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.     

The sexual selection paradigm: have we overlooked other mechanisms in the evolution of male ornaments?

Extravagant male ornaments expressed during reproduction are almost invariably assumed to be sexually selected and evolve through competition for mating opportunities. Yet in species where male reproductive success depends on the defence of offspring, male ornaments could also evolve through social competition for offspring survival. However, in contrast to female ornaments, this possibility has received little attention in males. We show that a male ornament that is traditionally assumed to be sexually selected—the red nuptial coloration of the three-spined stickleback—is under stronger selection for offspring survival than for mating success. Males express most coloration during parenting, when they no longer attract females, and the colour correlates with nest retention and hatching success but not with attractiveness to females. This contradicts earlier assumptions and suggests that social selection for offspring survival rather than for sexual selection for mating success is the main mechanism maintaining the ornament in the population. These results suggest that we should consider other forms of social selection beyond sexual selection when seeking to explain the function and evolution of male ornaments. An incorrect assignment of selection pressures could hamper our understanding of evolution.     

Tail colour signals performance in blue tit nestlings

Indirect sexual selection arises when reproductive individuals choose their mates based on heritable ornaments that are genetically correlated to fitness. Evidence for genetic associations between ornamental colouration and fitness remains scarce. In this study, we investigate the quantitative genetic relationship between different aspects of tail structural colouration (brightness, hue and UV chroma) and performance (cell‐mediated immunity, body mass and wing length) in blue tit (Cyanistes caeruleus) nestlings. In line with previous studies, we find low heritability for structural colouration and moderate heritability for performance measures. Multivariate animal models show positive genetic correlations between the three measures of performance, indicating quantitative genetic variation for overall performance, and tail brightness and UV chroma, two genetically independent colour measures, are genetically correlated with performance (positively and negatively, respectively). Our results suggest that mate choice based on independent aspects of tail colouration can have fitness payoffs in blue tits and provide support for the indirect benefits hypothesis. However, low heritability of tail structural colouration implies that indirect sexual selection on mate choice for this ornament will be a weak evolutionary force.     

Melanin‐based coloration of sneaker male Atlantic salmon is linked to viability and emergence timing of their offspring

The ‘good genes’ hypothesis of sexual selection predicts that male ornaments are favoured by female mate choice because male ornament reveals genetic quality. In species with different male reproductive tactics, variation in genetic quality among ‘sneaking’ males has rarely been investigated, as usually ‘sneakers’ are thought not to be chosen by females. Here we focused on the alternative reproductive tactic in Atlantic salmon (Salmo salar Linnaeus, 1758) to test whether the skin colour of sneakers may reveal the performance traits of their offspring. A fully factorial breeding design was realized between 20 sneakers and two females using in vitro fertilization. We quantified the red and dark colorations of males and measured the survival of their progeny under semi‐natural conditions. In addition, the size of offspring and their emergence timing from the gravel nest were monitored in the laboratory. We found that darker males sired more viable offspring, whereas red coloration was negatively correlated with offspring survival. Nevertheless, darker and redder male pigmentations were linked to a delay in offspring emergence. These results demonstrate that colours can reveal individual genetic quality in an alternative male reproductive tactic, with male melanin‐based coloration being linked to both beneficial and detrimental effects for the offspring. Our results imply that sneaker ornaments may potentially play a role in both intra‐ and intersexual selection. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 126–135.     

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.     

Speciational evolution of coloration in the genus Carduelis

Sexual selection has been hypothesized to promote speciation, but evidence relating sexual selection to differences in speciation rates among taxa is equivocal. We note that evolutionary changes in ornaments are the link connecting sexual selection to speciation, and that ornament evolution is influenced by many factors so that its relationship with the strength of sexual selection may not be linear. We test if the evolution of ornamental coloration in Carduelis finches is related with speciation and if more ornamented lineages speciate more. We found that coloration evolves with a speciational pattern, but we found no evidence that the evolutionary changes associated with speciation are predominantly gains in ornamentation. The speciational pattern was found for both carotenoid- and melanin-based coloration, suggesting that traits putatively under stronger sexual selection by female choice (carotenoid coloration) are not the sole ones facilitating reproductive isolation. We conclude that in the genus Carduelis the evolutionary lability of ornaments influences speciation more than the strength of sexual selection, and we suggest that ornament lability should be considered as a possible causal factor in studies comparing cladogenesis among taxa.     

