Conservation of social effects (Ψ) between two species of Drosophila despite reversal of sexual dimorphism

Indirect genetic effects (IGEs) describe the effect of the genes of social partners on the phenotype of a focal individual. Here, we measure indirect genetic effects using the “coefficient of interaction” (Ψ) to test whether Ψ evolved between Drosophila melanogaster and D. simulans. We compare Ψ for locomotion between ethanol and nonethanol environments in both species, but only D. melanogaster utilizes ethanol ecologically. We find that while sexual dimorphism for locomotion has been reversed in D. simulans, there has been no evolution of social effects between these two species. What did evolve was the interaction between genotype‐specific Ψ and the environment, as D. melanogaster varies unpredictably between environments and D. simulans does not. In this system, this suggests evolutionary lability of sexual dimorphism but a conservation of social effects, which brings forth interesting questions about the role of the social environment in sexual selection.     

Parasitism and the expression of sexual dimorphism

Although a negative covariance between parasite load and sexually selected trait expression is a requirement of few sexual selection models, such a covariance may be a general result of life‐history allocation trade‐offs. If both allocation to sexually selected traits and to somatic maintenance (immunocompetence) are condition dependent, then in populations where individuals vary in condition, a positive covariance between trait expression and immunocompetence, and thus a negative covariance between trait and parasite load, is expected. We test the prediction that parasite load is generally related to the expression of sexual dimorphism across two breeding seasons in a wild salamander population and show that males have higher trematode parasite loads for their body size than females and that a key sexually selected trait covaries negatively with parasite load in males. We found evidence of a weaker negative relationship between the analogous female trait and parasite infection. These results underscore that parasite infection may covary with expression of sexually selected traits, both within and among species, regardless of the model of sexual selection, and also suggest that the evolution of condition dependence in males may affect the evolution of female trait expression.     

The interplay between natural and sexual selection in the evolution of sexual size dimorphism in Sceloporus lizards (Squamata: Phrynosomatidae)

Sexual size dimorphism (SSD) evolves because body size is usually related to reproductive success through different pathways in females and males. Female body size is strongly correlated with fecundity, while in males, body size is correlated with mating success. In many lizard species, males are larger than females, whereas in others, females are the larger sex, suggesting that selection on fecundity has been stronger than sexual selection on males. As placental development or egg retention requires more space within the abdominal cavity, it has been suggested that females of viviparous lizards have larger abdomens or body size than their oviparous relatives. Thus, it would be expected that females of viviparous species attain larger sizes than their oviparous relatives, generating more biased patterns of SSD. We test these predictions using lizards of the genus Sceloporus. After controlling for phylogenetic effects, our results confirm a strong relationship between female body size and fecundity, suggesting that selection for higher fecundity has had a main role in the evolution of female body size. However, oviparous and viviparous females exhibit similar sizes and allometric relationships. Even though there is a strong effect of body size on female fecundity, once phylogenetic effects are considered, we find that the slope of male on female body size is significantly larger than one, providing evidence of greater evolutionary divergence of male body size. These results suggest that the relative impact of sexual selection acting on males has been stronger than fecundity selection acting on females within Sceloporus lizards.     

Sex-limited mutations and the evolution of sexual dimorphism

Abstract.— Although the developmental and genetic mechanisms underlying sex differences are being elucidated in great detail in a number of species, there remains a breach between proximate and evolutionary studies of sexual dimorphism. More precisely, the evolution of sex-limited gene expression at autosomal loci has not been well reasoned using either theoretical or empirical methods. Here, I show that a Mendelian genetic model including elementary details of sexual differentiation provides novel insight into the evolution of sex differences via sex limitation. This model indicates that the nature of allelic effects and the pattern of selection must be known in both sexes to predict the evolution of sex differences. That is, selection interacts with genetic variation for sexual dimorphism to produce unanticipated patterns of trait divergence or convergence between the sexes. Ultimately, this model may explain why previous models for the evolution of sexual dimorphism do not predict the erratic behavior of the sex difference during artificial selection experiments.     

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.     

