An examination of genetic variation and selection on condition in Drosophila melanogaster males

According to the genic capture hypothesis, the maintenance of additive genetic variation in fitness-related traits is due to both condition-dependence of these traits and high genetic variation for condition. Evidence supporting this latter assumption is scarce. In this study, we investigated, using hemiclonal analysis, standing genetic variation for condition and relative adult fitness in male Drosophila melanogaster (Meigen) (Diptera: Drosophilidae). The absolute fat and the relative fat content were used as indices of body condition and were measured along with adult relative fitness from males reared in high or low larval densities. The results did not demonstrate genetic variation for condition or adult relative fitness. However, the larval density encountered during development had a strong and significant effect on all traits. Surprisingly, although not significant, negative selection gradients acting on absolute fat and relative fat content were also found in both treatments. These findings challenge one of the main assumptions of the genic capture hypothesis and the use of fat content as an ideal index of condition.     

Genic capture and the genetic basis of sexually selected traits in the zebra finch

Abstract The lek paradox, in which female choice erodes genetic variation in male sexually selected traits, is a fundamental issue in sexual selection. If females gain only genetic benefits from preferentially having their ova fertilized by males with particular traits, what maintains variation in these traits? Under strong directional selection mediated through mate choice, the alleles for beneficial male traits are expected to go to fixation and exhibit little variation. A theoretical solution to the lek paradox is the genic capture hypothesis which states that: costly male traits subject to female choice are condition dependent, that male condition is dependent on genes at many loci and exhibits additive genetic variance, and that positive genetic correlations exist between sexually selected traits and condition. Using a captive population of the zebra finch Taeniopygia guttata, we tested two key predictions from this model: (1) that genetic variance exists in beak color which is a sexually selected trait, but also in condition and immune function, and (2) that positive genetic correlations exist between condition and beak color, and between beak color, condition, and immune function. Genetic parameters were estimated from a large breeding experiment involving 81 sires, 972 offspring, a pedigree of 1526 individuals, using the animal model. We employed the following index of body condition: residuals from a log‐log plot of body mass on tarsus length following a standardized and extended period of exercise, in which residual mass is known to reflect fat and protein reserves. Our results were broadly consistent with the genic capture hypothesis because we found (1) additive genetic variation in beak color and immune function and condition, and (2) positive genetic correlations between condition and beak color, and between condition, beak color, and several assays of immune responsiveness. However, both of these results need qualification. In the first case we identified an important general problem in estimating the coefficient of additive genetic variance (CV_A) in body condition. In the second case, although most of the genetic correlations were positive as predicted, only some were statistically significant, possibly due to our relatively small sample sizes, because genetic correlations typically have large standard errors and therefore require very large samples to be statistically significant. The statistically significant, positive genetic correlations included those between beak color and immune function (response to tetanus), and between immune function (response to tetanus) and condition, both of which indicate that females gain good genes from mating with males in good condition and/or with a redder beak color. We discuss the implications of our results for devising more rigorous but pragmatic tests of the genic capture hypothesis.     

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.     

Low inbreeding depression in a sexual trait in the stalk-eyed fly <Emphasis Type="Italic">Teleopsis dalmanni</Emphasis>

The genic capture hypothesis implies that the expression of sexual ornaments largely depends on genes affecting resource acquisition and use. The ornaments should thus show high degree of directional dominance typical of life-history traits, and consequently, they should be severely affected by inbreeding. Here we investigated the effect of inbreeding on a sexual ornament (male eyespan) in stalk-eyed fly, Teleopsis dalmanni. For comparison, we also measured inbreeding depression in non-sexual morphological traits: female eyespan as well as wing and thorax lengths in both sexes. Both eyespan, and other morphological traits we measured, showed significant inbreeding depression. In accord with predictions of genic capture hypothesis, male eyespan did decrease under inbreeding significantly more than female eyespan. However, the decline in male eyespan was fully explained by overall decline in body length. Moreover, the magnitude of inbreeding depression in male eyespan was considerably lower than that typically observed for life-histories; in fact, it fitted within the range typically characterizing morphological traits. We therefore conclude that our results provide weak support for genic capture hypothesis.     

