Role of cell death in the formation of sexual dimorphism in the Drosophila central nervous system

Currently, sex differences in behavior are believed to result from sexually dimorphic neural circuits in the central nervous system (CNS). Drosophila melanogaster is a common model organism for studying the relationship between brain structure, behavior, and genes. Recent studies of sex‐specific reproductive behaviors in D. melanogaster have addressed the contribution of sexual differences in the CNS to the control of sex‐specific behaviors and the development of sexual dimorphism. For example, sexually dimorphic regions of the CNS are involved in the initiation of male courtship behavior, the generation of the courtship song, and the induction of male‐specific muscles in D. melanogaster. In this review, I discuss recent findings about the contribution of cell death to the formation of sexually dimorphic neural circuitry and the regulation of sex‐specific cell death by two sex determination factors, Fruitless and Doublesex, in Drosophila.     

年龄和性别因素对奇台沙蜥食性的影响

采用胃容物分析法研究年龄和性别因素对奇台沙蜥(Phrynocephalus grumgrzimailoi)食性的影响.共解剖220号浸制标本,取出整胃分离胃容物,鉴别胃容物中的食物种类,统计各种食物组分的数量频率、重量比例、出现频率和相对重要性指数(index of relative importance,IRI).结...     

Socioecology and the ontogeny of sexual size dimorphism in anthropoid primates

This study examines statistical correlations between socioecological variables (including measures of group composition, intermale competition, and habitat preference) and the ontogeny of body size sexual dimorphism in anthropoid primates. A regression-based multivariate measure of dimorphism in body weight ontogeny is derived from a sample of 37 species. Quantitative estimates of covariation between socioecological variables and this multivariate measure are evaluated. Statistically significant covariation between the ontogeny of dimorphism and socioecological variables, with the possible exception of habitat preference, is observed. Sex differences in ontogeny are lacking in species that exhibit low levels of intermale competition and are classifiable as species with monogamous/polyandrous mating systems. Among dimorphic species, two modes of dimorphic growth are apparent, which seem to be related to different kinds of group compositions. Multimale/multifemale species tend to become dimorphic through bimaturism (sex differences in duration of growth) with minimal sex differences in growth rate. Single-male/multifemale species tend to attain dimorphism through differences in rate of growth, often with limited bimaturism. Measures of intermale competition may also covary with these modes of dimorphic growth, but the relations among these variables are sometimes ambiguous. Correlations between dimorphic growth and behavioral variables may reflect alternative life history strategies in primates. Specifically, the ways in which risks faced by subadult males are distributed and the relations of these risks to growth rates seem to influence the evolution of size ontogenies. The absence of dimorphic ontogeny in some species can be tied to similar distributions of risk in each sex. In taxa that become dimorphic primarily through rate differences in growth, the lifetime distribution of risks for males may change rapidly. In contrast, males may face a pattern of uniformly changing or stable risk in species that become dimorphic through bimaturism. Finally, much variation recorded by this study remains unexplained, providing additional evidence of the need to specially examine female ontogeny before primate body size dimorphism can be satisfactorily explained. © 1995 Wiley-Liss, Inc.     

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.     

Causes of secondary sexual differences in plants — Evidence from extreme leaf dimorphism in Leucadendron (Proteaceae)

In extreme cases leaves in male plants of the dioecious genus Leucadendron (Proteaceae) are up to an order of magnitude smaller than female leaves. This secondary sexual dimorphism (SSD) in leaf size has previously been suggested to be due to intra-male sexual selection, leading to an increase in male allocation to reproduction in dimorphic species. After critically evaluating previous data provided to support this hypothesis, I suggest on both theoretical grounds and on re-analysis that this argument is unlikely and unsupported. Leaf size dimorphism could theoretically evolve directly due to disruptive ecological selection between genders, leading to niche dimorphism either within or between habitats. I test this ecological causation hypothesis by providing data on specific leaf area (sla) and water use efficiency (δ ¹³C) of leaves from males and females of several Leucadendron species. Results confirm the expectation of minimal gender differences. I argue that leaf dimorphism is a consequence of selection on flower size and architecture.     

