The evolution of sexual size dimorphism in the house finch. IV. Population divergence in ontogeny

Differences among taxa in sexual size dimorphism of adults can be produced by changes in distinct developmental processes and thus may reflect different evolutionary histories. Here we examine whether divergence in sexual dimorphism of adults between recently established Montana and Alabama populations of the house finch (Carpodacus mexicanus) can be attributed to population differences in growth of males and females. In both populations, males and females were similar at hatching, but as a result of sex-specific growth attained sexual size dimorphism by the time of independence. Timing and extent of growth varied between the sexes: Females maintained maximum rates of growth for a longer time than males, whereas males had higher initial growth rates and achieved maximum growth earlier and at smaller sizes than females. Ontogeny of sexual dimorphism differed between populations, but in each population, sexual dimorphism in growth parameters and sexual dimorphism at the time of nest leaving were similar to sexual dimorphism of adults. Variation in growth of females contributed more to population divergence than did growth of males. In each population, we found close correspondence between patterns of sexual dimorphism in growth and population divergence in morphology of adults: Traits that were the most sexually dimorphic in growth in each population contributed the most to population divergence in both sexes. We suggest that sex-specific expression of phenotypic and genetic variation throughout the ontogeny of house finches can result in different responses to selection between males and females of the same age, and thus produce fast population divergence in the sexual size dimorphism.     

The evolution of sexual size dimorphism in the house finch. II. Population divergence in relation to local selection

Recent colonization of ecologically distinct areas in North America by the house finch (Carpodacus mexicanus) was accompanied by strong population divergence in sexual size dimorphism. Here we examined whether this divergence was produced by population differences in local selection pressures acting on each sex. In a long-term study of recently established populations in Alabama, Michigan, and Montana, we examined three selection episodes for each sex: selection for pairing success, overwinter survival, and within-season fecundity. Populations varied in intensity of these selection episodes, the contribution of each episode to the net selection, and in the targets of selection. Direction and intensity of selection strongly differed between sexes, and different selection episodes often favored opposite changes in morphological traits. In each population, current net selection for sexual dimorphism was highly concordant with observed sexual dimorphism--in each population, selection for dimorphism was the strongest on the most dimorphic traits. Strong directional selection on sexually dimorphic traits, and similar intensities of selection in both sexes, suggest that in each of the recently established populations, both males and females are far from their local fitness optimum, and that sexual dimorphism has arisen from adaptive responses in both sexes. Population differences in patterns of selection on dimorphism, combined with both low levels of ontogenetic integration in heritable sexually dimorphic traits and sexual dimorphism in growth patterns, may account for the close correspondence between dimorphism in selection and observed dimorphism in morphology across house finch populations.     

The evolution of sexual size dimorphism in the house finch. V. Maternal effects

The phenotype of a mother and the environment that she provides might differentially affect the phenotypes of her sons and daughters, leading to change in sexual size dimorphism. Whereas these maternal effects should evolve to accommodate the adaptations of both the maternal and offspring generations, the mechanisms by which this is accomplished are rarely known. In birds, females adjust the onset of incubation (coincident with the first egg or after all eggs are laid) in response to the environment during breeding, and thus, indirectly, determine the duration of offspring growth. In the two house finch (Carpodacus mexicanus) populations that breed at the extremes of the species' distribution (Montana and Alabama), females experience highly distinct climatic conditions during nesting. We show that in close association with these conditions, females adjusted jointly the onset of incubation and the sequence in which they produced male and female eggs and consequently modified the growth of sons and daughters. The onset of incubation in newly breeding females closely tracked ambient temperature in a pattern consistent with the maintenance of egg viability. Because of the very different climates in Montana and Alabama, females in these populations showed the opposite patterns of seasonal change in incubation onset and the opposite sex bias in egg-laying order. In females with breeding experience, incubation onset and sex bias in laying order were closely linked regardless of the climatic variation. In nests in which incubation began with the onset of egg laying, the first-laid eggs were mostly females in Montana, but mostly males in Alabama. Because in both populations, male, but not female, embryos grew faster when exposed to longer incubation, the sex-bias produced highly divergent sizes of male and female juveniles between the populations. Overall, the compensatory interaction between the onset of incubation and the sex-biased laying order achieved a compromise between maternal and offspring adaptations and contributed to rapid morphological divergence in sexual dimorphism between populations of the house finch breeding at the climatic extremes of the species range.     

