance [1, 2], in conflict with the expectation that sexual selection will deplete it [3-5]. Condition dependence is thought to resolve this paradox [5-7], but experimental tests that relate the direction of sexual selection to the availability of genetic variance are lacking. Here, we show that condition-dependent expression is not sufficient to maintain genetic variance available to sexual selection in multiple male sexually selected traits. We employed an experimental design that simultaneously determined the quantitative genetic basis of nine male cuticular hydrocarbons (CHCs) of Drosophila bunnanda, the extent of condition dependence of these traits, and the strength and direction of sexual selection acting upon them. The CHCs of D. bunnanda are condition dependent, with 18% of the genetic variance in male body size explained by genetic variance in CHCs. Despite the presence of genetic variance in individual male traits, 98% of the genetic variance in CHCs was found to be orientated more than 88 degrees away from the direction of sexual selection and therefore unavailable to selection. A lack of genetic variance in male traits in the direction of sexual selection may represent a general feature of sexually selected systems, even in the presence of condition-dependent trait expression.     

Genetic divergence does not predict change in ornament expression among populations of stalk-eyed flies

Stalk-eyed flies (Diptera: Diopsidae) possess eyes at the ends of elongated peduncles, and exhibit dramatic variation in eye span, relative to body length, among species. In some sexually dimorphic species, evidence indicates that eye span is under both intra- and intersexual selection. Theory predicts that isolated populations should evolve differences in sexually selected traits due to drift. To determine if eye span changes as a function of divergence time, 1370 flies from 10 populations of the sexually dimorphic species, Cyrtodiopsis dalmanni and Cyrtodiopsis whitei, and one population of the sexually monomorphic congener, Cyrtodiopsis quinqueguttata, were collected from Southeast Asia and measured. Genetic differentiation was used to assess divergence time by comparing mitochondrial (cytochrome oxidase II and 16S ribosomal RNA gene fragments) and nuclear (wingless gene fragment) DNA sequences for c. five individuals per population. Phylogenetic analyses indicate that most populations cluster as monophyletic units with up to 9% nucleotide substitutions between populations within a species. Analyses of molecular variance suggest a high degree of genetic structure within and among the populations; > 97% of the genetic variance occurs between populations and species while < 3% is distributed within populations, indicating that most populations have been isolated for thousands of years. Nevertheless, significant change in the allometric slope of male eye span on body length was detected for only one population of either dimorphic species. These results are not consistent with genetic drift. Rather, relative eye span appears to be under net stabilizing selection in most populations of stalk-eyed flies. Given that one population exhibited dramatic evolutionary change, selection, rather than genetic variation, appears to constrain eye span evolution.     

Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis?

The handicap hypothesis of sexual selection predicts that sexual ornaments have evolved heightened condition-dependent expression. The prediction has only recently been subject to experimental investigation. Many of the experiments are of limited value as they: (i) fail to compare condition dependence in sexual ornaments with suitable non-sexual trait controls; (ii) do not adequately account for body size variation; and (iii) typically consider no stress and extreme stress manipulations rather than a range of stresses similar to those experienced in nature. There is also a dearth of experimental studies investigating the genetic basis of condition dependence. Despite the common claim that sexual ornaments are condition-dependent, the unexpected conclusion from our literature review is that there is little support from well-designed experiments.     

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

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

On the evolution of heightened condition dependence of male sexual displays

The maintenance of genetic variation in male sexual display traits in the face of strong directional sexual selection from female preferences is an ongoing evolutionary conundrum. Condition dependence and the genic capture hypothesis are often cited as theoretical resolutions to this problem, yet little is known about the ability of condition dependence itself to evolve. We set out to test how a suite of cuticular hydrocarbons (CHCs) used in sexual displays are affected by adult diet and the potential for any condition-dependent response to evolve in a laboratory-adapted population of the Australian fruit fly Drosophila serrata. We performed a dietary manipulation within a half-sib breeding design, raising adult males either with or without access to live yeast, a manipulation that had previously shown strong effects on female fitness. Diet had strong phenotypic effects, with males from the different diets producing different CHC blends. The blend of CHCs under sexual selection showed a degree of elevated condition dependence. Regardless of the heightened sensitivity of favoured CHC blends to diet and the presence of genetic variance for the traits, we were unable to detect any genetic variance in the reaction norms for the male dietary response. Our results suggest that there is limited opportunity for males to evolve further condition dependence in response to yeast availability in this population.     

