Components of phenotypic variation in avian ornamental and non-ornamental feathers

Phenotypic variation, measured as the coefficient of variation (CV), is usually larger in secondary sexual characters than in ordinary morphological traits. We tested if intraspecific differences in the CV between ornamental and non-ornamental feather traits in 67 evolutionary events of feather ornamentation in birds were due to differences in (1) the allometric pattern (slope of the regression line when regressing trait size on an indicator of body size), or (2) the dispersion of observations around the regression line. We found that only dispersion of observations around the regression line contributed significantly to total variation. A large dispersion of observations around the regression line for ornamental feathers is consistent with these characters showing condition-dependence, supporting indicator models of sexual selection more strongly than a pure Fisher process. Ornamental feathers in males demonstrated negative allometry when regressed on tarsus length, which is a measure of skeletal body size. This finding is consistent with ornamental feather traits being subject to directional selection due to female mate preferences, where large body size is less important than in male–male competition. This pattern of phenotypic variation for avian secondary sexual characters contrasts with patterns of variation for insect genitalia, supposedly subject to sexual selection, since the latter traits only differ from ordinary morphology traits in allometry coefficient. The prevailing regime of selection (directional or stabilizing) and the effects of environmental factors are proposed to account for these differences among traits.     

The allometric pattern of sexually size dimorphic feather ornaments and factors affecting allometry

The static allometry of secondary sexual characters is currently subject to debate. While some studies suggest an almost universal positive allometry for such traits, but isometry or negative allometry for nonornamental traits, other studies maintain that any kind of allometric pattern is possible. Therefore, we investigated the allometry of sexually size dimorphic feather ornaments in 67 species of birds. We also studied the allometry of female feathers homologous to male ornaments (female ornaments in the following) and ordinary nonsexual traits. Allometries were estimated as reduced major axis slopes of trait length on tarsus length. Ornamental feathers showed positive allometric slopes in both sexes, although that was not a peculiarity for ornamental feathers, because nonsexual tail feathers also showed positive allometry. Migration distance (in males) and relative size of the tail ornament (in females) tended to be negatively related to the allometric slope of tail feather ornaments, although these results were not conclusive. Finally, we found an association between mating system and allometry of tail feather ornaments, with species with more intense sexual selection showing a smaller degree of allometry of tail ornaments. This study is consistent with theoretical models that predict no specific kind of allometric pattern for sexual and nonsexual characters.     

Multiple speciation events in an arthropod with divergent evolution in sexual morphology

Sexual selection can facilitate divergent evolution of traits related to mating and consequently promote speciation. Theoretically, independent operation of sexual selection in different populations can lead to divergence of sexual traits among populations and result in allopatric speciation. Here, we show that divergent evolution in sexual morphology affecting mating compatibility (body size and genital morphologies) and speciation have occurred in a lineage of millipedes, the Parafontaria tonominea species complex. In this millipede group, male and female body and genital sizes exhibit marked, correlated divergence among populations, and the diverged morphologies result in mechanical reproductive isolation between sympatric species. The morphological divergence occurred among populations independently and without any correlation with climatic variables, although matching between sexes has been maintained, suggesting that morphological divergence was not a by-product of climatic adaptation. The diverged populations underwent restricted dispersal and secondary contact without hybridization. The extent of morphological difference between sympatric species is variable, as is diversity among allopatric populations; consequently, the species complex appears to contain many species. This millipede case suggests that sexual selection does contribute to species richness via morphological diversification when a lineage of organisms consists of highly divided populations owing to limited dispersal.     

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.     