The evolution of sexual size dimorphism in the house finch. III. Developmental basis

Sexual size dimorphism of adults proximately results from a combination of sexually dimorphic growth patterns and selection on growing individuals. Yet, most studies of the evolution of dimorphism have focused on correlates of only adult morphologies. Here we examined the ontogeny of sexual size dimorphism in an isolated population of the house finch (Carpodacus mexicanus). Sexes differed in growth rates and growth duration; in most traits, females grew faster than males, but males grew for a longer period. Sexual dimorphism in bill traits (bill length, width, depth) and in body traits (wing, tarsus, and tail length; mass) developed during different periods of ontogeny. Growth of bill traits was most different between sexes during the juvenile period (after leaving the nest), whereas growth of body traits was most sexually dimorphic during the first few days after hatching. Postgrowth selection on juveniles strongly influenced sexual dimorphism in all traits; in some traits, this selection canceled or reversed dimorphism patterns produced by growth differences between sexes. The net result was that adult sexual dimorphism, to a large degree, was an outcome of selection for survival during juvenile stages. We suggest that previously documented fast and extensive divergence of house finch populations in sexual size dimorphism may be partially produced by distinct environmental conditions during growth in these populations.     

Gene duplication in the evolution of sexual dimorphism

Males and females share most of the same genes, so selection in one sex will typically produce a correlated response in the other sex. Yet, the sexes have evolved to differ in a multitude of behavioral, morphological, and physiological traits. How did this sexual dimorphism evolve despite the presence of a common underlying genome? We investigated the potential role of gene duplication in the evolution of sexual dimorphism. Because duplication events provide extra genetic material, the sexes each might use this redundancy to facilitate sex‐specific gene expression, permitting the evolution of dimorphism. We investigated this hypothesis at the genome‐wide level in Drosophila melanogaster, using the presence of sex‐biased expression as a proxy for the sex‐specific specialization of gene function. We expected that if sexually antagonistic selection is a potent force acting upon individual genes, duplication will result in paralog families whose members differ in sex‐biased expression. Gene members of the same duplicate family can have different expression patterns in males versus females. In particular, duplicate pairs containing a male‐biased gene are found more frequently than expected, in agreement with previous studies. Furthermore, when the singleton ortholog is unbiased, duplication appears to allow one of the paralog copies to acquire male‐biased expression. Conversely, female‐biased expression is not common among duplicates; fewer duplicate genes are expressed in the female‐soma and ovaries than in the male‐soma and testes. Expression divergence exists more in older than in younger duplicates pairs, but expression divergence does not correlate with protein sequence divergence. Finally, genomic proximity may have an effect on whether paralogs differ in sex‐biased expression. We conclude that the data are consistent with a role of gene duplication in fostering male‐biased, but not female‐biased, gene expression, thereby aiding the evolution of sexual dimorphism.     

Predicting the evolution of sexual size dimorphism

11 , Evolution 34 : 292–305) equations for predicting the evolution of sexual size dimorphism (SSD) through frequency‐dependent sexual selection, and frequency‐independent natural selection, were tested against results obtained from a stochastic genetic simulation model. The SSD evolved faster than predicted, due to temporary increases in the genetic variance brought about by directional selection. Predictions for the magnitude of SSD at equilibrium were very accurate for weak sexual selection. With stronger sexual selection the total response was greater than predicted. Large changes in SSD can occur without significant long‐term change in the genetic correlation between the sexes. Our results suggest that genetic correlations constrain both the short‐term and long‐term evolution of SSD less than predicted by the Lande model.     

