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.     

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.     

Experimental stress during molt suggests the evolution of condition‐dependent and condition‐independent ornaments in the king penguin

Sexual selection and social selection are two important theories proposed for explaining the evolution of colorful ornamental traits in animals. Understanding signal honesty requires studying how environmental and physiological factors during development influence the showy nature of sexual and social ornaments. We experimentally manipulated physiological stress and immunity status during the molt in adult king penguins (Aptenodytes patagonicus), and studied the consequences of our treatments on colourful ornaments (yellow‐orange and UV beak spots and yellow‐orange auricular feather patches) known to be used in sexual and social contexts in this species. Whereas some ornamental features showed strong condition‐dependence (yellow auricular feather chroma, yellow and UV chroma of the beak), others were condition‐independent and remained highly correlated before and after the molt (auricular patch size and beak UV hue). Our study provides a rare examination of the links between ornament determinism and selection processes in the wild. We highlight the coexistence of ornaments costly to produce that may be honest signals used in mate choice, and ornaments for which honesty may be enforced by social mediation or rely on genetic constraints.     

Mate Choice and Colored Beak Spots of King Penguins

The theory of sexual selection explains sexual dimorphisms in ornaments used in mate choice. Mutual mate choice is a form of sexual selection that might explain sexually monomorphic ornamental traits. Under mutual mate choice, both sexes select partners based on the same ornament. We tested the mutual mate choice hypothesis in a mutually ornamented seabird, the king penguin (Aptenodytes patagonicus), through observations of the pair formation process in the field. Penguins that were ready to mate formed displaying pairs at the edge of the colony. Some of these pairs moved into the breeding colony and produced an egg (definitive pairs), while other pairs separated and often switched to another potential partner (temporary pairs). Colored ornaments were quantified using color vision modeling. We predicted that birds would mate assortatively by their elaborate ornamental traits (specifically, colors of beak spots, auricular patches of feathers, and breast patch of feathers). We also predicted that definitive pairs would exhibit more elaborate ornaments than temporary pairs. The mutual mate choice hypothesis was supported by assortative pairing for color of the beak spots, but not for color or size of the auricular patches or for the color of the breast patch. An alternative hypothesis was also consistent with our results, that female choice for a male ornamental trait and superior female condition associated with the same trait produced assortative pairing patterns. More UV‐ and yellow‐colored beak spots for females in definitive than temporary pairs supported the female choice hypothesis over the mutual mate choice hypothesis, but previous experimental results from altered beak spot colors supported the latter. Evidence to date thus supports both the mutual mate choice and female choice hypotheses.     

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.     

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.     

Female guppies agree to differ: phenotypic and genetic variation in mate-choice behavior and the consequences for sexual selection

Variation among females in mate choice may influence evolution by sexual selection. The genetic basis of this variation is of interest because the elaboration of mating preferences requires additive genetic variation in these traits. Here we measure the repeatability and heritability of two components of female choosiness (responsiveness and discrimination) and of female preference functions for the multiple ornaments borne by male guppies (Poecilia reticulata). We show that there is significant repeatable variation in both components of choosiness and in some preference functions but not in others. There appear to be several male ornaments that females find uniformly attractive and others for which females differ in preference. One consequence is that there is no universally attractive male phenotype. Only responsiveness shows significant additive genetic variation. Variation in responsiveness appears to mask variation in discrimination and some preference functions and may be the most biologically relevant source of phenotypic and genetic variation in mate-choice behavior. To test the potential evolutionary importance of the phenotypic variation in mate choice that we report, we estimated the opportunity for and the intensity of sexual selection under models of mate choice that excluded and that incorporated individual female variation. We then compared these estimates with estimates based on measured mating success. Incorporating individual variation in mate choice generally did not predict the outcome of sexual selection any better than models that ignored such variation.     

Mutually honest? Physiological ‘qualities’ signalled by colour ornaments in monomorphic king penguins

Mate choice is expected to be important for the fitness of both sexes for species in which successful reproduction relies strongly on shared and substantial parental investment by males and females. Reciprocal selection may then favour the evolution of morphological signals providing mutual information on the condition/quality of tentative partners. However, because males and females often have differing physiological constraints, it is unclear which proximate physiological pathways guarantee the honesty of male and female signals in similarly ornamented species. We used the monomorphic king penguin (Aptenodytes patagonicus) as a model to investigate the physiological qualities signalled by colour and morphological ornaments known to be under sexual selection (coloration of the beak spots and size of auricular feather patches). In both sexes of this slow‐breeding seabird, we investigated the links between ornaments and multiple indices of individual quality; including body condition, immunity, stress and energy status. In both sexes, individual innate immunity, resting metabolic rate, and the ability to mount a stress response in answer to an acute disturbance (capture) were similarly signalled by various aspects of beak coloration or auricular patch size. However, we also reveal interesting and contrasting relationships between males and females in how ornaments may signal individual quality. Body condition and oxidative stress status were signalled by beak coloration, although in opposite directions for the sexes. Over an exhaustive set of physiological variables, several suggestive patterns indicated the conveyance of honest information about mate quality in this monomorphic species. However, sex‐specific patterns suggested that monomorphic ornaments may signal different information concerning body mass and oxidative balance of males and females, at least in king penguins.     