Condition dependence and the maintenance of genetic variance in a sexually dimorphic black scavenger fly

The maintenance of genetic variation in traits under strong sexual selection is a longstanding problem in evolutionary biology. The genic capture model proposes that this problem can be explained by the evolution of condition dependence in exaggerated male traits. We tested the predictions that condition dependence should be more pronounced in male sexual traits and that genetic variance in expression of these traits should increase under stress as among‐genotype variation in overall condition is exposed. Genetic variance in female and nonsexual traits should, by contrast, be similar across environments as a result of stabilizing selection on trait expression. The relationship between the degree of sexual dimorphism, condition dependence and additive genetic variance (V_a) was assessed for two morphological traits (body size and relative fore femur width) affecting male mating success in the black scavenger fly Sepsis punctum (Diptera: Sepsidae) and for development time (a nonsexual trait often correlated with body size). We compared trait expression between the sexes for two cross‐continental populations that differ in degree of sexual dimorphism (Ottawa and Zurich). Condition dependence was indeed most pronounced in males of the strongly dimorphic Zurich population (males larger), and V_a was similar for males and females unless the trait was strongly sex specific and condition dependent. Contrary to prediction, however, V_a primarily increased under food limitation in both sexes, and genetic variance in fore femur width was low to nil, perhaps depleted by putatively strong sexual selection. Solely for body size of Zurich males, V_a increased more in males than females at limited food, in accordance with the predictions of the genic capture model. Overall therefore, quantitative genetic evidence in support of the model was inconsistent and weak at best.     

Variation in preference for a male ornament is positively associated with female eyespan in the stalk-eyed fly Diasemopsis meigenii

There is currently much interest in mate preferences for sexual ornaments. However, few studies have focused on individual variation in mate preference despite its importance for the rate and direction of sexual selection. Females of the sexually dimorphic stalk-eyed fly, Diasemopsis meigenii, exhibit an unambiguous rejection response towards unattractive males bearing small ornaments. We investigated individual mate preferences using repeated sequential sampling of female rejection or acceptance responses to a wide range of male ornament phenotypes. We found significant variation in the strength of individual preference. In addition, preference was positively associated with female eyespan, a condition-dependent trait putatively linked to visual acuity.     

Multivariate quantitative genetics and the lek paradox: genetic variance in male sexually selected traits of Drosophila serrata under field conditions

Single male sexually selected traits have been found to exhibit substantial genetic variance, even though natural and sexual selection are predicted to deplete genetic variance in these traits. We tested whether genetic variance in multiple male display traits of Drosophila serrata was maintained under field conditions. A breeding design involving 300 field-reared males and their laboratory-reared offspring allowed the estimation of the genetic variance-covariance matrix for six male cuticular hydrocarbons (CHCs) under field conditions. Despite individual CHCs displaying substantial genetic variance under field conditions, the vast majority of genetic variance in CHCs was not closely associated with the direction of sexual selection measured on field phenotypes. Relative concentrations of three CHCs correlated positively with body size in the field, but not under laboratory conditions, suggesting condition-dependent expression of CHCs under field conditions. Therefore condition dependence may not maintain genetic variance in preferred combinations of male CHCs under field conditions, suggesting that the large mutational target supplied by the evolution of condition dependence may not provide a solution to the lek paradox in this species. Sustained sexual selection may be adequate to deplete genetic variance in the direction of selection, perhaps as a consequence of the low rate of favorable mutations expected in multiple trait systems.     