Geographic variation in male ornamentation and female mate preference in the house finch: a comparative test of models of sexual selection

I compared the mate preferences of female house finches (Carpodacusmexicanus) from populations in which males differ in both plumagecoloration and the extent of ventral pigmentation (patch size).Phylogenetic analysis indicated that the small patch of ventralcoloration displayed by males in some populations is derivedfrom a larger-patched ancestral state. Regardless of the appearanceof males in their own populations, however, females from allpopulations showed a preference for the most brightly coloredmales and males with the largest patches. A reduction in patchsize independent of a change in female mate preference is notconsistent with sensory-bias or reproductive isolation modelsof sexual selection or with general predictions of runaway modelsof sexual selection. In contrast, a lack of congruence betweenfemale mate preference and male trait expression is predictedby the honest advertisement model, with house finches respondingto variation in regional and local access to carotenoid plumagepigments.     

Pairing success relative to male plumage redness and pigment symmetry in the house finch: temporal and geographic constancy

Male house finches (Carpodacus mexicanus) have carotenoid-based ornamentalplumage coloration. In previous research it was shown that fora single population of house finches in a single year, malesthat paired were on average redder in plumage coloration thanmales that did not pair, and males with redder plumage tendedto nest earlier than males with less red plumage. Here we showthat these patterns continued over 6 years and at two widely separatedlocations. We also tested whether the symmetry of carotenoid-based crownpigmentation differed between paired and unpaired males andfound that paired males have, on average, more perfect symmetryof crown pigmentation than males not paired. These observationssupport the idea that expression of carotenoid-based plumagecoloration by males is a persistent and widespread criterionin female mate choice in the house finch.     

Convergent evolution of sexual shape dimorphism in Diptera

Several patterns of sexual shape dimorphism, such as male body elongation, eye stalks, or extensions of the exoskeleton, have evolved repeatedly in the true flies (Diptera). Although these dimorphisms may have evolved in response to sexual selection on male body shape, conserved genetic factors may have contributed to this convergent evolution, resulting in stronger phenotypic convergence than might be expected from functional requirements alone. I compared phenotypic variation in body shape in two distantly related species exhibiting sexually dimorphic body elongation: Prochyliza xanthostoma (Piophilidae) and Telostylinus angusticollis (Neriidae). Although sexual selection appears to act differently on male body shape in these species, they exhibited strikingly similar patterns of sexual dimorphism. Likewise, patterns of within-sex shape variation were similar in the two species, particularly in males: relative elongation of the male head capsule, antenna, and legs was associated with reduced head capsule width and wing length, but was nearly independent of variation in thorax length. However, the two species presented contrasting patterns of static allometry: male sexual traits exhibited elevated allometric slopes in T. angusticollis, but not in P. xanthostoma. These results suggest that a shared pattern of covariation among traits may have channeled the evolution of sexually dimorphic body elongation in these species. Nonetheless, static allometries may have been shaped by species-specific selection pressures or genetic architectures.     

A multivariate view of the evolution of sexual dimorphism

Sexual differences are often dramatic and widespread across taxa. Their extravagance and ubiquity can be puzzling because the common underlying genome of males and females is expected to impede rather than foster phenotypic divergence. Widespread dimorphism, despite a shared genome, may be more readily explained by considering the multivariate, rather than univariate, framework governing the evolution of sexual dimorphism. In the univariate formulation, differences in genetic variances and a low intersexual genetic correlation () can facilitate the evolution of sexual dimorphism. However, studies that have analysed sex‐specific differences in heritabilities or genetic variances do not always find significant differences. Furthermore, many of the reported estimates of are very high and positive. When monomorphic heritabilities and a high are present together, the evolution of sexual dimorphism on a trait‐by‐trait basis is severely constrained. By contrast, the multivariate formulation has greater generality and more flexibility. Although the number of multivariate sexual dimorphism studies is low, almost all support sex‐specific differences in the G (variance‐covariance) matrix; G matrices can differ with respect to size and/or orientation, affecting the response to selection differently between the sexes. Second, whereas positive values of the univariate quantity only hinder positive changes in sexual dimorphism, positive covariances in the intersexual covariance B matrix can either help or hinder. Similarly, the handful of studies reporting B matrices indicate that it is often asymmetric, so that B can affect the evolution of single traits differently between the sexes. Multivariate approaches typically demonstrate that genetic covariances among traits can strongly constrain trait evolution when compared with univariate approaches. By contrast, in the evolution of sexual dimorphism, a multivariate view potentially reveals more opportunities for sexual dimorphism to evolve by considering the effect sex‐specific selection has on sex‐specific G matrices and an asymmetric B matrix.     