Sexual dimorphism inAnastrepha suspensa (Loew) and other tephritid fruit flies (Diptera: Tephritidae): Possible roles of developmental rate,fecundity, and dispersal

Larger male Caribbean fruit flies are more likely to be chosen as mates and defeat rivals in territorial contests. Yet males are smaller than females. Adaptive explanations for relatively small male size include (1) acceleration of male development to maximize female encounter rates, (2) selection for greater female size to increase fecundity, and (3) selection for body sizes most suitable for sexually dimorphic degrees of mobility, speed, and distance flight. None of these unambiguously accounts for the degree of sexual dimorphism. Male development is not accelerated relative to that of females. On average, males remain inside fruit longer than females and those males with extended development periods are smaller than more rapidly developing individuals. There is no evidence that female enlargement alone, presumably for greater fecundity, has generated the degree of dimorphism in the Caribbean fruit fly or other fruit flies. The relationship between dimorphism and mean female body size in 27 species of Tephritidae is the opposite of what would be predicted if differences in dimorphism were due to differences in unilateral female enlargement. Larger size in a species or in one sex of a species may be an adaptation for extensive flight. In general, among 32 species of fruit flies, as body size increases, wing shape becomes progressively more suited for distance flight. However, there are important exceptions to this correlation. Both sexual selection and nonadaptive allometries may contribute to the range of dimorphisms within the family.     

Sexual growth dimorphism affects birth sex ratio in house mice

We present the first empirical evidence that mammalian sex-ratio deviations result from variation in adult-weight sexual dimorphism via correlated effects on blastocyst development. Two selection lines of mice exhibiting high and low sexual dimorphism in adult weight showed correlated sexual weight differences at birth and at weaning, caused by relatively decelerated growth of males in the low line from before birth. The sex ratio at birth was significantly female-biased in the low line, and significantly lower than in the highly dimorphic line. Concomitantly, blastomere numbers were at significantly higher variance in the low than in the highly dimorphic line, owing to an increased frequency of slowly growing blastocysts. Since low-dimorphism mice produced more corpora lutea and more female pups than the high-dimorphism mice, but not more males, birth sex-ratio bias most parsimoniously resulted from the loss of slowly growing male blastocysts. This is in agreement with the observation that sex-ratio skews in mammals arise when timing of uterine responsiveness (i.e. its temporally limited capacity for implantation) varies in relation to sex-specific embryonic growth rates. Hence, natural mammalian sex-ratio variation that stems from developmental asynchrony might be a by-product of natural selection for sexual dimorphism in adult weight.     

Anthropometric analysis of homosexuals and heterosexuals: implications for early hormone exposure

Early exposure to sex steroids is thought to be important in mediating the differentiation of male-typical sexual orientation. Bone morphology is a marker of childhood sex steroid exposure, because estrogens and androgens control sexual dimorphism in skeletal size. Anthropometric analysis of heterosexuals and homosexuals indicates that those bones, which become sexually dimorphic in childhood, but not those which become sexually dimorphic after puberty, are different in length in homosexuals and heterosexuals. Persons with a sexual preference for males have less long bone growth in the arms, legs and hands, than those with sexual preference for females. The data support the hypothesis that male homosexuals have had less steroid exposure during development than male heterosexuals and that female homosexuals have had greater steroid exposure during development than their heterosexual counterparts.     

A Genome-Wide Survey of Sexually Dimorphic Expression of Drosophila miRNAs Identifies the Steroid Hormone-Induced miRNA let-7 as a Regulator of Sexual Identity

MiRNAs bear an increasing number of functions throughout development and in the aging adult. Here we address their role in establishing sexually dimorphic traits and sexual identity in male and female Drosophila. Our survey of miRNA populations in each sex identifies sets of miRNAs differentially expressed in male and female tissues across various stages of development. The pervasive sex-biased expression of miRNAs generally increases with the complexity and sexual dimorphism of tissues, gonads revealing the most striking biases. We find that the male-specific regulation of the X chromosome is relevant to miRNA expression on two levels. First, in the male gonad, testis-biased miRNAs tend to reside on the X chromosome. Second, in the soma, X-linked miRNAs do not systematically rely on dosage compensation. We set out to address the importance of a sex-biased expression of miRNAs in establishing sexually dimorphic traits. Our study of the conserved let-7-C miRNA cluster controlled by the sex-biased hormone ecdysone places let-7 as a primary modulator of the sex-determination hierarchy. Flies with modified let-7 levels present doublesex-related phenotypes and express sex-determination genes normally restricted to the opposite sex. In testes and ovaries, alterations of the ecdysone-induced let-7 result in aberrant gonadal somatic cell behavior and non-cell-autonomous defects in early germline differentiation. Gonadal defects as well as aberrant expression of sex-determination genes persist in aging adults under hormonal control. Together, our findings place ecdysone and let-7 as modulators of a somatic systemic signal that helps establish and sustain sexual identity in males and females and differentiation in gonads. This work establishes the foundation for a role of miRNAs in sexual dimorphism and demonstrates that similar to vertebrate hormonal control of cellular sexual identity exists in Drosophila.     