Microcephaly genes and the evolution of sexual dimorphism in primate brain size

Microcephaly genes are amongst the most intensively studied genes with candidate roles in brain evolution. Early controversies surrounded the suggestion that they experienced differential selection pressures in different human populations, but several association studies failed to find any link between variation in microcephaly genes and brain size in humans. Recently, however, sex‐dependent associations were found between variation in three microcephaly genes and human brain size, suggesting that these genes could contribute to the evolution of sexually dimorphic traits in the brain. Here, we test the hypothesis that microcephaly genes contribute to the evolution of sexual dimorphism in brain mass across anthropoid primates using a comparative approach. The results suggest a link between selection pressures acting on MCPH1 and CENPJ and different scores of sexual dimorphism.     

Low siring success of females with an acquired male function illustrates the legacy of sexual dimorphism in constraining the breakdown of dioecy

Dioecy has often broken down in flowering plants, yielding functional hermaphroditism. We reasoned that evolutionary transitions from dioecy to functional hermaphroditism must overcome an inertia of sexual dimorphism, because modified males or females will express the opposite sexual function for which their phenotypes have been optimised. We tested this prediction by assessing the siring success of monoecious individuals of the plant Mercurialis annua with an acquired male function but that are phenotypically still female‐like. We found that pollen dispersed by female‐like monoecious individuals was ~ 1/3 poorer at siring outcrossed offspring than pollen from monoecious individuals with an alternative male‐like inflorescence. We conclude that whereas dioecy might evolve from functional hermaphroditism by conferring upon individuals certain benefits of sexual specialisation, reversion from a strategy of separate sexes to one of combined sexes must overcome constraints imposed by the advantages of sexual dimorphism. The breakdown of dioecy must therefore often be limited to situations in which outcrossing cannot be maintained and where selection favours a capacity for inbreeding by functional hermaphrodites.     

Cranial ontogeny and sexual dimorphism in two new world monkeys: Alouatta caraya (Atelidae) and Cebus apella (Cebidae)

Pattern of skull development and sexual dimorphism was studied in Cebus apella and Alouatta caraya using univariate, bivariate, and multivariate statistics. In both species, sexual dimorphism develops because the common growth trajectory in males extends and because of differences in growth rates between sexes. The expectation that the ontogenetic bases of adult dimorphism vary interspecifically is well substantiated by this study. A. caraya exhibits transitional dimorphism in its subadult stage, although the condylobasal length, zygomatic breadth, and rostrum length are strongly dimorphic in the final adult stage, being greater in males. Most cranial measurements in C. apella exhibit significant dimorphism in the adult stage, being strongly influenced by a faster rate of growth in males. Sexual dimorphism is also evidenced through sex differences in growth rates in several cranial measurements. These results also indicate that different ontogenetic mechanisms are acting in C. apella and A. caraya and reveal differences in the way through which neotropical primates attain adult sexual dimorphism. J. Morphol. 2011. © 2011 Wiley‐Liss, Inc.     

Sexual dimorphism in striped dolphin (Stenella coeruleoalba) crania from South Africa

This study assessed the extent of sexual dimorphism in striped dolphin (Stenella coeruleoalba) cranial size and shape off the South African coast. Dorsal and ventral features of 60 striped dolphin crania from both the western and eastern coasts of South Africa were analyzed using landmark‐based geometric morphometrics. Although there was no evidence of dimorphism in cranial size, evidence for small, but significant, variation in both dorsal and ventral cranial shape was found between the sexes. The observed dimorphism was partly associated with changes in shape around the temporal fossa, occipital condyle and supraoccipital bone, the nasal bone, and the paraoccipital process and basiocciptal. The temporal fossa serves as an attachment point for the temporal muscle, which functions to close the lower jaw, and the occipital area serves as the anterior insertion of the epaxial muscles, which power the upstroke of the flukes during swimming. Both the paraoccipital process and basiocciptal are associated with the functioning of the hyoid apparatus, which serves as an attachment point for muscles and ligaments involved in feeding and sound production. These findings suggest the possibility of differences in diet, foraging behavior, vocalizations, and locomotion between the sexes of this species.     