Carotenoid-based ornamentation and status signaling in the house finch

The status signaling hypothesis (SSH) was devised primarilyto explain the adaptive significance of avian ornamental colorationduring the nonbreeding season. It proposes that conspicuousmale plumage serves as an honest signal of social status withina population of birds. However, to date this hypothesis hasbeen well tested and supported for only one type of plumage coloration, melanin-based coloration. Carotenoid-based pigmentationis known to positively reveal male health and condition duringmolt in a variety of species, but it is poorly understood whetherthis ornament type can also function as a status signal duringthe winter. We tested the SSH in male house finches (Carpodacusmexicanus) by manipulating the carotenoid-based plumage brightnessof first-year males and then pairing unfamiliar birds of differingcoloration in a series of dominance trials in captivity. Manipulated plumage color was unrelated to win/loss outcome in these trials.Similarly, the natural pigmentation of males was a poor predictorof winter dominance; as in other studies with this species,we found only a weak tendency for naturally drab males to dominatenaturally bright males. These results suggest that carotenoid-basedcoloration is not a reliable indicator of social status inmale house finches during the nonbreeding season. In fact, carotenoid-based coloration may function only in mate choice in this species,and it may be retained throughout the year either because timeconstraints preclude a second plumage molt or because it aidsin pair formation that begins in late winter.     

Environmental enrichment,sexual dimorphism,and brain size in sticklebacks

Evidence for phenotypic plasticity in brain size and the size of different brain parts is widespread, but experimental investigations into this effect remain scarce and are usually conducted using individuals from a single population. As the costs and benefits of plasticity may differ among populations, the extent of brain plasticity may also differ from one population to another. In a common garden experiment conducted with three‐spined sticklebacks (Gasterosteus aculeatus) originating from four different populations, we investigated whether environmental enrichment (aquaria provided with structural complexity) caused an increase in the brain size or size of different brain parts compared to controls (bare aquaria). We found no evidence for a positive effect of environmental enrichment on brain size or size of different brain parts in either of the sexes in any of the populations. However, in all populations, males had larger brains than females, and the degree of sexual size dimorphism (SSD) in relative brain size ranged from 5.1 to 11.6% across the populations. Evidence was also found for genetically based differences in relative brain size among populations, as well as for plasticity in the size of different brain parts, as evidenced by consistent size differences among replicate blocks that differed in their temperature.     

Sexual behaviour and evolution of sexual dimorphism in body size in Jaera (Isopoda Asellota)

Individuals of the genus Jaera do not mate at random. In the species from the Mediterranean group, J. italica and. J. nordmanni, large males and medium sized females are at an advantage and their sizes are positively assorted. These effects are attributable to sexual competition between males. In the Ponlo-caspian species J. istri, no advantage of large males exists, but sexual selection could be the cause for a long passive phase prior to copulation and for normalizing selection upon female size at pairing. In the Atlantic species, J. albifrons, no selection can be ascertained.
Differential mating success in males appears as one of the causes of the evolution of sexual dimorphism in body size, which makes males larger, of equal size, or smaller than females according to the species. The reason for this reversal in dimorphism seems to differ in the two sexes. Sexual selection provides an explanation for the evolution of male size, while the interspecific changes in female length are more likely due to ecological factors.     