Sexual selection and the evolution of male and female cognition: A test using experimental evolution in seed beetles*

The mating system is thought to be important in shaping animal intelligence and sexual selection has been depicted as a driver of cognitive evolution, either directly by promoting superior cognitive ability during mate competition, or indirectly via genic capture of sexually selected traits. However, it remains unclear if intensified sexual selection leads to general improvements in cognitive abilities. Here, we evaluated this hypothesis by applying experimental evolution in seed beetles. Replicate lines, maintained for 35 generations of either enforced monogamy (eliminating sexual selection) or polygamy, were challenged to locate and discriminate among mates (male assays) or host seeds (female assays) in a spatial chemosensory learning task. All lines displayed learning between trials. Moreover, polygamous males outperformed monogamous males, providing evidence that sexual selection can lead to the evolution of improved male cognition. However, there were no differences between regimes in rates of male learning, and polygamous females showed no improvement in host search and even signs of reduced learning. Hence, sexual selection increased performance in cognitively demanding mate search, but it did not lead to general increases in cognitive abilities. We discuss the possibility that sexually antagonistic selection is an important factor maintaining abundant genetic variation in cognitive traits.     

Mating tactics determine patterns of condition dependence in a dimorphic horned beetle

The persistence of genetic variability in performance traits such as strength is surprising given the directional selection that such traits experience, which should cause the fixation of the best genetic variants. One possible explanation is ‘genic capture’ which is usually considered as a candidate mechanism for the maintenance of high genetic variability in sexual signalling traits. This states that if a trait is ‘condition dependent’, with expression being strongly influenced by the bearer''s overall viability, then genetic variability can be maintained via mutation-selection balance. Using a species of dimorphic beetle with males that gain matings either by fighting or by ‘sneaking’, we tested the prediction of strong condition dependence for strength, walking speed and testes mass. Strength was strongly condition dependent only in those beetles that fight for access to females. Walking speed, with less of an obvious selective advantage, showed no condition dependence, and testes mass was more condition dependent in sneaks, which engage in higher levels of sperm competition. Within a species, therefore, condition dependent expression varies between morphs, and corresponds to the specific selection pressures experienced by that morph. These results support genic capture as a general explanation for the maintenance of genetic variability in traits under directional selection.     

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.     

Sexual selection, genetic architecture, and the condition dependence of body shape in the sexually dimorphic fly Prochyliza xanthostoma (Piophilidae)

The hypothesis that sexual selection drives the evolution of condition dependence is not firmly supported by empirical evidence, and the process remains poorly understood. First, even though sexual competition typically involves multiple traits, studies usually compare a single sexual trait with a single "control" trait, ignoring variation among sexual traits and raising the possibility of sampling bias. Second, few studies have addressed the genetic basis of condition dependence. Third, even though condition dependence is thought to result from a form of sex-specific epistasis, the evolution of condition dependence has never been considered in relation to intralocus sexual conflict. We argue that condition dependence may weaken intersexual genetic correlations and facilitate the evolution of sexual dimorphism. To address these questions, we manipulated an environmental factor affecting condition (larval diet) and examined its effects on four sexual and four nonsexual traits in Prochyliza xanthostoma adults. As predicted by theory, the strength of condition dependence increased with degree of exaggeration among male traits. Body shape was more condition dependent in males than in females and, perhaps as a result, genetic and environmental effects on body shape were congruent in males, but not in females. However, of the four male sexual traits, only head length was significantly larger in high-condition males after controlling for body size. Strong condition dependence was associated with reduced intersexual genetic correlation. However, homologous male and female traits exhibited correlated responses to condition, suggesting an intersexual genetic correlation for condition dependence itself. Our findings support the role of sexual selection in the evolution of condition dependence, but reveal considerable variation in condition dependence among sexual traits. It is not clear whether the evolution of condition dependence has mitigated or exacerbated intralocus sexual conflict in this species.     

Genetic and environmental effects on secondary sex traits in guppies (Poecilia reticulata)

Male guppies (Poecilia reticulata) exhibit extreme phenotypic and genetic variability for several traits that are important to male fitness, and several lines of evidence suggest that resource level affects phenotypic expression of these traits in nature. We tested the hypothesis that genetic variation for male secondary sex traits could be maintained by genotype-specific effects of variable resource levels (genotype-environment interaction). To do this, we measured genetic variation and covariation under two environmental conditions--relatively low and relatively high food availability. We found high levels of genetic variation for most traits, but we only found a significant G x E interaction across food levels for one trait (body size) for one population. The across-environment correlations for size were large and positive, indicating that the reaction norms for size did not cross. We also found that male colour pattern elements had nearly an order of magnitude more genetic variation than did male size. Heritability estimates indicated that Y-linked genes are responsible for some of the genetic variation in male size and colour traits. We discuss implications of these results for theories of the maintenance of genetic variation in male secondary sexual traits in guppies.     