Genetic variation of ecophysiological traits in two gynodioecious species of Schiedea (Caryophyllaceae)

Evolution of dimorphic breeding systems may involve changes in ecophysiological traits as well as floral morphology because of greater resource demands on females. Differences between related species suggest that ecophysiological traits should be heritable, and species with higher female frequencies should show greater sexual differentiation. We used modified partial diallel crossing designs to estimate narrow-sense heritabilities and genetic correlations of sex-specific ecophysiological and morphological traits in closely related gynodioecious Schiedea salicaria (13% females) and Schiedea adamantis (39% females). In S. salicaria, hermaphrodites and females differed in photosynthetic rate and specific leaf area (SLA). Narrow-sense heritabilities were significant for stomatal conductance, SLA and inflorescence number in hermaphrodites, and for SLA and inflorescence number in females. Schiedea adamantis had no sexual dimorphism in measured traits; stomatal conductance, stem number and inflorescence number were heritable in females, and stem number was heritable in hermaphrodites. In both species, significant genetic correlations of traits between sexes were rare, indicating that traits can evolve independently in response to sex-differential selection. Significant genetic correlations were detected between certain traits within sexes of both species. Low heritability of some ecophysiological traits may reflect low additive genetic variability or high phenotypic plasticity in these traits.     

Evolution of putative barrier loci at an intermediate stage of speciation with gene flow in campions (Silene)

Understanding the origin of new species is a central goal in evolutionary biology. Diverging lineages often evolve highly heterogeneous patterns of genetic differentiation; however, the underlying mechanisms are not well understood. We investigated evolutionary processes governing genetic differentiation between the hybridizing campions Silene dioica (L.) Clairv. and S. latifolia Poiret. Demographic modelling indicated that the two species diverged with gene flow. The best‐supported scenario with heterogeneity in both migration rate and effective population size suggested that a small proportion of the loci evolved without gene flow. Differentiation (F _ST) and sequence divergence (d _XY) were correlated and both tended to peak in the middle of most linkage groups, consistent with reduced gene flow at highly differentiated loci. Highly differentiated loci further exhibited signatures of selection. In between‐species population pairs, isolation by distance was stronger for genomic regions with low between‐species differentiation than for highly differentiated regions that may contain barrier loci. Moreover, differentiation landscapes within and between species were only weakly correlated, suggesting that linked selection due to shared recombination and gene density landscapes is not the dominant determinant of genetic differentiation in these lineages. Instead, our results suggest that divergent selection shaped the genomic landscape of differentiation between the two Silene species, consistent with predictions for speciation in the face of gene flow.     

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.     

Patterns of growth and sexual size dimorphism in two species of box turtles with environmental sex determination

An adaptive explanation for environmental sex determination is that it promotes sexual size dimorphism when larger size benefits one sex more than the other. That is, if growth rates are determined by environment during development, then it is beneficial to match developmental environment to the sex that benefits more from larger size. However, larger size may also be a consequence of larger size at hatching or growing for a longer time, i.e., delayed age at first reproduction. Therefore, the adaptive significance of sexual size dimorphism and environmental sex determination can only be interpreted within the context of both growth and maturation. In addition, in those animals that continue to grow after maturation, sexual size dimorphism at age of first reproduction could differ from sexual size dimorphism at later ages as growth competes for energy with reproduction and maintenance. I compared growth using annuli on carapace scales in two species of box turtles (Terrapene carolina and T. ornata) that have similar patterns of environmental sex determination but, reportedly, have different patterns of sexual size dimorphism. In the populations I studied, sexual size dimorphism was in the same direction in both species; adult females were, on average, larger than adult males. This was due in part to males maturing earlier and therefore at smaller sizes than females. In spite of similar patterns of environmental sex determination, patterns of growth differed between the species. In T. carolina, males grew faster than females as juveniles but females had the larger asymptotic size. In T. ornata, males and females grew at similar rates and had similar asymptotic sizes. Sexual size dimorphism was greatest at maturation because, although males matured younger and smaller, they grew more as adults. There was, therefore, no consistent pattern of faster growth for females that may be ascribed to developmental temperature. Received: 20 March 1996 / Accepted: 10 March 1998     

