Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila

In the fruitfly, Drosophila melanogaster, mate choice during courtship depends on detecting olfactory cues, sex pheromones, which are initially processed in the antennal lobe (AL), a primary olfactory centre of the brain. However, no sexual differences in the structure of the AL have been found in Drosophila. We compared the central brain anatomy of 37 species of Drosophilidae from the islands of the Hawaiian archipelago, uncovering an extreme sexual dimorphism within the AL in which two out of the 51 identifiable glomeruli were markedly enlarged in males. A phylogeny indicated that the sexual dimorphism of the homologous glomeruli arose 0.4-1.9 Myr ago independently in two species groups of Hawaiian endemic Drosophilidae. The corresponding glomeruli in D. melanogaster were also found to be sexually dimorphic. The formation of glomeruli of male size is prevented by the ectopic expression of female-type transformer (tra) cDNA in males, indicating that the glomerular sexual dimorphism is under the control of the sex-determination cascade of genes. It is suggested that a defined set of glomeruli in Drosophila can enlarge in response to sex-determination genetic signals, the mutations of which may result in species differences in sexual dimorphism of the brain.     

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.     

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.     

Mammalian sexual dimorphism

Sexual dimorphisms (SDs) have evolved in mammals to assure greater reproductive success for individuals, usually males. Secondary sexual characteristics (SSC) developed to further this objective, tending to be more pronounced in species which are polygynous, diurnal and open-habitat dwellers. Sexual selection has underpinned many of these changes, which are not necessarily advantageous for individual survival. Domestication has affected certain characteristics, more in terms of their quantitative rather than qualitative expression. However, restrictions imposed by domestication can also affect behaviors such as isolation and post-natal bonding while artificial selection can, by focusing on certain traits, cause unforeseen effects in genetically linked traits, which, when sex-specific or sex-linked, can be reflected in SD. On a global scale, environmental changes can have important phylogenetic implications for species which rely upon environmental cues for activities as migration, hibernation and breeding, especially when SD occurs in response to such cues. Understanding the evolutionary rationale behind the development of SDs, as well as the dynamics which occur at the interface between natural and artificial selection, allows positive insights into areas as diverse as wildlife preservation and livestock management. For both, greatest "success" should be achieved when artificial selection occurs in harmony with natural selection within a supportive environment. Thus the aim of this review is to discuss current knowledge relating to the evolution, benefits and costs of mammalian sexual dimorphisms and, where possible, draw conclusions that might be beneficial for the husbandry and propagation of mammals today.     

Establishing sexual dimorphism in humans

Sexual dimorphism, i.e. the distinct recognition of only two sexes per species, is the phenotypic expression of a multi-stage procedure at chromosomal, gonadal, hormonal and behavioral level. Chromosomal--genetic sexual dimorphism refers to the presence of two identical (XX) or two different (XY) gonosomes in females and males, respectively. This is due to the distinct content of the X and Y-chromosomes in both genes and regulatory sequences, SRY being the key regulator Hormones (AMH, testosterone, Insl3) secreted by the foetal testis (gonadal sexual dimorphism), impede Müller duct development, masculinize Wolff duct derivatives and are involved in testicular descent (hormonal sexual dimorphism). Steroid hormone receptors detected in the nervous system, link androgens with behavioral sexual dimorphism. Furthermore, sex chromosome genes directly affect brain sexual dimorphism and this may precede gonadal differentiation.     

Pelvic sexual dimorphism and relative neonatal brain size really are related

Primate species in which the neonatal brain size is large relative to the birth canal tend to have more sexually dimorphic pelves: this is a classic comparative relation, discovered by Schultz and Leutenegger. The original work did not correct for phylogenetic nonindependence of the data points; it only partly corrected for body size; it used ratios in both variables, and the size of the female pubis featured in both x- and y-variables. A recent publication by Tague placed a question mark over the validity of the relation. I therefore retested it, correcting for all four statistical defects. A strongly significant statistical relation exists. © 1995 Wiley-Liss, Inc.     

Disproportionate sexual dimorphism in the human face

Analysis of facial dimensions of 86 young adults and their 76 parents indicates that a disproportionate sexual dimorphism exists in the ramus of the mandible, demonstrating a regional difference in growth response. The male ramus is on the average 14% longer than the female ramus, whereas other facial dimensions approximate an 8% sex difference. The findings have relevance to the analysis of skeletal remains and suggest the desirability of age specific discriminant function analysis for the sexing of adult mandibles.     