A developmental perspective on the evolution of sexual size dimorphism of a moth

Males and females of almost all organisms exhibit sexual differences in body size, a phenomenon called sexual size dimorphism (SSD). How the sexes evolve to be different sizes, despite sharing the same genes that control growth and development, and hence a common genetic architecture, has remained elusive. Here, we show that the genetic architecture (heritabilities and genetic correlations) of the physiological mechanism that regulates size during the last stage of larval development of a moth, differs between the sexes, and thus probably facilitates, rather than hinders, the evolution of SSD. We further show that the endocrine system plays a critical role in generating SSD. Our results demonstrate that knowledge of the genetic architecture underlying the physiological process during development that ultimately produces SSD in adults can elucidate how males and females of organisms evolve to be of different sizes.     

Evolution of sexual dimorphism in phenotypic covariance structure in Phymata

Sexual dimorphism is a consequence of both sex‐specific selection and potential constraints imposed by a shared genetic architecture underlying sexually homologous traits. However, genetic architecture is expected to evolve to mitigate these constraints, allowing the sexes to approach their respective optimal mean phenotype. In addition, sex‐specific selection is expected to generate sexual dimorphism of trait covariance structure (e.g., the phenotypic covariance matrix, P ), but previous empirical work has not fully addressed this prediction. We compared patterns of phenotypic divergence, for three traits in seven taxa in the insect genus Phymata (Reduviidae), to ask whether sexual dimorphism in P is common and whether its magnitude relates to the extent of sexual dimorphism in trait means. We found that sexual dimorphism in both mean and covariance structure was pervasive but also that the multivariate distance between sex‐specific means was correlated with sex differences in the leading eigenvector of P , while accounting for uncertainty in phylogenetic relationships. Collectively, our findings suggest that sexual dimorphism in covariance structure may be a common but underappreciated feature of dioecious populations.     

Isolation and characterization of eight microsatellite loci from the house finch (Carpodacus mexicanus)

I isolated the first set of polymorphic microsatellite markers from the house finch, Carpodacus mexicanus, a well‐studied North American bird species, as part of an effort to compare levels of genetic diversity in introduced and native populations. Here, I describe eight independently assorting microsatellite loci screened for polymorphism using 40 house finches. Polymorphism levels ranged from six to 14 alleles (mean = 10.6), making these markers a powerful tool for paternity and population level analyses of this widely distributed North American species.     

Sexual selection on male size drives the evolution of male‐biased sexual size dimorphism via the prolongation of male development

Sexual size dimorphism (SSD) arises when the net effects of natural and sexual selection on body size differ between the sexes. Quantitative SSD variation between taxa is common, but directional intraspecific SSD reversals are rare. We combined micro‐ and macroevolutionary approaches to study geographic SSD variation in closely related black scavenger flies. Common garden experiments revealed stark intra‐ and interspecific variation: Sepsis biflexuosa is monomorphic across the Holarctic, while S. cynipsea (only in Europe) consistently exhibits female‐biased SSD. Interestingly, S. neocynipsea displays contrasting SSD in Europe (females larger) and North America (males larger), a pattern opposite to the geographic reversal in SSD of S. punctum documented in a previous study. In accordance with the differential equilibrium model for the evolution of SSD, the intensity of sexual selection on male size varied between continents (weaker in Europe), whereas fecundity selection on female body size did not. Subsequent comparative analyses of 49 taxa documented at least six independent origins of male‐biased SSD in Sepsidae, which is likely caused by sexual selection on male size and mediated by bimaturism. Therefore, reversals in SSD and the associated changes in larval development might be much more common and rapid and less constrained than currently assumed.     