Morphological divergence within and between the Mexican sailfin mollies, Poecilia velifera and Poecilia petenensis

This study examined the patterns of morphological variation both between species, and between sexes and among populations within each species of the Mexican sailfin mollies, Poecilia velifera and Poecilia petenensis , using geometric morphometrics and linear measurements of morphological traits. While sexes within each species differed in characteristics that may be important in sexual selection, such as length of the dorsal fin, species differed in traits, such as body depth, that may also be influenced by natural selection due to differences in habitats. Within each species, many morphological traits were similar among populations, but important differences, including caudal peduncle depth in P. petenensis (but not in P. velifera ), suggested that habitat differences may also be important in shaping population divergence independently within each species. Indeed, the evolutionary vectors of male morphological population divergence for each species differed by an angle of 98·5°, representing nearly orthogonal vectors and suggesting independent shape divergence between these two molly species. Finally, geographic isolation did not explain the morphological differentiation seen among populations, suggesting that natural and sexual selection were strong forces promoting morphological diversification within these two species, despite the potential for a high degree of population connectivity and gene flow.     

Sexual selection and the evolution of genital shape and complexity in water striders

Animal genitalia show two striking but incompletely understood evolutionary trends: a great evolutionary divergence in the shape of genitalic structures, and characteristic structural complexity. Both features are thought to result from sexual selection, but explicit comparative tests are hampered by the fact that it is difficult to quantify both morphological complexity and divergence in shape. We undertake a comparative study of multiple nongenitalic and male genital traits in a clade of 15 water strider species to quantify complexity and shape divergence. We show that genital structures are more complex and their shape more divergent among species than nongenital traits. Further, intromittent genital traits are more complex and have evolved more divergently than nonintromittent genital traits. More importantly, shape and complexity of nonintromittent genital traits show correlated evolution with indices of premating sexual selection and intromittent genital traits with postmating sexual selection, suggesting that the evolution of different components of genital morphology are shaped independently by distinct forms of sexual selection. Our quantitative results provide direct comparative support for the hypothesis that sexual selection is associated with morphological complexity in genitalic traits and highlight the importance of quantifying morphological shape and complexity, rather than size in studies of genital evolution.     

Phenotypic variation and fluctuating asymmetry in sexually dimorphic feather ornaments in relation to sex and mating system

Secondary sexual characters have been hypothesized to demonstrate increased phenotypic variation between and within individuals as compared to ordinary morphological traits. We tested whether this was the case by studying phenotypic variation, expressed as the coefficient of variation (CV), and developmental instability, measured as fluctuating asymmetry (FA), in ornamental and non-ornamental traits of 70 bird species with feather ornamentation while controlling for similarity among species due to common descent. Secondary sexual characters differed from ordinary morphological traits by showing large phenotypic CV and FA. This difference can be explained by the different mode of selection operating on each kind of trait: a history of intense directional (ornaments) and stabilizing selection (non-ornaments). Phenotypic variation is reduced in the sex with more intense sexual selection (males), but does not differ among species with different mating systems. The strength of stabilizing selection arising from natural selection is associated with decreased CV (wing CV is smaller than tarsus or tail CVs). We found evidence of FA being reduced in ornamental feathers strongly affected by aerodynamics (tail feathers) compared to other ornaments, but only in females. In conclusion, CV and FA were not related, suggesting mat phenotypic plasticity and developmental instability are independent components of phenotypic variation.     

Intralocus sexual conflict and the genetic architecture of sexually dimorphic traits in Prochyliza xanthostoma (Diptera: Piophilidae)