Ornaments or offspring: costs to reproductive success restrict sexual selection processes

If, in their partner choice, males seek direct benefits (fecund females), the result will be selection for traits indicating female quality rather than for arbitrary (Fisherian) traits. However, the costs of developing and maintaining the sexually selected traits (ornaments) may reduce the resources available to the female for allocation to reproduction and hence result in lower reproductive success per brood. This hitherto unrecognized fecundity cost of sexually selected traits will constrain both the potency of sexual selection mechanisms and the degree of elaboration of sexually selected traits in females, and can also apply to males which invest in their offspring: sexual selection becomes self-limiting. The fitness implications of these costs are examined for both sexes in a variety of mating and parental care patterns. Sexual selection acting on both sexes may lead to either dimorphism or monomorphism, the latter being the case when the quality indicators chosen by both sexes coincide. Ways of evasion or reduction of these reproductive costs of allocations to sexually selected traits include using different resource components for the ornament and for reproduction, or partitioning the two allocations in time.     

Multivariate genetic architecture of the Anolis dewlap reveals both shared and sex‐specific features of a sexually dimorphic ornament

Darwin viewed the ornamentation of females as an indirect consequence of sexual selection on males and the transmission of male phenotypes to females via the ‘laws of inheritance’. Although a number of studies have supported this view by demonstrating substantial between‐sex genetic covariance for ornament expression, the majority of this work has focused on avian plumage. Moreover, few studies have considered the genetic basis of ornaments from a multivariate perspective, which may be crucial for understanding the evolution of sex differences in general, and of complex ornaments in particular. Here, we provide a multivariate, quantitative‐genetic analysis of a sexually dimorphic ornament that has figured prominently in studies of sexual selection: the brightly coloured dewlap of Anolis lizards. Using data from a paternal half‐sibling breeding experiment in brown anoles (Anolis sagrei), we show that multiple aspects of dewlap size and colour exhibit significant heritability and a genetic variance–covariance structure ( G ) that is broadly similar in males ( G _m) and females ( G _f). Whereas sexually monomorphic aspects of the dewlap, such as hue, exhibit significant between‐sex genetic correlations (r_mf), sexually dimorphic features, such as area and brightness, exhibit reduced r_mf values that do not differ from zero. Using a modified random skewers analysis, we show that the between‐sex genetic variance–covariance matrix ( B) should not strongly constrain the independent responses of males and females to sexually antagonistic selection. Our microevolutionary analysis is in broad agreement with macroevolutionary perspectives indicating considerable scope for the independent evolution of coloration and ornamentation in males and females.     

Stabilizing sexual selection for female ornaments in a dance fly

Ornamental traits function by improving attractiveness and are generally presumed to experience directional selection for mating success. However, given the greater investment of females in offspring than males, female-specific ornaments can in theory signal fecundity yet be constrained by fecundity costs. Theoretical work predicts that such constraints can lead to stabilizing selection via male choice for intermediately ornamented females. Female dance flies Rhamphomyia longicauda (Diptera: Empididae) display two female-specific ornaments in mating swarms - inflatable abdominal sacs and pinnate tibial scales. We investigated the intensity and form of sexual selection on female traits including ornaments and found no evidence for directional sexual selection. Instead, we found marginally nonsignificant quadratic selection for all three measures of ornament expression. Canonical analysis confirmed that the strongest vectors of nonlinear selection were associated with ornamental traits, although the significance of the quadratic coefficients associated with these vectors depended on the statistical approach. Direct Mitchell-Olds and Shaw tests for the location of the maximum fitted fitness value for both raw morphological traits and canonical axes revealed only one marginally nonsignificant result for the multivariate axis loading most heavily on pinnate leg scales. Together, these results provide the first tentative support for stabilizing selection on female-specific ornaments.     