Sex and Weapons: Contrasting Sexual Dimorphisms in Weaponry and Aggression in Snapping Shrimp

Sexual dimorphisms in weaponry and aggression are common in species in which one sex (usually males) competes for access to mates or resources necessary for reproduction – sexually dimorphic weaponry and aggression, in other words, are frequently the result of intrasexual selection. In snapping shrimp, the major chela (snapping claw) can be a deadly weapon, and males of many species have larger chelae than females, a pattern readily interpreted as resulting from intrasexual selection. Thus, males might be expected to show more sex‐specific aggression than females, and be more aggressive overall. We tested these predictions in two species of snapping shrimp in a territorial defense context. Neither of these predictions was supported: in both species, females, but not males, engaged in sex‐specific aggression and females were more aggressive than males overall. These contrasting sexual dimorphisms – larger weaponry in males but higher aggression in females – highlight the importance of considering the function of weaponry and aggression in contexts other than direct competitions over mates. In addition, species differences in the degree of sexual dimorphism in chela size were due to differences in female, not male, chela size, and the species with greater sexual dimorphism in weaponry was significantly less aggressive overall; also, while paired and solitary males did not differ in residual chela size, for the species with greater sexual dimorphism, females carrying embryos had smaller residual chela sizes. These results suggest that understanding the sexual dimorphisms in weaponry and aggression in snapping shrimp requires understanding the relative costs and benefits of both in females as well as males.     

Ontogeny and the evolution of adult body size dimorphism in apes

This analysis investigates the ontogeny of body size dimorphism in apes. The processes that lead to adult body size dimorphism are illustrated and described. Potential covariation between ontogenetic processes and socioecological variables is evaluated. Mixed-longitudinal growth data from 395 captive individuals (representing Hylobates lar [gibbon], Hylobates syndactylus [siamang], Pongo pygmaeus [orangutan], Gorilla gorilla [gorilla], Pan paniscus [pygmy chimpanzee], and Pan troglodytes [“common” chimpanzee]) form the basis of this study. Results illustrate heterogeneity in the growth processes that produce ape dimorphism. Hylobatids show no sexual differentiation in body weight growth. Adult body size dimorphism in Pongo can be largely attributed to indeterminate male growth. Dimorphism in African apes is produced by two different ontogenetic processes. Both pygmy chimpanzees (Pan paniscus) and gorillas (Gorilla gorilla) become dimorphic primarily through bimaturism (sex differences in duration of growth). In contrast, sex differences in rate of growth account for the majority of dimorphism in common chimpanzees (Pan troglodytes). Diversity in the ontogenetic pathways that produce adult body size dimorphism may be related to multiple evolutionary causes of dimorphism. The lack of sex differences in hylobatid growth is consistent with a monogamous social organization. Adult dimorphism in Pongo can be attributed to sexual selection for indeterminate male growth. Interpretation of dimorphism in African apes is complicated because factors that influence female ontogeny have a substantial effect on the resultant adult dimorphism. Sexual selection for prolonged male growth in gorillas may also increase bimaturism relative to common chimpanzees. Variation in female growth is hypothesized to covary with foraging adaptations and with differences in female competition that result from these foraging adaptations. Variation in male growth probably corresponds to variation in level of sexual selection. © 1995 Wiley-Liss, Inc.     

Evolution of sexual size dimorphism in birds: test of hypotheses using blue tits in contrasted Mediterranean habitats

Many hypotheses, either sex‐related or environment‐related, have been proposed to explain sexual size dimorphism in birds. Two populations of blue tits provide an interesting case study for testing these hypotheses because they live in contrasting environments in continental France and in Corsica and exhibit different degree of sexual size dimorphism. Contrary to several predictions, the insular population is less dimorphic than the continental one but neither the sexual selection hypothesis nor the niche variation hypothesis explain the observed patterns. In the mainland population it is advantageous for both sexes to be large, and males are larger than females. In Corsica, however, reproductive success was greater for pairs in which the male was relatively small, i.e. pairs in which sexual size dimorphism is reduced. The most likely explanation is that interpopulation differences in sexual size dimorphism are determined not by sex‐related factors, but by differences in sex‐specific reproductive roles and responses to environmental factors. Because of environmental stress on the island as a result of food shortage and high parasite infestations, the share of parents in caring for young favours small size in males so that a reduced sexual size dimorphism is not the target of selection but a by‐product of mechanisms that operate at the level of individual sexes.     