Reversed brain size sexual dimorphism accompanies loss of parental care in white sticklebacks

Uncovering factors that shape variation in brain morphology remains a major challenge in evolutionary biology. Recently, it has been shown that brain size is positively associated with level of parental care behavior in various taxa. One explanation for this pattern is that the cognitive demands of performing complex parental care may require increased brain size. This idea is known as the parental brain hypothesis (PBH). We set out to test the predictions of this hypothesis in wild populations of threespine stickleback (Gasterosteus aculeatus). These fish are commonly known to exhibit (1) uniparental male care and (2) sexual dimorphism in brain size (males>females). To test the PBH, we took advantage of the existence of closely related populations of stickleback that display variation in parental care behavior: common marine threespine sticklebacks (uniparental male care) and white threespine sticklebacks (no care). To begin, we quantified genetic differentiation among two common populations and three white populations from Nova Scotia. We found overall low differentiation among populations, although F_ST was increased in between‐type comparisons. We then measured the brain weights of males and females from all five populations along with two additional common populations from British Columbia. We found that sexual dimorphism in brain size is reversed in white stickleback populations: males have smaller brains than females. Thus, while several alternatives need to be ruled out, the PBH appears to be a reasonable explanation for sexual dimorphism in brain size in threespine sticklebacks.     

Socio-bioenergetics and sexual dimorphism in primates

Socio-bioenergetics is presented as a practical method of estimating energy budgets of primates in a social context. Energy budgets are estimated on the basis of behavioral observations and a series of empirical formulae, which consider body weight, activity, and reproductive status. Data on a captive colony of Sykes' monkeys and baboons are incorporated as illustrations of the possible effects of group composition, body size, reproductive status, and activity patterns on energy requirements.Supported by the Wenner-Gren Foundation for Anthropological Research Incorporated and the National Science Foundation Grant GU-1598.     

Measuring sexual size dimorphism in birds

Vocal displays are supposed to be an honest signal of the phenotypic and genetic quality of individuals and their territory. Moreover, signal interactions are nearly always associated with individuals in aggregations, and their function could in part be explained as social behaviour. Conspecific density has been shown to be a particularly strong proximate and ultimate factor acting on several individual/population features; thus, it may be expected to affect vocal behaviour too. Here, I investigate the hypothesis that, in long-lived, territorial species, density affects the vocal displays of mated males, masking their honesty as a possible signal of male/territory quality. Each month I listened to the dusk calls of 17 breeding male Eurasian Eagle Owls Bubo bubo during their prelaying period. Nine males bred in a low-density situation, the other eight in a high-density one. Conspecific density was found to affect the honesty of call features as signals of male and/or territory quality. The call display as a reliable predictor of male fitness measured as productivity persisted only in situations of high breeding owl density, where male–male competition was stronger. Accommodation of call activity allows individuals to minimize the costs of aggressive calling by adjusting the territoriality threshold to local conditions. The results of this study emphasize the importance, when investigating the evolution and maintenance of honest territorial or sexual signals, of considering the environmental and social context experienced by the individual, thereby corroborating the idea that male–male competition contributes to the maintenance of honest signalling.     

On sexual dimorphism in immune function

Sexual dimorphism in immune function is a common pattern in vertebrates and also in a number of invertebrates. Most often, females are more 'immunocompetent' than males. The underlying causes are explained by either the role of immunosuppressive substances, such as testosterone, or by fundamental differences in male and female life histories. Here, we investigate some of the main predictions of the immunocompetence handicap hypothesis (ICHH) in a comparative framework using mammals. We focus specifically on the prediction that measures of sexual competition across species explain the observed patterns of variation in sex-specific immunocompetence within species. Our results are not consistent with the ICHH, but we do find that female mammals tend to have higher white blood cell counts (WBC), with some further associations between cell counts and longevity in females. We also document positive covariance between sexual dimorphism in immunity, as measured by a subset of WBC, and dimorphism in the duration of effective breeding. This is consistent with the application of 'Bateman's principle' to immunity, with females maximizing fitness by lengthening lifespan through greater investment in immune defences. Moreover, we present a meta-analysis of insect immunity, as the lack of testosterone in insects provides a means to investigate Bateman's principle for immunity independently of the ICHH. Here, we also find a systematic female bias in the expression of one of the two components of insect immune function that we investigated (phenoloxidase). From these analyses, we conclude that the mechanistic explanations of the ICHH lack empirical support. Instead, fitness-related differences between the sexes are potentially sufficient to explain many natural patterns in immunocompetence.     

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.     

Development of sexual dimorphism in the embryonic gonad

Summary Differentiation of gonads in embryonic pigs (ages 24 to 44 days) was studied by light and electron microscopy. Incipient short cord-like structures were seen in embryos of both sexes at the age of 24 days. The cords were ultrastructurally similar. Medullary cords appeared in the testis at 26 days and in the ovary at 28 days. The cords in the ovary degenerated gradually and new cortical cords started to develop at 34 days. The formation of cords in both sexes is difficult to explain with the H-Y antigen theory, according to which the antigen should organize cords only in the male. The present results indicate that new approaches are needed for further development of the H-Y antigen theory.     