Viability of brown trout embryos positively linked to melanin-based but negatively to carotenoid-based colours of their fathers

'Good-genes' models of sexual selection predict significant additive genetic variation for fitness-correlated traits within populations to be revealed by phenotypic traits. To test this prediction, we sampled brown trout (Salmo trutta) from their natural spawning place, analysed their carotenoid-based red and melanin-based dark skin colours and tested whether these colours can be used to predict offspring viability. We produced half-sib families by in vitro fertilization, reared the resulting embryos under standardized conditions, released the hatchlings into a streamlet and identified the surviving juveniles 20 months later with microsatellite markers. Embryo viability was revealed by the sires' dark pigmentation: darker males sired more viable offspring. However, the sires' red coloration correlated negatively with embryo survival. Our study demonstrates that genetic variation for fitness-correlated traits is revealed by male colour traits in our study population, but contrary to predictions from other studies, intense red colours do not signal good genes.     

The role of maternal and paternal effects in the evolution of parental quality by sexual selection

Genetic models of maternal effects and models of mate choice have focused on the evolutionary effects of variation in parental quality. There have been, however, few attempts to combine these into a single model for the evolution of sexually selected traits. We present a quantitative genetic model that considers how male and female parental quality (together or separately) affect the expression of a sexually selected offspring trait. We allow female choice of males based on this parentally affected trait and examine the evolution of mate choice, parental quality and the indicator trait. Our model reveals a number of consequences of maternal and paternal effects. (1) The force of sexual selection owing to adaptive mate choice can displace parental quality from its natural selection optimum. (2) The force of sexual selection can displace female parental quality from its natural selection optimum even when nonadaptive mate choice occurs (e.g. runaway sexual selection), because females of higher parental quality produce more attractive sons and these sons counterbalance the loss in fitness owing to over-investment in each offspring. (3) Maternal and paternal effects can provide a source of genetic variation for offspring traits, allowing evolution by sexual selection even when those traits do not show direct genetic variation (i.e. are not heritable). (4) The correlation between paternal investment and the offspring trait influenced by the parental effects can result in adaptive mate choice and lead to the elaboration of both female preference and the male sexually selected trait. When parental effects exist, sexual selection can drive the evolution of parental quality when investment increases the attractiveness of offspring, leading to the elaboration of indicator traits and higher than expected levels of parental investment.     

Brighter yellow blue tits make better parents

Whether or not bird ornaments are a signal for direct (e.g. good parents) or indirect (e.g. good genes) benefits to prospective partners in sexual selection is controversial. Carotene coloration in Parus species is directly related to the ingestion of caterpillars, so that a brightly carotene-coloured tit may be signalling its ability to find caterpillars, a main high-quality food source for good fledgling development, and hence its parental abilities. If carotene-based plumage coloration is related to the good-parent hypothesis, we predict that yellow plumage brightness of tit fathers should be positively correlated to their investment in offspring provisioning. Here, we use cross-fostering experiments in blue tits (Parus caeruleus) to show that chick development (as measured by tarsus length) is related to yellowness of the foster father, but not to that of the genetic parents. Using these data, we were able to measure, for the first time to our knowledge, the separate contribution of genetic and environmental factors (i.e. parental plumage coloration) to chick development, and hence parental investment. Our data, which relate carotenoid coloration to models of good parents, and data from other authors, which relate ultraviolet coloration to good-genes models, stress that different kinds of coloration within an individual may provide different units of information to prospective females.     

Parental effort and response to nestling begging in the house sparrow: repeatability,heritability and parent–offspring co‐evolution

Parental effort has a direct impact on individual fitness. Theoretical models exploring how parental effort evolves to cope with offspring demand and sexual conflicts may differ in the assumptions they make in respect to the genetic heritability of parental behaviours. Only a few attempts, however, have been made to estimate the heritability of parental behaviours and their possible co‐evolution with offspring solicitation behaviour. Analysing parent and offspring behaviours in four generations of cross‐fostered broods of house sparrows, we found that parental effort (food delivery rate) was repeatable across consecutive broods and heritable across generations. In contrast, parental response to experimentally induced changes in nestling begging was neither repeatable across broods nor heritable across generations or correlated to nestling begging. Thus, the results give no indication for genetic covariance between begging intensity and parental response, but provide the first cross‐fostering‐based evidence for the heritability of parental investment levels across generations.     