Because homologous traits of males and females are likely to have a common genetic basis, sex-specific selection (often resulting from sexual selection on one sex) may generate an evolutionary tug-of-war known as intralocus sexual conflict, which will constrain the adaptive divergence of the sexes. Theory suggests that intralocus sexual conflict can be mitigated through reduction of the intersexual genetic correlation (rMF), predicting negative covariation between rMF and sexual dimorphism. In addition, recent work showed that selection should favor reduced expression of alleles inherited from the opposite-sex parent (intersexual inheritance) in traits subject to intralocus sexual conflict. For traits under sexual selection in males, this should be manifested either in reduced maternal heritability or, when conflict is severe, in reduced heritability through the opposite-sex parent in offspring of both sexes. However, because we do not know how far these hypothesized evolutionary responses can actually proceed, the importance of intralocus sexual conflict as a long-term constraint on adaptive evolution remains unclear. In this study, we investigated the genetic architecture of sexual and nonsexual morphological traits in Prochyliza xanthostoma. The lowest rMF and greatest dimorphism were exhibited by two sexual traits (head length and antenna length) and, among all traits, the degree of sexual dimorphism was correlated negatively with rMF. Moreover, sexual traits exhibited reduced maternal heritabilities, and the most strongly dimorphic sexual trait (antenna length) was heritable only through the same-sex parent in offspring of both sexes. Our results support theory and suggest that intralocus sexual conflict can be resolved substantially by genomic adaptation. Further work is required to identify the proximate mechanisms underlying these patterns.     

Variation in Body Shape across Species and Populations in a Radiation of Diaptomid Copepods

Inter and intra-population variation in morphological traits, such as body size and shape, provides important insights into the ecological importance of individual natural populations. The radiation of Diaptomid species (~400 species) has apparently produced little morphological differentiation other than those in secondary sexual characteristics, suggesting sexual, rather than ecological, selection has driven speciation. This evolutionary history suggests that species, and conspecific populations, would be ecologically redundant but recent work found contrasting ecosystem effects among both species and populations. This study provides the first quantification of shape variation among species, populations, and/or sexes (beyond taxonomic illustrations and body size measurements) to gain insight into the ecological differentiation of Diaptomids. Here we quantify the shape of five Diaptomid species (family Diaptomidae) from four populations each, using morphometric landmarks on the prosome, urosome, and antennae. We partition morphological variation among species, populations, and sexes, and test for phenotype-by-environment correlations to reveal possible functional consequences of shape variation. We found that intraspecific variation was 18-35% as large as interspecific variation across all measured traits. Interspecific variation in body size and relative antennae length, the two traits showing significant sexual dimorphism, were correlated with lake size and geographic location suggesting some niche differentiation between species. Observed relationships between intraspecific morphological variation and the environment suggest that divergent selection in contrasting lakes might contribute to shape differences among local populations, but confirming this requires further analyses. Our results show that although Diaptomid species differ in their reproductive traits, they also differ in other morphological traits that might indicate ecological differences among species and populations.     

Evolutionary allometry reveals a shift in selection pressure on male horn size

How selection pressures acting within species interact with developmental constraints to shape macro‐evolutionary patterns of species divergence is still poorly understood. In particular, whether or not sexual selection affects evolutionary allometry, the increase in trait size with body size across species, of secondary sexual characters, remains largely unknown. In this context, bovid horn size is an especially relevant trait to study because horns are present in both sexes, but the intensity of sexual selection acting on them is expected to vary both among species and between sexes. Using a unique data set of sex‐specific horn size and body mass including 91 species of bovids, we compared the evolutionary allometry between horn size and body mass between sexes while accounting for both the intensity of sexual selection and phylogenetic relationship among species. We found a nonlinear evolutionary allometry where the allometric slope decreased with increasing species body mass. This pattern, much more pronounced in males than in females, suggests either that horn size is limited by some constraints in the largest bovids or is no longer the direct target of sexual selection in very large species.     

Geographical variation of genetic and phenotypic traits in the Mexican sailfin mollies, Poecilia velifera and P. petenensis

Comparing the patterns of population divergence using both neutral genetic and phenotypic traits provides an opportunity to examine the relative importance of evolutionary mechanisms in shaping population differences. We used microsatellite markers to examine population genetic structure in the Mexican sailfin mollies Poecilia velifera and P. petenensis. We compared patterns of genetic structure and divergence to that in two types of phenotypic traits: morphological characters and mating behaviours. Populations within each species were genetically distinct, and conformed to a model of isolation by distance, with populations within different geographical regions being more genetically similar to one another than were populations from different regions. Bayesian clustering and barrier analyses provided additional support for population separation, especially between geographical regions. In contrast, none of the phenotypic traits showed any type of geographical pattern, and population divergence in these traits was uncorrelated with that found in neutral markers. There was also a weaker pattern of regional differences among geographical regions compared to neutral genetic divergence. These results suggest that while divergence in neutral traits is likely a product of population history and genetic drift, phenotypic divergence is governed by different mechanisms, such as natural and sexual selection, and arises at spatial scales independent from those of neutral markers.     