Insights into the genetic architecture of sexual dimorphism from an interspecific cross between two diverging Silene (Caryophyllaceae) species

The evolution of sexual dimorphism in species with separate sexes is influenced by the resolution of sexual conflicts creating sex differences through genetic linkage or sex‐biased expression. Plants with different degrees of sexual dimorphism are thus ideal to study the genetic basis of sexual dimorphism. In this study we explore the genetic architecture of sexual dimorphism between Silene latifolia and Silene dioica. These species have chromosomal sex determination and differ in the extent of sexual dimorphism. To test whether QTL for sexually dimorphic traits have accumulated on the sex chromosomes and to quantify their contribution to species differences, we create a linkage map and performed QTL analysis of life history, flower and vegetative traits using an unidirectional interspecific F2 hybrid cross. We found support for an accumulation of QTL on the sex chromosomes and that sex differences explained a large proportion of the variance between species, suggesting that both natural and sexual selection contributed to species divergence. Sexually dimorphic traits that also differed between species displayed transgressive segregation. We observed a reversal in sexual dimorphism in the F2 population, where males tended to be larger than females, indicating that sexual dimorphism is constrained within populations but not in recombinant hybrids. This study contributes to the understanding of the genetic basis of sexual dimorphism and its evolution in Silene.     

Wind pollination, sexual dimorphism, and changes in floral traits of Schiedea (Caryophyllaceae)

Both changes in sex allocation and pollination mode may promote the separation of sexes in plant populations. Simultaneous evolution of wind pollination and dimorphism has occurred in Schiedea, where species with different female frequencies provide an opportunity to observe the effect of wind pollination on sex allocation and floral morphology. Differences among species in the ratio of anther to ovary volume were not the result of sex allocation trade-offs, but instead resulted from production of vestigial stamens in females; there were no changes in ovary volume in males and hermaphrodites (MH) of dimorphic species. Relative to hermaphroditic species, dimorphic species had more condensed inflorescences, a pattern often associated with wind pollination. Within dimorphic species, MH had longer filament lengths than females, and females had longer stigmas than MHs. These traits are characteristic of wind pollination, but there was no relationship between the degree of sexual dimorphism and female frequency. Ovary volume and ovule number and size had positive phenotypic correlations between females and MH of dimorphic species, making sex specialization more difficult. In dimorphic Schiedea species, selection for wind pollination may have a greater effect on floral traits than trade-offs in allocation between male and female function.     

Active pollination favours sexual dimorphism in floral scent

Zoophilous flowers often transmit olfactory signals to attract pollinators. In plants with unisexual flowers, such signals are usually similar between the sexes because attraction of the same animal to both male and female flowers is essential for conspecific pollen transfer. Here, we present a remarkable example of sexual dimorphism in floral signal observed in reproductively highly specialized clades of the tribe Phyllantheae (Phyllanthaceae). These plants are pollinated by species-specific, seed-parasitic Epicephala moths (Gracillariidae) that actively collect pollen from male flowers and pollinate the female flowers in which they oviposit; by doing so, they ensure seeds for their offspring. We found that Epicephala-pollinated Phyllanthaceae plants consistently exhibit major qualitative differences in scent between male and female flowers, often involving compounds derived from different biosynthetic pathways. In a choice test, mated female Epicephala moths preferred the scent of male flowers over that of female flowers, suggesting that male floral scent elicits pollen-collecting behaviour. Epicephala pollination evolved multiple times in Phyllantheae, at least thrice accompanied by transition from sexual monomorphism to dimorphism in floral scent. This is the first example in which sexually dimorphic floral scent has evolved to signal an alternative reward provided by each sex, provoking the pollinator''s legitimate altruistic behaviour.     

Androgen receptors are required for full masculinization of the ventromedial hypothalamus (VMH) in rats

The ventromedial hypothalamus (VMH) is one of several sexually dimorphic nuclei that regulate mating behavior, and is rich in steroid hormone receptors and aromatase activity. We looked at the contribution of the androgen receptor (AR) to the volume of the VMH in rats by measuring each of the four subdivisions of the VMH in 90 day old male, female, and XY male rats carrying a mutant AR allele (tfm), which renders animals largely unresponsive to androgens. Confirming published reports, total VMH volume was greater in wild-type males than in females (P<0.01). The mean total volume of the VMH in TFM males was intermediate, but not significantly different from either females or males (Ps>0.10). The sex difference in VMH volume was primarily accounted for by the ventrolateral subdivision (VMHvl), which in both females and TFM males was significantly smaller than in wild-type males (Ps<0.005). There was no significant sex difference in the volume of the other three subdivisions of the VMH. Neuronal somata were larger in males than females in VMHvl, central VMH (VMHc) and the dorsomedial VMH (VMHdm), with TFM males having feminine neuronal somata in the VMHdm and VMHc. These data suggest that AR plays a role during sexual differentiation of the VMH, imparting its greatest effect in the VMHvl. ARs may regulate aromatase expression or activity to affect estrogen receptor activation, or may act independently of estrogen receptors to influence VMH morphology.     