Melanin, carotenoid and structural plumage ornaments: information content and role in great tits Parus major

The importance of plumage colour as an indicator of individual quality and the basis of sexual selection has long been recognized. Of the three generally distinguished classes of plumage colours, melanin-based ornaments are traditionally considered to provide less reliable information than carotenoid-based traits. However, the role of structural ornaments in multiple signalling systems has rarely been examined, and no study has compared the information content and role of the three ornament types simultaneously. Here we investigated three plumage ornaments in great tits Parus major : the size of the melanin-based breast stripe, the carotenoid-based colour of the yellow breast and the structurally based reflectance properties of the black crown. We worked on both the mechanistic and the functional levels. First, we assessed the dependence of ornaments on body condition during moult using ptilochronology. Second, we estimated assortative mating for these traits, as a measure of mutual sexual selection. Only the spectral attributes of crown feathers correlated with body condition during moult. However, breast stripe size was related to age, while the brightness of the yellow breast indicated body size. Relative crown ultraviolet reflectance was much higher in males than in females. Assortative mating was strongest for crown ultraviolet reflectance, but composite measures suggest that a system of multiple sexually selected traits with different information content may work in this population. These data support the accumulating evidence that the condition-dependence of melanin and carotenoid coloration is not qualitatively different. They also suggest that more research should target the reflectance properties of dark plumage areas in general, and ultraviolet crown ornamentation in tits in particular.     

Carotenoid ornaments and the spandrels of physiology: a critique of theory to explain condition dependency

Even as numerous studies have documented that the red and yellow coloration resulting from the deposition of carotenoids serves as an honest signal of condition, the evolution of condition dependency is contentious. The resource trade-off hypothesis proposes that condition-dependent honest signalling relies on a trade-off of resources between ornamental display and body maintenance. By this model, condition dependency can evolve through selection for a re-allocation of resources to promote ornament expression. By contrast, the index hypothesis proposes that selection focuses mate choice on carotenoid coloration that is inherently condition dependent because production of such coloration is inexorably tied to vital cellular processes. These hypotheses for the origins of condition dependency make strongly contrasting and testable predictions about ornamental traits. To assess these two models, we review the mechanisms of production of carotenoids, patterns of condition dependency involving different classes of carotenoids, and patterns of behavioural responses to carotenoid coloration. We review evidence that traits can be condition dependent without the influence of sexual selection and that novel traits can show condition-dependent expression as soon as they appear in a population, without the possibility of sexual selection. We conclude by highlighting new opportunities for studying condition-dependent signalling made possible by genetic manipulation and expression of ornamental traits in synthetic biological systems.     

Corticosterone regulates multiple colour traits in Lacerta [Zootoca] vivipara males

Ornamental colours usually evolve as honest signals of quality, which is supported by the fact that they frequently depend on individual condition. It has generally been suggested that some, but not all types of ornamental colours are condition dependent, indicating that different evolutionary mechanisms underlie the evolution of multiple types of ornamental colours even when these are exhibited by the same species. Stress hormones, which negatively affect condition, have been shown to affect colour traits based on different pigments and structures, suggesting that they mediate condition dependence of multiple ornament types both among and within individuals. However, studies investigating effects of stress hormones on different ornament types within individuals are lacking, and thus, evidence for this hypothesis is scant. Here, we investigated whether corticosterone mediates condition dependence of multiple ornaments by manipulating corticosterone levels and body condition (via food availability) using a two‐factorial design and by assessing their effect on multiple colour traits in male common lizards. Corticosterone negatively affected ventral melanin‐ and carotenoid‐based coloration, whereas food availability did not affect coloration, despite its significant effect on body condition. The corticosterone effect on melanin‐ and carotenoid‐based coloration demonstrates the condition dependence of both ornaments. Moreover, corticosterone affected ventral coloration and had no effect on the nonsexually selected dorsal coloration, showing specific effects of corticosterone on ornamental ventral colours. This suggests that corticosterone simultaneously mediates condition dependence of multiple colour traits and that it therefore accounts for covariation among them, which may influence their evolution via correlational selection.     