The sexually-selected sperm hypothesis: sex-biased inheritance and sexual antagonism

When females are inseminated by more than one male (polyandry) sexual selection continues after insemination in the form of sperm competition and cryptic female choice. The sexually-selected sperm hypothesis proposes that, under the risk of sperm competition, additive variation in male traits determining fertilising efficiency will select for female propensity to be polyandrous in order to increase the probability of producing sons with superior fertilising efficiency. Two factors complicate this prediction: sex-biased transmission of male fertilising efficiency traits and sexual antagonism of sex-limited traits, fostered by sex-biased inheritance. Here, we (i) review the evidence that male traits contributing towards fertilising efficiency are heritable through sex-biased mechanisms, and (ii) explore the evolutionary implications for male and female reproductive strategies caused by both sex-biased transmission and sexual antagonism of fertilising efficiency traits. Many male fertilising efficiency traits are heritable through sex-biased mechanisms and may not necessarily increase female fitness. The predictions of the sexually-selected sperm hypothesis change dramatically under these different mechanisms of inheritance of fertilising efficiency traits, and different fitness pay-offs derived by females from the expression of such traits. Both sex-biased control of fertilising efficiency and sexual antagonism may also be important in explaining the maintenance of the genetic variance and selection potential of fertilising efficiency. We propose that a useful approach to test the sexually-selected sperm hypothesis is to combine studies which identify behavioural and physiological mechanisms explaining variation in reproductive success with artificial selection experiments to infer the underlying evolutionary patterns.     

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.     

SEXUAL CONFLICT AND THE MAINTENANCE OF MULTIVARIATE GENETIC VARIATION

Mate choice should erode additive genetic variation in sexual displays, yet these traits often harbor substantial genetic variation. Nevertheless, recent developments in quantitative genetics have suggested that multivariate genetic variation in the combinations of traits under selection may still be depleted. Accordingly, the erosion and maintenance of variation may only be detectable by studying whole suites of traits. One potential process favoring the maintenance of genetic variance in multiple trait combinations is the modification of sexual selection via sexually antagonistic interactions between males and females. Here we consider how interlocus sexual conflict can shape the genetic architecture of male sexual traits in the cricket, Teleogryllus commodus. In this species, the ability of each sex to manipulate insemination success significantly alters the selection acting on male courtship call properties. Using a quantitative genetic breeding design we estimated the additive genetic variation in these traits and then predicted the change in variation due to previously documented patterns of sexual selection. Our results indicate that female choice should indeed deplete multivariate genetic variance, but that sexual conflict over insemination success may oppose this loss of variance. We suggest that changes in the direction of selection due to sexually antagonistic interactions will be an important and potentially widespread factor in maintaining multivariate genetic variation.     

Geographic variation in sexual dimorphism in the barn owl Tyto alba: a role for direct selection or genetic correlation?

Geographic variation in sexually selected traits is commonly attributed to geographic variation in the net benefit accrued from bearing such traits. Although natural and sexual selection are potentially important in shaping geographic variation, genetic constraints may also play a role. Although a genetic correlation between two traits may itself be the outcome of natural or sexual selection, it may indirectly reinforce the establishment and maintenance of cline variation with respect to one particular trait when across the cline different values of other traits are selected. Using the barn owl Tyto alba, a species in which the plumage of females is more reddish‐brown and more marked with black spots than that of males, I report results that are consistent with the hypothesis that both direct selection and genetic constraints may help establish and maintain cline variation in sexual dichromatism. In this species, inter‐individual variation in plumage coloration and spottiness has a genetic basis, and these traits are not sensitive to the environment. Data, based on the measurement of skin specimens, is consistent with the hypothesis that the stronger European cline variation in male spottiness than in female spottiness depends on the combined effects of (1) the similar cline variation in male and female plumage coloration and (2) the more intense phenotypic correlation between plumage coloration and spottiness in males (darker birds are more heavily spotted in the two sexes, but especially males) which is a general feature among the globally distributed barn owls. In northern Europe, male and female T. a. guttata are reddish‐brown and heavily spotted, and in southern Europe male and female T. a. alba are white, but only females display many spots. Here, I discuss the relative importance of direct selection, genetic correlation and the post‐ice age invasion of Europe by T. alba, in generating sex‐specific cline variation in plumage spottiness and non‐sex‐specific cline variation in plumage coloration.     