Sexual variation in heritability and genetic correlations of morphological traits in house sparrow (Passer domesticus)

Estimates of genetic components are important for our understanding of how individual characteristics are transferred between generations. We show that the level of heritability varies between 0.12 and 0.68 in six morphological traits in house sparrows (Passer domesticus L.) in northern Norway. Positive and negative genetic correlations were present among traits, suggesting evolutionary constraints on the evolution of some of these characters. A sexual difference in the amount of heritable genetic variation was found in tarsus length, wing length, bill depth and body condition index, with generally higher heritability in females. In addition, the structure of the genetic variance-covariance matrix for the traits differed between the sexes. Genetic correlations between males and females for the morphological traits were however large and not significantly different from one, indicating that sex-specific responses to selection will be influenced by intersexual differences in selection differentials. Despite this, some traits had heritability above 0.1 in females, even after conditioning on the additive genetic covariance between sexes and the additive genetic variances in males. Moreover, a meta-analysis indicated that higher heritability in females than in males may be common in birds. Thus, this indicates sexual differences in the genetic architecture of birds. Consequently, as in house sparrows, the evolutionary responses to selection will often be larger in females than males. Hence, our results suggest that sex-specific additive genetic variances and covariances, although ignored in most studies, should be included when making predictions of evolutionary changes from standard quantitative genetic models.     

Developmental stability,sexual selection and speciation

Fluctuating asymmetry occurs when an individual is unable to undergo identical development of an otherwise bilaterally symmetric trait on both sides of its body. Since both sides of a bilaterally symmetric trait are the result of the actions of a single genome, fluctuating asymmetry represents an epigenetic measure of the sensitivity of development to stress. Different morphological traits may show a direct relationship between their functional importance and their degree of developmental canalization. This may explain why some characters show high degrees of fluctuating asymmetry, and why these characters more often become exaggerated secondary sexual ornaments. The degree of fluctuating asymmetry is generally larger in small marginal populations living in novel environments, and this will particularly lead to relatively large degrees of asymmetry in the least developmentally canalized traits. More stringent selection against heterozygotes in marginal populations may further break down developmental stability and linkage groups which would lead to increased genetic variance. Females may prefer to mate with males having large, but relatively symmetric morphological characters, because it is more difficult to make large traits (a good genes argument), a large trait is more easily perceived (a sensory bias preference), and because symmetry signals ability to cope with stress (a good genes argument). The low degree of developmental stability and the large amount of genetic variance in secondary sexual characters in small, marginal populations could set the scene for rapid development of divergence and speciation in marginal populations.     

Sexual dimorphism in the tusked frog, Adelotus brevis (Anura:Myobatrachidae): the roles of natural and sexual selection