Potential fitness benefits from mate selection in the Atlantic cod (Gadus morhua)

Little evidence of benefits from female mate choice has been found when males provide no parental care or resources. Yet, good genes models of sexual selection suggest that elaborated male sexual characters are reliable signals of mate quality and that the offspring of males with elaborate sexual ornaments will perform better than those of males with less elaborate ornaments. We used cod (Gadus morhua L.), an externally fertilizing species where males provide nothing but sperm, to examine the potential of optimal mate selection with respect to offspring survival. By applying in vitro fertilizations, we crossed eight females with nine males in all possible combinations and reared each of the 72 sib groups. We found that offspring survival was dependent on which female was mated with which male and that optimal mate selection has the potential to increase mean offspring survival from 31.9 to 55.6% (a 74% increase). However, the size of the male sexual ornaments and sperm quality (i.e. sperm velocity and sperm density) could not predict offspring survival. Thus, even if there may be large fitness benefits of mate selection, we might not yet have identified the male characteristics generating high offspring survival.     

When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring

Quality differences between offspring sired by the social and by an extra-pair partner are usually assumed to have a genetic basis, reflecting genetic benefits of female extra-pair mate choice. In the zebra finch (Taeniopygia guttata), we identified a colour ornament that is under sexual selection and appears to have a heritable basis. Hence, by engaging in extra-pair copulations with highly ornamented males, females could, in theory, obtain genes for increased offspring attractiveness. Indeed, sons sired by extra-pair partners had larger ornaments, seemingly supporting the genetic benefit hypothesis. Yet, when comparing ornament size of the social and extra-pair partners, there was no difference. Hence, the observed differences most likely had an environmental basis, mediated, for example, via differential maternal investment of resources into the eggs fertilized by extra-pair and social partners. Such maternal effects may (at least partly) be mediated by egg size, which we found to be associated with mean ornament expression in sons. Our results are consistent with the idea that maternal effects can shape sexual selection by altering the genotype-phenotype relationship for ornamentation. They also caution against automatically attributing greater offspring attractiveness or viability to an extra-pair mate's superior genetic quality, as without controlling for differential maternal investment we may significantly overestimate the role of genetic benefits in the evolution of extra-pair mating behaviour.     

Ornament evolution in dragon lizards: multiple gains and widespread losses reveal a complex history of evolutionary change

The expression in females of ornaments thought to be the target of sexual selection in males is a long-standing puzzle. Two main hypotheses are proposed to account for the existence of conspicuous ornaments in both sexes (mutual ornamentation): genetic correlation between the sexes and sexual selection on females as well as males. We examined the pattern of ornament gains and losses in 240 species of dragon lizards (Agamidae) in order to elucidate the relative contribution of these two factors in the evolution of mutual ornamentation. In addition, we tested whether the type of shelter used by lizards to avoid predators predicts the evolutionary loss or constraint of ornament expression. We found evidence that the origin of female ornaments is broadly consistent with the predictions of the genetic correlation hypothesis. Ornaments appear congruently in both sexes with some lineages subsequently evolving male biased sexual dimorphism, apparently through the process of natural selection for reduced ornamentation in females. Nevertheless, ornaments have also frequently evolved in both sexes independently. This suggests that genetic correlations are potentially weak for several lineages and sexual selection on females is responsible for at least some evolutionary change in this group. Unexpectedly, we found that the evolutionary loss of some ornaments is concentrated more in males than females and this trend cannot be fully explained by our measures of natural selection.     

JOINT ALLELIC EFFECTS ON FITNESS AND METRIC TRAITS

Theoretical explanations of empirically observed standing genetic variation, mutation, and selection suggest that many alleles must jointly affect fitness and metric traits. However, there are few direct demonstrations of the nature and extent of these pleiotropic associations. We implemented a mutation accumulation (MA) divergence experimental design in Drosophila serrata to segregate genetic variants for fitness and metric traits. By exploiting naturally occurring MA line extinctions as a measure of line‐level total fitness, manipulating sexual selection, and measuring productivity we were able to demonstrate genetic covariance between fitness and standard metric traits, wing size, and shape. Larger size was associated with lower total fitness and male sexual fitness, but higher productivity. Multivariate wing shape traits, capturing major axes of wing shape variation among MA lines, evolved only in the absence of sexual selection, and to the greatest extent in lines that went extinct, indicating that mutations contributing wing shape variation also typically had deleterious effects on both total fitness and male sexual fitness. This pleiotropic covariance of metric traits with fitness will drive their evolution, and generate the appearance of selection on the metric traits even in the absence of a direct contribution to fitness.