Genic capture and resolving the lek paradox

The genic capture hypothesis offers a resolution to the question of how genetic variation in male sexually selected traits is maintained in the face of strong female preferences. The hypothesis is that male display traits are costly to produce and hence depend upon overall condition, which itself is dependent upon genes at many loci. Few attempts have been made to test the assumptions and predictions of the genic capture hypothesis rigorously and, in particular, little attention has been paid to determining the genetic basis of condition. Such tests are crucial to our understanding of the maintenance of genetic variation and in the evaluation of recent models that propose a role for sexual selection in the maintenance of sex. Here, we review approaches to testing the link between genetically determined condition and levels of sexual trait expression and consider the probable importance of deleterious mutations.     

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.     

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.     

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.     

Female choice for genetic complementarity in birds: a review

Data from avian species have played a prominent role in developing and testing theories of female mate choice. One of the most prominent models of sexual selection, the "good genes" model, emphasizes the indirect benefits of female preferences for male ornaments as indicators of a potential sire's additive genetic quality. However, there is growing interest in non-additive sources of genetic quality and mate choice models for self-referential disassortative mating based on optimal levels of genetic dissimilarity. We reviewed the empirical evidence for genetic-complementarity-based female mate choice among birds. We found the evidence for such choice is mixed but in general against the genetic complementarity hypothesis. The lack of evidence for genetic complementarity in many birds may be due to an inability to make the fine distinctions among potential mates based on genes, possibly due to the comparative anosmatic nature of avian sensory system. For some species however there is compelling evidence for genetic complementarity as a criterion used in female mate choice. Understanding the ubiquity of female mate choice based on genetic complementarity and the variation in this source of female preference among and within species remains a challenge.     

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.     

The evolution of compensation to herbivory in scarlet gilia, Ipomopsis aggregata: herbivore-imposed natural selection and the quantitative genetics of tolerance

Tolerance is the ability of plants to maintain fitness after experiencing herbivore damage. We investigated scarlet gilia tolerance to browsing in the framework of phenotypic plasticity using both an operational and candidate trait approach. Individuals from full-sib families were split into an artificial clipping treatment, a natural-damage treatment, or left as controls. We tested for genetic variation in tolerance by evaluating family x herbivory treatment interactions on fitness in a mixed model analysis of variance. In addition, we used selection analyses to assess the function of flowering phenology and compensatory regrowth (via branch production) as candidate tolerance traits. We found a strong detrimental fitness effect of browsing and considerable variation among sire half-sib families in levels of tolerance (25% to 63% of the fitness of controls). There was no evidence of overcompensation at either the population or family level and no additive genetic variation in operationally defined tolerance. Phenotypic selection analyses provide evidence that early flowering and compensatory regrowth function as tolerance characters. We found strong linear and correlational selection for early flowering and increased branch production for damaged plants and linear selection for apical dominance (reduced branchiness) and early flowering in control plants. Moreover, reduced phenological delay and increased plasticity in branch production were correlated with tolerance. We detected significant additive genetic variation in flowering phenology in both treatments and a positive genetic correlation between the phenology of control and damaged plants. We found significant additive genetic variation in branch production in undamaged and naturally damaged plants, but not in clipped plants. Damaged plants exhibited marginally significant additive genetic variance in fitness, although its heritability was very low (approximately 3.6%). We failed to find additive genetic variation in the fitness of control plants. Our results suggest that tolerance traits are under herbivore-imposed natural selection in this population, but that responses to selection are limited by available genetic variation and selective constraints.     