At least two adaptive processes can lead to the evolution of sexual dimorphism: sexual selection (e.g. male-male combat) or natural selection (e.g. dietary divergence). We investigated the adaptive significance of a distinctive pattern of sexual dimorphism in a south-eastern Australian frog, Adelotus brevis. Male Adelotus grow larger than female conspecifics, have larger heads relative to body size, and have large paired projections (‘tusks’) in the lower jaw. All of these traits are rare among anurans. We quantified the degree of dimorphism in Adelotus, and gathered data on diets and mating systems of this species to evaluate the possible roles of sexual selection and dietary divergence in favoring die evolution of these sexually dimorphic traits. Analysis of prey items in alimentary tracts revealed significant sex differences in prey types. For example, females ate proportionally more arthropods and fewer molluscs than did males. However, this difference is likely to be a secondary consequence of habitat differences between the sexes (due in turn to their different reproductive roles) rather than a selective force for the evolution of sexual dimorphism. Calling males spend their time in moist habitats where pondsnails are abundant, whereas females are more often encountered in the drier arthropod-rich woodlands. A three-year behavioural ecology study on a field population revealed that reproductive males engage in agonistic interactions, with the sexually dimorphic tusks used to attack rivals. Larger body size contributed to male reproductive success. Small males were excluded from calling sites and, among the calling males, larger animals had higher reproductive success (numbers of matings) than did smaller individuals. Hence, the atypical pattern of sexual dimorphism in Adelotus brevis seems to have resulted from sexual selection for larger body size and tusk size in males, in the context of male-male agonistic behaviour, rather than natural selection for ecological divergence between the sexes.     

Evidence for stabilizing selection and slow divergent evolution of male genitalia in a millipede (Antichiropus variabilis)

It is generally accepted that postcopulatory sexual selection drives rapid divergence of genital morphology among isolated populations. The mode of selection operating upon genitalia can be explored by comparing patterns of population divergence in genetic and genitalic traits. We collected Antichiropus variabilis millipedes from eight localities across the species range. Levels of among-population genetic divergence, at microsatellite loci, and the mitochondrial COI gene were very high. Following geometric morphometric analyses, genital morphology was also found to be highly divergent among the populations surveyed, whereas head morphology had not diverged as markedly. However, pairwise comparisons of F(ST) and P(ST) showed that among-population divergence in both genital and head shape was significantly lower than that experienced by neutral genetic markers. Our results suggest that the genitalia of A. variabilis are currently experiencing a period of stabilizing selection, the mode of selection expected for genitalia that function in species recognition via a "lock-and-key" mechanism. Our results demonstrate that although genital morphology can clearly diverge among genetically isolated populations, divergence is not necessarily as rapid as commonly argued, and continuous directional sexual selection may not always underpin the evolutionary divergence of male genitalia.     

Molecular population divergence and sexual selection on morphology in the banded demoiselle (Calopteryx splendens)

The importance of sexual selection in population divergence is of much interest, mainly because it is thought to cause reproductive isolation and hence could lead to speciation. Sexually selected traits have been hypothesized to diverge faster between populations than other traits, presumably because of differences in the strength, mechanism or dynamics of selection. We investigated this by quantifying population divergence in eight morphological characters in 12 south Swedish populations of a sexually dimorphic damselfly, the banded demoiselle (Calopteryx splendens). The morphological characters included a secondary sexual character, the male melanized wing spot, which has an important function in both inter- and intrasexual selection. In addition, we investigated molecular population divergence, revealed by amplified fragment length polymorphism (AFLP) analysis. Molecular population divergence was highly significant among these Northern European populations (overall F(st)=0.054; pairwise population F(st)'s ranged from approximately 0 to 0.13). We found evidence for isolation-by-distance (r=0.70) for the molecular markers and a significant correlation between molecular and phenotypic population divergence (r=0.39). One interpretation is that population divergence for the AFLP loci are affected by genetic drift, but is also indirectly influenced by selection, due to linkage with loci for the phenotypic traits. Field estimates of sexual and natural selection from two of the populations revealed fairly strong sexual selection on wing spot length, indicating that this trait has the potential to rapidly diverge, provided that variation is heritable and the observed selection is chronic.     