Evolutionary dynamics of a sexual ornament in the house sparrow (Passer domesticus): the role of indirect selection within and between sexes

The relative contribution of sexual and natural selection to evolution of sexual ornaments has rarely been quantified under natural conditions. In this study we used a long-term dataset of house sparrows in which parents and offspring were matched genetically to estimate the within- and across-sex genetic basis for variation and covariation among morphological traits. By applying two-sex multivariate "animal models" to estimate genetic parameters, we estimated evolutionary changes in a male sexual ornament, badge size, from the contribution of direct and indirect selection on correlated traits within males and females, after accounting for overlapping generations and age-structure. Indirect natural selection on genetically correlated traits in males and females was the major force causing evolutionary change in the male ornament. Thus, natural selection on female morphology may cause indirect evolutionary changes in male ornaments. We observed however no directional phenotypic change in the ornament size of one-year-old males during the study period. On the other hand, changes were recorded in other morphological characters of both sexes. Our analyses of evolutionary dynamics in sexual characters require application of appropriate two-sex models to account for how selection on correlated traits in both sexes affects the evolutionary outcome of sexual selection.     

Sexual selection and immune function in Drosophila melanogaster

The evolution of immune function depends not only on variation in genes contributing directly to the immune response, but also on genetic variation in other traits indirectly affecting immunocompetence. In particular, sexual selection is predicted to trade-off with immunocompetence because the extra investment of resources needed to increase sexual competitiveness reduces investment in immune function. Additional possible immunological consequences of intensifying sexual selection include an exaggeration of immunological sexual dimorphism, and the reduction of condition-dependent immunological costs due to selection of 'good genes' (the immunocompetence handicap hypothesis, ICHH). We tested for these evolutionary possibilities by increasing sexual selection in laboratory populations of Drosophila melanogaster for 58 generations by reestablishing a male-biased sex ratio at the start of each generation. Sexually selected flies were larger, took longer to develop, and the males were more sexually competitive than males from control (equal sex ratio) lines. We found support for the trade-off hypothesis: sexually selected males were found to have reduced immune function compared to control males. However, we found no evidence that sexual selection promoted immunological sexual dimorphism because females showed a similar reduction in immune function. We found no evidence of evolutionary changes in the condition-dependent expression of immunocompetence contrary to the expectations of the ICHH. Lastly, we compared males from the unselected base population that were either successful (IS) or unsuccessful (IU) in a competitive mating experiment. IS males showed reduced immune function relative to IU males, suggesting that patterns of phenotypic correlation largely mirror patterns of genetic correlation revealed by the selection experiment. Our results suggest increased disease susceptibility could be an important cost limiting increases in sexual competitiveness in populations experiencing intense sexual selection. Such costs may be particularly important given the high intersex correlation, because this represents an apparent genetic conflict, preventing males from reaching their sexually selected optimum.     

The evolution of condition-dependent sexual dimorphism

Theory suggests that the net benefit of allocating resources to a sexual trait depends both on the strength of sexual selection on that trait and on individual condition. This predicts a tight coevolution between sexual dimorphism and condition dependence and suggests that these patterns of within-sex and between-sex variation may share a common genetic and developmental basis. Although condition-dependent expression of sexual traits is widely documented, the extent of covariation between condition dependence and sexual dimorphism remains poorly known. I investigated the effects of condition (larval diet quality) on multivariate sexual dimorphism in the fly Telostylinus angusticollis (Neriidae). Condition determined the direction of sexual size dimorphism and modulated sexual shape dimorphism by affecting allometric slopes and/or intercepts of sexually homologous traits in both sexes. Although the greatest responses to condition manipulation were observed in male sexual traits, both sexual and nonsexual traits exhibited substantial variation in the nature and magnitude of condition effects. Nonetheless, condition dependence and sexual dimorphism were remarkably congruent: variation in the strength of condition effects on male traits explained more than 90% of the variation in the magnitude of sexual dimorphism, whether quantified in terms of trait size or allometric slope. The genetic mechanisms that give rise to multivariate sexual dimorphism in body shape thus function in a strongly condition-dependent manner in this species, suggesting a common genetic basis for body shape variation within and between sexes.     