On the origins of sexual dimorphism in butterflies

The processes governing the evolution of sexual dimorphism provided a foundation for sexual selection theory. Two alternative processes, originally proposed by Darwin and Wallace, differ primarily in the timing of events creating the dimorphism. In the process advocated by Darwin, a novel ornament arises in a single sex, with no temporal separation in the origin and sex-limitation of the novel trait. By contrast, Wallace proposed a process where novel ornaments appear simultaneously in both sexes, but are then converted into sex-limited expression by natural selection acting against showy coloration in one sex. Here, we investigate these alternative modes of sexual dimorphism evolution in a phylogenetic framework and demonstrate that both processes contribute to dimorphic wing patterns in the butterfly genera Bicyclus and Junonia. In some lineages, eyespots and bands arise in a single sex, whereas in other lineages they appear in both sexes but are then lost in one of the sexes. In addition, lineages displaying sexual dimorphism were more likely to become sexually monomorphic than they were to remain dimorphic. This derived monomorphism was either owing to a loss of the ornament ('drab monomorphism') or owing to a gain of the same ornament by the opposite sex ('mutual ornamentation'). Our results demonstrate the necessity of a plurality in theories explaining the evolution of sexual dimorphism within and across taxa. The origins and evolutionary fate of sexual dimorphism are probably influenced by underlying genetic architecture responsible for sex-limited expression and the degree of intralocus sexual conflict. Future comparative and developmental work on sexual dimorphism within and among taxa will provide a better understanding of the biases and constraints governing the evolution of animal sexual dimorphism.     

Estimating sexual dimorphism by method-of-moments

Estimating the degree of sexual dimorphism is difficult in fossil species because most specimens lack indicators of sex. We present a procedure that estimates sexual dimorphism in samples of unknown sex using method-of-moments. We assume that the distribution of a metric trait is composed of two underlying normal distributions, one for males and one for females. We use three moments around the mean of the combined-sex distribution to estimate the means and the common standard deviation of the two underlying distributions. This procedure has advantages over previous methods: it is relatively simple to use, specimens need not be assigned to sex a priori, no reference to living species analogs is required, and the method provides conservative estimates of dimorphism under a variety of conditions. The method performs best when the male and female distributions overlap minimally but also works well when overlap is substantial. Simulations indicate that this relatively simple method is more accurate and reliable than previous methods for estimating dimorphism. © 1996 Wiley-Liss, Inc.     

Statistics of sexual size dimorphism

In comparative studies of sexual size dimorphism (SSD), the methods used to quantify dimorphism are controversial. SSD is commonly expressed as a ratio between species mean values of males and females, such as M/F or (M-F)/([M+F]/2), but a number of investigators have suggested that ratios should not be used, mainly because their distributions usually violate the assumptions of parametric statistical tests, or because they lead to spurious relationships that invalidate the interpretation and statistical significance of regressions and correlations. As an alternative to ratios, the comparative study of SSD can be conducted by a combination of regression with sex-specific data and residuals from this regression. Twenty-five data sets were selected from the literature and used to duplicate a variety of statistical procedures commonly employed in studies of SSD. All analyses were repeated with five different ratios and with methods that avoid the calculation of any ratios. These data and a review of the statistical properties of ratios and residuals indicate that: (1) most of the ratios used in the SSD literature are unnecessary, and several commonly used ratios are statistically inferior to others. Only two ratios are needed, one on a logarithmic scale and one on a linear scale; (2) there is no problem with spurious correlation or non-normality when ratios are used in several types of statistical procedures commonly employed in studies of SSD; (3) residuals cannot replace ratios for the evaluation of many questions regarding the pattern of SSD among species; and (4) residuals usually are used incorrectly, leading to misspecified regression equations. Most of the questions for which residuals are used should be addressed by multiple regression. These results apply to studies using comparative methods with or without adjustments for phylogenetic effects.     

Human enhancement and sexual dimorphism

I argue that the existence of sexual dimorphism poses a profound challenge to those philosophers who wish to deny the moral significance of the idea of 'normal human capacities' in debates about the ethics of human enhancement. The biological sex of a child will make a much greater difference to their life prospects than many of the genetic variations that the philosophical and bioethical literature has previously been concerned with. It seems, then, that bioethicists should have something to say about the choice between a male and a female embryo. Either, 1) parents have reason to choose boys over girls; (2) parents have reason to choose girls over boys; or, (3) parents have neither reason to choose girls over boys nor reason to choose boys over girls. Embracing either of the first two alternatives has strongly counterintuitive--and arguably morally repugnant--consequences. To motivate the third option we must either make reference to the idea of 'normal human capacities' or argue that parents should consider the interests of society when thinking about what sort of children they should bring into the world - an implication that should be extremely controversial in debates about the 'new eugenics'. I conclude, then, that the idea of 'normal human capacities' is properly crucial to reasoning about the ethics of shaping future persons.