Sexual selection and the evolution of secondary sexual traits: sex comb evolution in Drosophila

Sexual selection can drive rapid evolutionary change in reproductive behaviour, morphology and physiology. This often leads to the evolution of sexual dimorphism, and continued exaggerated expression of dimorphic sexual characteristics, although a variety of other alternative selection scenarios exist. Here, we examined the evolutionary significance of a rapidly evolving, sexually dimorphic trait, sex comb tooth number, in two Drosophila species. The presence of the sex comb in both D. melanogaster and D. pseudoobscura is known to be positively related to mating success, although little is yet known about the sexually selected benefits of sex comb structure. In this study, we used experimental evolution to test the idea that enhancing or eliminating sexual selection would lead to variation in sex comb tooth number. However, the results showed no effect of either enforced monogamy or elevated promiscuity on this trait. We discuss several hypotheses to explain the lack of divergence, focussing on sexually antagonistic coevolution, stabilizing selection via species recognition and nonlinear selection. We discuss how these are important, but relatively ignored, alternatives in understanding the evolution of rapidly evolving sexually dimorphic traits.     

Sexual dimorphism and sexual conflict in the diving beetle Agabus uliginosus (L.) (Coleoptera: Dytiscidae)

Sexual conflict can drive intersexual arms races, with female resistance and male persistence traits coevolving antagonistically. Such arms races are well documented in some diving beetles, although the extent of sexual conflict in this family remains unclear. The European dytiscid Agabus uliginosus has a strikingly dimorphic female; individuals from most regions are smooth and male‐like, whereas those from some populations have a strongly roughened dorsum, a trait that has attracted the name dispar. We demonstrate that rough and smooth females differ consistently in the development of dorsal surface microreticulation, and that these females are associated with males that differ in the development of their persistence traits. These findings extend the occurrence of pre‐insemination sexual conflict and associated intrasexual dimorphism in Dytiscidae, and suggest that such mating systems are relatively widespread in these beetles.     

On the sexual dimorphism in the skull of the tiger (Panthera tigris)

Sexual dimorphism in the skull of the tiger (Panthera tigris) is reviewed and described in detail. The most significant diagnostic differences between the sexes are absolute length of the cranium, breadth of interorbital region and muzzle, zygomatic arch, and occipital region, length of upper carnassial, and the degree of the development of the cranial prominences. The degree of sexual dimorphism is closely related to geographic variation, and its form is rather complex.     

Within/between population crosses reveal genetic basis for siring success in Silene latifolia (Caryophyllaceae)

Divergence at reproductive traits can generate barriers among populations, and may result from several mechanisms, including drift, local selection and co-adaptation between the sexes. Intersexual co-adaptation can arise through sexually antagonistic co-evolution, a timely hypothesis addressed in animals but, to our knowledge, not yet in flowering plants. We investigated whether male and female population of origin affected pollen competition success, offspring fitness and sex ratio in crosses within/between six genetically differentiated populations of the white campion, Silene latifolia. Each female was crossed with pollen from one focus male from the same population, and pollen from two focus males from two distinct populations, both as single-donor and two-donor crosses against a fixed tester male with a 2-h interpollination interval (n = 288 crosses). We analysed paternity with microsatellite DNA. Male populations of origin significantly differed for siring success and in vitro pollen germination rates. In vitro pollen germination rate was heritable. Siring success also depended on sex ratio in the female family of origin, but only in between-population crosses. In some female populations, two-donor crosses produced less female-biased sex ratios compared with single-donor crosses, yet in other female populations the reverse was true. Offspring sex ratio varied with donor number, depending on the female population. Within/between population crosses did not differ significantly in seed set or offspring fitness, nor were siring success and offspring fitness significantly correlated. Altogether this suggests reproductive divergence for traits affecting pollen competition in S. latifolia.     

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.