Variable sexual ornaments in scarlet-tufted malachite sunbirds (Nectarinia johnstoni) on Mount Kenya

In order to be elaborated by sexual selection, sexual ornaments must vary perceptibly and genetically among individuals in natural populations. Rather little is known about ornament variation in monogamous species, in which sexual selection should act more weakly than in polygynous species. We report phenotypic variation in feather ornament size (elongated tails and pectoral tufts) and body size in the scarlet-tufted malachite sunbird Nectarinia johnstoni , a monogamous, sexually dimorphic nectarivore of East African alpine zones. Fully-expressed male ornaments are highly significantly more variable (CVs = 12–29%) than are skeletal and wing measures primarily affected by natural selection (CVs = 2 4%). Female sunbirds have pectoral tufts which are significantly (22–25%) smaller than those of adult males, but more variable (CV_s= 21–22%, CV_s= 12–15%), and more variable than body size. Among males with fully-grown ornaments, those with longer tails tend to have longer wings and wider tufts. The high variation in fully-grown ornaments in malachite sunbirds is consistent with the view that the ornaments are condition-dependent sexual signals. Finally, we review studies of feather ornament variation to date, and show that ornaments are much more variable in monogamous than non-monogamous species, apparently due to the relatively weak pressure of sexual selection.     

Pleiotropy and the genomic location of sexually selected genes

Sexual selection drives the evolution of traits involved in the competition for mates. Although considerable research has focused on the evolution of sexually selected traits, their underlying genetic architecture is poorly resolved. Here I address the pleiotropic effects and genomic locations of sexually selected genes. These two important characteristics can impose considerable constraints on evolvability and may influence our understanding of the process of sexual selection. Theoretical models are inconsistent regarding the genomic location of sexually selected genes. Models that do not incorporate pleiotropic effects often predict sex linkage. Conversely, sex linkage is not explicitly predicted by the condition-dependent model (which considers pleiotropic effects). Evidence largely based on reciprocal crosses supports the notion of sex linkage. However, although they infer genetic contribution, reciprocal crosses cannot identify the genes or their pleiotropic effects. By surveying the genome of Drosophila melanogaster, I provide evidence for the genomic location and pleiotropic effects of 63 putatively sexually selected genes. Interestingly, most are pleiotropic (73%), and they are not preferentially sex linked. Their pleiotropic effects include fertility, development, life span, and viability, which may contribute to condition and/or fitness. My findings may also provide evidence for the capture of genetic variation in condition via the pleiotropic effects of sexually selected genes.     

Condition‐dependent mutation rates and sexual selection

‘Good genes’ models of sexual selection show that females can gain indirect benefits for their offspring if male ornaments are condition‐dependent signals of genetic quality. Recurrent deleterious mutation is viewed as a major contributor to variance in genetic quality, and previous theoretical treatments of ‘good genes’ processes have assumed that the influx of new mutations is constant. I propose that this assumption is too simplistic, and that mutation rates vary in ways that are important for sexual selection. Recent data have shown that individuals in poor condition can have higher mutation rates, and I argue that if both male sexual ornaments and mutation rates are condition‐dependent, then females can use male ornamentation to evaluate their mate’s mutation rate. As most mutations are deleterious, females benefit from choosing well‐ornamented mates, as they are less likely to contribute germline‐derived mutations to offspring. I discuss some of the evolutionary ramifications of condition‐dependent mutation rates and sexual selection.     

Sexual selection and condition-dependent mate preferences

The last decade has witnessed considerable theoretical and empirical investigation of how male sexual ornaments evolve. This strong male-biased perspective has resulted in the relative neglect of variation in female mate preferences and its consequences for ornament evolution. As sexual selection is a co-evolutionary process between males and females, ignoring variation in females overlooks a key aspect of this process. Here, we review the empirical evidence that female mate preferences, like male ornaments, are condition dependent. We show accumulating support for the hypothesis that high quality females show the strongest mate preference. Nonetheless, this is still an infant field, and we highlight areas in need of more research, both theoretical and empirical. We also examine some of the wider implications of condition-dependent mating decisions and their effect on the strength of sexual selection.     