Rapid antagonistic coevolution between primary and secondary sexual characters in horned beetles

Different structures may compete during development for a shared and limited pool of resources to sustain growth and differentiation. The resulting resource allocation trade-offs have the potential to alter both ontogenetic outcomes and evolutionary trajectories. However, little is known about the evolutionary causes and consequences of resource allocation trade-offs in natural populations. Here, we explore the significance of resource allocation trade-offs between primary and secondary sexual traits in shaping early morphological divergences between four recently separated populations of the horned beetle Onthophagus taurus as well as macroevolutionary divergence patterns across 10 Onthophagus species. We show that resource allocation trade-offs leave a strong signature in morphological divergence patterns both within and between species. Furthermore, our results suggest that genital divergence may, under certain circumstances, occur as a byproduct of evolutionary changes in secondary sexual traits. Given the importance of copulatory organ morphology for reproductive isolation our findings begin to raise the possibility that secondary sexual trait evolution may promote speciation as a byproduct. We discuss the implications of our results on the causes and consequences of resource allocation trade-offs in insects.     

Evolution of male sexual characters in the oriental Drosophila melanogaster species group

Understanding the genetic and molecular mechanisms of morphological evolution is one of the greatest challenges in evolutionary biology. Sexually dimorphic traits, which often evolve at a high rate due to their involvement in mate choice and sexual selection, present unique opportunities for investigating changes in development over short evolutionary distances. Phylogenetic analysis is essential to provide a historical framework for comparative studies of development by establishing the order and polarity of morphological changes. In this report, we apply a new molecular phylogeny to reconstruct the evolution of male sexual characters in a group of species closely related to the model species Drosophila melanogaster. These highly variable traits include wing melanin patterns, the sex comb, and the structure of external genitalia and analia. We show that sexually dimorphic characters can diverge very rapidly among closely related species. More surprisingly, we also find a pervasive pattern of independent origin and secondary loss of male sexual traits in different evolutionary lineages.     

Patterns of fluctuating asymmetry in sexual ornaments predict female choice

Extravagant secondary sexual characters are assumed to have arisen and be maintained by sexual selection. While traits like horns, antlers and spurs can be ascribed to intrasexual competition, other traits such as extravagant feather ornaments, displays and pheromones have to be ascribed to mate choice. A number of studies have tested whether females exert selection on the size of male ornaments, but only some of these have recorded female preferences for the most extravagantly ornamented males. Here I demonstrate that female choice can be directly predicted from the relationship between the degree of fluctuating asymmetry and the size of a secondary sexual character. Fluctuating asymmetry is an epigenetic measure of the ability of individuals to cope with stress, and it occurs when an individual is unable to undergo identical development of an otherwise bilaterally symmetric trait on both sides of its body. There is a negative relationship between the degree of fluctuating asymmetry and the absolute size of an ornament in those bird species with a female preference for the largest male sex trait, while there is a flat or U-shaped relationship among species without a female preference. These results suggest that females prefer exaggerated secondary sexual characters if they reliably demonstrate the ability of males to cope with genetic and environmental stress. Some species may demonstrate a flat or U-shaped relationship between the degree of fluctuating asymmetry and the absolute size of an ornament because (i) the genetic variance in viability signalled by the secondary sex trait has been depleted; (ii) the secondary sex trait is not particularly costly and therefore does not demonstrate condition dependence; or because (iii) the sex traits can be considered arbitrary traits rather than characters reflecting good genes.     

Rates of phenotypic evolution of ecological characters and sexual traits during the Tanganyikan cichlid adaptive radiation

Theory suggests that sexual traits evolve faster than ecological characters. However, characteristics of a species niche may also influence evolution of sexual traits. Hence, a pending question is whether ecological characters and sexual traits present similar tempo and mode of evolution during periods of rapid ecological divergence, such as adaptive radiation. Here, we use recently developed phylogenetic comparative methods to analyse the temporal dynamics of evolution for ecological and sexual traits in Tanganyikan cichlids. Our results indicate that whereas disparity in ecological characters was concentrated early in the radiation, disparity in sexual traits remained high throughout the radiation. Thus, closely related Tanganyikan cichlids presented higher disparity in sexual traits than ecological characters. Sexual traits were also under stronger selection than ecological characters. In sum, our results suggest that ecological characters and sexual traits present distinct evolutionary patterns, and that sexual traits can evolve faster than ecological characters, even during adaptive radiation.