Immune function during early adolescence positively predicts adult facial sexual dimorphism in both men and women

Evolutionary theories suggest that humans prefer sexual dimorphism in faces because masculinity in men and femininity in women may be an indicator of immune function during development. In particular, the immunocompetence handicap hypothesis proposes that sexual dimorphism indicates good immune function during development because the sex hormones, particularly testosterone in men, required for the development of sexually dimorphic facial features also taxes the immune system. Therefore, only healthy males can afford the high level of testosterone for the development of sexually dimorphic traits without compromising their survival. Researchers have suggested that a similar mechanism via the effects of oestrogen might also explain male preferences for female femininity. Despite the prominence of the immunocompetence handicap hypothesis, no studies have tested whether immune function during development predicts adult facial sexual dimorphism. Here, using data from a longitudinal public health dataset, the Western Australian Pregnancy Cohort (Raine) Study (Generation 2), we show that some aspects of immune function during early adolescence (14 years) positively predict sexually dimorphic 3D face shape in both men and women. Our results support a fundamental assumption that facial sexual dimorphism is an indicator of immune function during the development of facial sexual dimorphism.     

Sexual dimorphism, extrapair fertilizations, and operational sex ratio in great frigatebirds (Fregata minor)

Across taxa, the presence of sexual ornaments in one sex isusually correlated with disproportionately great parental effortby the other. Frigatebirds (Fregatidae) are sexually dimorphic,with males exhibiting morphological and behavioral ornaments,but males and females share in all aspects of parental effort.All other taxa in a clade of 237 species exhibit biparentalcare, but only frigatebirds exhibit pronounced sexual dimorphism. We tested for the presence of two factors that could contributeto the evolution of male ornaments in great frigatebirds: ahigh frequency of extrapair fertilizations and a male-biasedoperational sex ratio. In 92 families sampled over two breedingseasons, there was only one extrapair fertilization. However,in both seasons, there were more males than females availablefor mating, and the sex ratio among individuals actively engagedin mate-acquisition behavior was strongly male biased, withtypically five or six males available per female. Our resultssuggest that extrapair fertilizations are not responsible forthe exaggeration of sexual ornaments in male frigatebirds,and that operational sex ratio may be related to sexual dimorphismin this species. Further work is needed to determine whetherthe male-biased operational sex ratio creates the variancein male reproductive success that would be needed to drivethe evolution of male ornaments.     

It takes two: Seasonal variation in sexually dimorphic weaponry results from divergent changes in males and females

Sexually dimorphic weaponry often results from intrasexual selection, and weapon size can vary seasonally when costs of bearing the weapon exceed the benefits outside of the reproductive season. Weapons can also be favored in competition over nonreproductive resources such as food or shelter, and if such nonreproductive competition occurs year‐round, weapons may be less likely to vary seasonally. In snapping shrimp (Alpheus angulosus), both sexes have an enlarged snapping claw (a potentially deadly weapon), and males of many species have larger claws than females, although females are more aggressive. This contrasting sexual dimorphism (larger weaponry in males, higher aggression in females) raises the question of whether weaponry and aggression are favored by the same mechanisms in males and females. We used field data to determine whether either sex shows seasonal variation in claw size such as described above. We found sexual dimorphism increased during the reproductive season due to opposing changes in both male and female claw size. Males had larger claws during the reproductive season than during the nonreproductive season, a pattern consistent with sexual selection. Females, however, had larger claws during the nonreproductive season than during the reproductive season—a previously unknown pattern of variation in weapon size. The observed changes in female weapon size suggest a trade‐off between claw growth and reproduction in the reproductive season, with investment in claw growth primarily in the nonreproductive season. Sexually dimorphic weaponry in snapping shrimp, then, varies seasonally due to sex differences in seasonal patterns of investment in claw growth, suggesting claws may be advantageous for both sexes but in different contexts. Thus, understanding sexual dimorphisms through the lens of one sex yields an incomplete understanding of the factors favoring their evolution.