Plumage color as a composite trait: developmental and functional integration of sexual ornamentation

Most studies of condition-dependent sexual ornaments have treated such ornaments as single traits. However, sexual ornaments are often composites of several components, each produced by partially independent developmental pathways. Depending on environmental and individual condition, components of these ornaments may reflect different behavioral or physiological properties of an individual. One of the best-known, condition-dependent ornaments is carotenoid-based plumage coloration, which has at least four distinct components: pigment elaboration, patch area, pigment symmetry, and patch area symmetry. Here we examined fitness consequences of variation in individual components of carotenoid ornamentation in male house finches (Carpodacus mexicanus). Over 5 yr and several selection episodes, we studied variation in the plumage components in a large sample (n = 498) of males from a Montana population. The ornament components were partially independent of each other and had distinct fitness consequences. Selection for higher fecundity favored an increase in redness of coloration and a decrease in pigment asymmetry and patch area asymmetry but did not act on patch area itself. In contrast, viability selection favored larger and more symmetrical ornamental patches but did not act on pigment elaboration. Developmental and functional interrelationships among individual components of ornamentation strongly differed between house finch populations. Distinct patterns of selection on individual components of condition-dependent ornaments, combined with partially independent development of components, should favor the evolution of composite sexual traits whose components reliably reflect condition across a wide array of environments.     

Female Mate Choice, Calling Song and Genetic Variance in the Cricket, Gryllodes sigillatus

Female preferences for song patterns of males of Gryllodes sigillatus and genetic variance of morphological traits correlated with them were analyzed. Females preferred short pulses associated with large males. The males’ thorax width, wing length and femur III length showed stronger relationship with the song pulse duration, whereas the relationship between pulse duration and wing width was not significant. Interestingly, this last trait was the only one that showed significant levels of genetic variance. Perhaps these results could be explained by the evolutionary response to sexual selection. Sexual selection could deplete the genetic variance in the male traits related to male‐mating success.     

Maintenance of genetic variation in sexual ornaments: a review of the mechanisms

Female preferences for elaborate male sexual traits have been documented in a number of species in which males contribute only genes to the next generation. In such systems, mate choice has been hypothesised to benefit females genetically. For the genetic benefits to be possible there must be additive genetic variation (V(A)) for sexual ornaments, such that highly ornamented males can pass fitter genes on to the progeny of choosy females. Here, I review the mechanisms that can contribute to the maintenance of this variation. The variation may be limited to sexual ornaments, resulting in Fisherian benefits in terms of the increased reproductive success of male progeny produced by choosy females. Alternatively, ornaments may capture V(A) in other life-history traits. In the latter case, "good genes" benefits may apply in terms of improved performance of the progeny of either sex. Some mechanisms, however, such as negative pleiotropy, sexually antagonistic variation or overdominance, can maintain V(A )in ornaments and other life-history traits with little variation in total fitness, leaving little room for any genetic benefits of mate choice. Distinguishing between these mechanisms has consequences not only for the theory of sexual selection, but also for evolution of sex and for biological conservation. I discuss how the traditional ways of testing for genetic benefits can usefully be supplemented by tests detecting benefits resulting from specific mechanisms maintaining V(A )in sexual ornaments.     

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.     

QTL linkage mapping of zebra finch beak color shows an oligogenic control of a sexually selected trait

Mate choice based on sexual ornaments can impose strong selection, which raises the question of how genetic variation in ornaments is maintained. One mechanism that has been proposed is genic capture. If ornament expression is influenced by general condition and condition is under polygenic control, selection will be inefficient in removing genetic variation. Here we analyze whether the genetic architecture of beak color in a population of zebra finches supports this hypothesis. Zebra finch beak color is commonly assumed to be under strong selection by mate choice, although some of the evidence is ambiguous. We show that beak redness has a heritability of 34% in our population and that it is strongly genetically correlated between the sexes, suggesting that it is largely controlled by the same genes in males and females. We mapped variation in beak redness based on 1404 single-nucleotide polymorphism (SNP) markers genotyped in a large pedigree. We find evidence for linkage on four chromosomes (Tgu1, Tgu5, Tgu13, Tgu21), which together explain a large part of the additive genetic variance. Our finding of genomic regions with major additive effects is not consistent with directional selection and genic capture, but rather suggests a role of antagonistic pleiotropy in maintaining genetic variation.