A biogeographic reversal in sexual size dimorphism along a continental temperature gradient

The magnitude and direction of sexual size dimorphism (SSD) varies greatly across the animal kingdom, reflecting differential selection pressures on the reproductive and/or ecological roles of males and females. If the selection pressures and constraints imposed on body size change along environmental gradients, then SSD will vary geographically in a predictable way. Here, we uncover a biogeographical reversal in SSD of lizards from Central and North America: in warm, low latitude environments, males are larger than females, but at colder, high latitudes, females are larger than males. Comparisons to expectations under a Brownian motion model of SSD evolution indicate that this pattern reflects differences in the evolutionary rates and/or trajectories of sex‐specific body sizes. The SSD gradient we found is strongly related to mean annual temperature, but is independent of species richness and body size differences among species within grid cells, suggesting that the biogeography of SSD reflects gradients in sexual and/or fecundity selection, rather than intersexual niche divergence to minimize intraspecific competition. We demonstrate that the SSD gradient is driven by stronger variation in male size than in female size and is independent of clutch mass. This suggests that gradients in sexual selection and male–male competition, rather than fecundity selection to maximize reproductive output by females in seasonal environments, are predominantly responsible for the gradient.     

A comparative study on the evolution of reversed size dimorphism in monogamous waders

Sexual dimorphism in size is common in birds. Males are usually larger than females, although in some taxa reversed size dimorphism (RSD) predominates. Whilst direct dimorphism is attributed to sexual selection in males giving greater reproductive access to females, the evolutionary causes of RSD are still unclear. Four different hypotheses could explain the evolution of RSD in monogamous birds: (1) The ‘energy storing’ hypothesis suggests that larger females could accumulate more reserves at wintering or refuelling areas to enable an earlier start to egg laying. (2) According to the ‘incubation ability’ hypothesis, RSD has evolved because large females can incubate more efficiently than small ones. (3) The ‘parental role division’ hypothesis suggests that RSD in monogamous waders has evolved in species with parental role division and uniparental male care of the chicks. It is based on the assumption that small male size facilitates food acquisition in terrestrial habitats where chick rearing takes place and that larger females can accumulate more reserves for egg laying in coastal sites. (3) The ‘display agility’ hypothesis suggests that small males perform better in acrobatic displays presumably involved in mate choice and so RSD may have evolved due to female preference for agile males. I tested these hypotheses in monogamous waders using several comparative methods. Given the current knowledge of the phylogeny of this group, the evolutionary history of waders seems only compatible with the hypothesis that RSD has evolved as an adaptation for increasing display performance in males. In addition, the analysis of wing shape showed that males of species with acrobatic flight displays had wings with higher aspect ratio (wing span/²wing area) than non-acrobatic species, which probably increases flight manoeuvrability during acrobatic displays. In species with acrobatic displays males also had a higher aspect ratio than females although no sexual difference was found in non-acrobatic species. These results suggest that acrobatic flight displays could have produced changes in the morphology of some species and suggest the existence of selection favouring higher manoeuvrability in species with acrobatic flight displays. This supports the validity of the mechanisms proposed by the ‘display agility’ hypothesis to explain the evolution of RSD in waders.     

Sexual dimorphism in relation to current selection in the house finch

Abstract.— Sexual dimorphism is thought to have evolved in response to selection pressures that differ between males and females. Our aim in this study was to determine the role of current net selection in shaping and maintaining contemporary sexual dimorphism in a recently established population of the house finch ( Carpodacus mexicanus ) in Montana. We found strong differences between sexes in direction of selection on sexually dimorphic traits, significant heritabilities of these traits, and a close congruence between current selection and observed sexual dimorphism in Montana house finches. Strong directional selection on sexually dimorphic traits and similar intensities of selection in each sex suggested that sexual dimorphism arises from adaptive responses in males and females, with both sexes being far from their local fitness optimum. This pattern is expected when a recently established population experiences continuous immigration from ecologically distinct areas of a species range or as a result of widely fluctuating selection pressures, as found in our study. Strong and sexually dimorphic selection pressures on heritable morphological traits, in combination with low phenotypic and genetic covariation among these traits during growth, may have accounted for close congruence between current selection and observed sexual dimorphism in the house finch. This conclusion is consistent with the profound adaptive population divergence in sexual dimorphism that accompanied very successful colonization of most of the North America by the house finch over the last 50 years.