Mutual Mate Choice for Colorful Traits in King Penguins

While studies of mate choice based on male color pattern are ubiquitous, studies of mate choice based on ornamental color traits in sexually monomorphic species are less common. We conducted manipulative field experiments on two color ornaments of king penguins (Aptenodytes patagonicus), the size of auricular patches of orange feathers and degree of UV reflectance from beak spots, to determine how the degree of ornamentation influenced pairing rate. In a reduction of auricular patch size, females paired significantly more quickly than males in both control and experimental samples. When this bias was taken into account statistically, pairing of individuals with reduced auricular patches was significantly delayed. We also reduced, but did not eliminate, UV reflectance from beak spots by applying a UV filter; no sex difference in pairing rate was evident in this experiment. Treated birds paired significantly more slowly than untreated control individuals, taking more than a week longer to pair on average than their unmanipulated counterparts, a result that was significant for males and approached significance for females. Our results may indicate mutual mate choice via UV reflectance of the beak spot. Given that this is a species where breeding is extremely slow and considerable investment by both males and females is required for successful reproduction, our results support the hypothesis that in such species, sexual selection might act on the same ornament in both sexes.     

The heritability of fitness: Bad news for 'good genes'?

Some models of sexual selection depend on a female preference for 'good genes': females choose conspicuous males as these are advertising their possession of genes for fitness characters which can be inherited by their offspring. In contrast, Fisher's fundamental theorem of natural selection - which underlies much of population genetics theory - predicts that in a population at equilibrium there can be no additive genetic variation in fitness. Recent work on collared flycatchers in the wild shows that characters influencing fitness do indeed have a relatively low heritability. However, other studies of the inheritance of fitness in the laboratory suggest that under some circumstances a population may retain considerable genetic diversity for fitness characters. Genetically based female choice might hence have the potential to control the evolution of male sexual ornaments. More work on natural populations is needed; and birds may be a good place to start looking.     

Sexual selection of multiple handicaps in the red-collared widowbird: female choice of tail length but not carotenoid display

Although sexual selection through female choice explains exaggerated male ornaments in many species, the evolution of the multicomponent nature of most sexual displays remains poorly understood. Theoretical models suggest that handicap signaling should converge on a single most informative quality indicator, whereas additional signals are more likely to be arbitrary Fisherian traits, amplifiers, or exploitations of receiver psychology. Male nuptial plumage in the highly polygynous red-collared widowbird (Euplectes ardens) comprises two of the commonly advocated quality advertisements (handicaps) in birds: a long graduated tail and red carotenoid coloration. Here we use multivariate selection analysis to investigate female choice in relation to male tail length, color (reflectance) of the collar, other aspects of morphology, ectoparasite load, display rate, and territory quality. The order and total number of active nests obtained are used as measures of male reproductive success. We demonstrate a strong female preference and net sexual selection for long tails, but marginal or no effects of color, morphology, or territory quality. Tail length explained 47% of male reproductive success, an unusually strong fitness effect of natural ornament variation. Fluctuating tail asymmetry was unrelated to tail length, and had no impact on mating success. For the red collar, there was negative net selection on collar area, presumably via its negative relationship with tail length. None of the color variables (hue, chroma, and brightness) had significant selection differentials, but a partial effect (selection gradient) of chroma might represent a color preference when tail length is controlled for. We suggest that the red collar functions in male agonistic interactions, which has been strongly supported by subsequent work. Thus, female choice targets only one handicap, extreme tail elongation, disregarding or even selecting against the carotenoid display. We discuss whether long tails might be better indicators of genetic quality than carotenoid pigmentation. As regards the evolution of multiple ornaments, we propose that multiple handicap signaling is stable not because of multiple messages but because of multiple receivers, in this case females and males.     

Cultural transmission and the evolution of cooperative behavior

Sociobiological theory predicts that humans should not cooperate with large groups of unrelated individuals. This prediction is based on genetic models that show that selection acting on variation between large unrelated groups will generally be much weaker than selection acting on variation between individuals. Recently, several authors have presented related models of human evolution that integrate cultural and genetic transmission of behavior. We show that in such models group selection is potentially a strong force. Data on ethnocentrism is examined in the context of these results.     

Variation in the peacock’s train shows a genetic component

Female peafowl (Pavo cristatus) show a strong mating preference for males with elaborate trains. This, however, poses something of a paradox because intense directional selection should erode genetic variation in the males’ trains, so that females will no longer benefit by discriminating among males on the basis of these traits. This situation is known as the ‘lek paradox’, and leads to the theoretical expectation of low heritability in the peacock’s train. We used two independent breeding experiments, involving a total of 42 sires and 86 of their male offspring, to estimate the narrow sense heritabilities of male ornaments and other morphometric traits. Contrary to expectation, we found significant levels of heritability in a trait known to be used by females during mate choice (train length), while no significant heritabilities were evident for other, non-fitness related morphological traits (tarsus length, body weight or spur length). This study adds to the building body of evidence that high levels of additive genetic variance can exist in secondary sexual traits under directional selection, but further emphasizes the main problem of what maintains this variation.