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.     

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.     

Evolution of genetic variation for condition-dependent traits in stalk-eyed flies

Sexual selection has been proposed to increase genetic variation for condition-dependent ornaments. The condition capture model predicts the genetic variance for a sexually selected trait from the genetic variance in condition and the slope of the relationship between the ornament and condition. Assuming that body size reflects condition we assess the efficacy of this model using six species of stalk-eyed flies (Diopsidae). Prior evidence indicates that male eye span exhibits strong condition dependence and is under sexual selection in sexually dimorphic but not monomorphic species. In contrast, thorax width is weakly related to condition and probably under stabilizing selection. We estimated additive genetic variances for eye span, body length and thorax width from half-sib breeding studies and found that the condition capture model explained 97% of the variation in eye span genetic variance but only 7% of thorax width genetic variance. Comparison of phylogenetically independent contrasts revealed that evolutionary change in male eye span genetic variance is due to evolutionary change in the allometric relationship between eye span and condition: not to evolutionary change in genetic variance for condition. These results suggest that sexual selection can accelerate evolutionary change in condition-dependent male ornaments by increasing the genetic variation available for selection.     

IDENTIFICATION OF GENETICALLY LINKED FEMALE PREFERENCE AND MALE TRAIT

Genetic variation in male traits and the female preferences for those traits allows for the evolution of sexual behavior. Trait–preference combinations are thought to improve the effectiveness of runaway sexual selection within a species, and are considered necessary for the induction of divergence between species. Novel traits, or variants of existing traits, and their associated preferences in the opposite sex are more likely to be maintained if they are genetically linked in proximity on a chromosome (the genetic coupling hypothesis), yet there is little empirical evidence that this genetic linkage occurs. Here we show for the first time that natural genetic variation at a single‐linked region can induce both species‐specific female choosiness and the male trait they are discriminating against. We found this effect in two separate regions of the genome, demonstrating that this linkage may be common. In contrast, female choosiness and male unattractiveness could not be alleviated by a single region. The close linkage of these loci and the strength of their effect provide an evolutionary means by which this preference–trait combination could arise and be maintained, thus enabling a more rapid route for runaway sexual selection, and providing empirical evidence supporting the genetic coupling hypothesis.     

Maternal inheritance,epigenetics and the evolution of polyandry

Growing evidence indicates that females actively engage in polyandry either to avoid genetic incompatibility or to bias paternity in favor of genetically superior males. Despite empirical support for the intrinsic male quality hypothesis, the maintenance of variation in male fitness remains a conundrum for traditional "good genes" models of sexual selection. Here, we discuss two mechanisms of non-Mendelian inheritance, maternal inheritance of mitochondria and epigenetic regulation of gene expression, which may explain the persistence of variation in male fitness traits important in post-copulatory sexual selection. The inability of males to transmit mitochondria precludes any direct evolutionary response to selection on mitochondrial mutations that reduce or enhance male fitness. Consequently, mitochondrial-based variation in sperm traits is likely to persist, even in the face of intense sperm competition. Indeed, mitochondrial nucleotide substitutions, deletions and insertions are now known to be a primary cause of low sperm count and poor sperm motility in humans. Paradoxically, in the field of sexual selection, female-limited response to selection has been largely overlooked. Similarly, the contribution of epigenetics (e.g., DNA methylation, histone modifications and non-coding RNAs) to heritable variation in male fitness has received little attention from evolutionary theorists. Unlike DNA sequence based variation, epigenetic variation can be strongly influenced by environmental and stochastic effects experienced during the lifetime of an individual. Remarkably, in some cases, acquired epigenetic changes can be stably transmitted to offspring. A recent study indicates that sperm exhibit particularly high levels of epigenetic variation both within and between individuals. We suggest that such epigenetic variation may have important implications for post-copulatory sexual selection and may account for recent findings linking sperm competitive ability to offspring fitness.