Macroevolutionary patterns of sexual size dimorphism in copepods

Major theories compete to explain the macroevolutionary trends observed in sexual size dimorphism (SSD) in animals. Quantitative genetic theory suggests that the sex under historically stronger directional selection will exhibit greater interspecific variance in size, with covariation between allometric slopes (male to female size) and the strength of SSD across clades. Rensch''s rule (RR) also suggests a correlation, but one in which males are always the more size variant sex. Examining free-living pelagic and parasitic Copepoda, we test these competing predictions. Females are commonly the larger sex in copepod species. Comparing clades that vary by four orders of magnitude in their degree of dimorphism, we show that isometry is widespread. As such we find no support for either RR or for covariation between allometry and SSD. Our results suggest that selection on both sexes has been equally important. We next test the prediction that variation in the degree of SSD is related to the adult sex ratio. As males become relatively less abundant, it has been hypothesized that this will lead to a reduction in both inter-male competition and male size. However, the lack of such a correlation across diverse free-living pelagic families of copepods provides no support for this hypothesis. By comparison, in sea lice of the family Caligidae, there is some qualitative support of the hypothesis, males may suffer elevated mortality when they leave the host and rove for sedentary females, and their female-biased SSD is greater than in many free-living families. However, other parasitic copepods which do not appear to have obvious differences in sex-based mate searching risks also show similar or even more extreme SSD, therefore suggesting other factors can drive the observed extremes.     

Long-term paternity skew and the opportunity for selection in a mammal with reversed sexual size dimorphism

Most mammalian groups are characterized by male-biased sexual size dimorphism, in which size-dependent male-male competition and reproductive skew are tightly linked. By comparison, little is known about the opportunity for sexual selection in mammalian systems without male-biased dimorphism, where the traits under sexual selection might be less obvious. We examined 10 years of parentage data in a colony of greater horseshoe bats (Rhinolophus ferrumequinum) to determine the magnitude of male reproductive skew and the opportunity for sexual selection in a mammal in which females are the larger sex. Annual paternity success was weakly skewed but consistent patterns led to strong longitudinal paternity skew among breeders. Just three males accounted for a third of all paternity assignments, representing at least a fifth of all colony offspring born in a decade. Paternity success was in part determined by age but was not influenced by dispersal status. Our results show that paternity skew and the opportunity for sexual selection in a species with reversed sexual size dimorphism can approach levels reported for classical examples of species with polygyny and male-biased dimorphism, even where the traits under sexual selection are not known.     

Adult sex ratio,sexual dimorphism and sexual selection in a Mesozoic reptile

The evolutionary history of sexual selection in the geologic past is poorly documented based on quantification, largely because of difficulty in sexing fossil specimens. Even such essential ecological parameters as adult sex ratio (ASR) and sexual size dimorphism (SSD) are rarely quantified, despite their implications for sexual selection. To enable their estimation, we propose a method for unbiased sex identification based on sexual shape dimorphism, using size-independent principal components of phenotypic data. We applied the method to test sexual selection in Keichousaurus hui, a Middle Triassic (about 237 Ma) sauropterygian with an unusually large sample size for a fossil reptile. Keichousaurus hui exhibited SSD biased towards males, as in the majority of extant reptiles, to a minor degree (sexual dimorphism index −0.087). The ASR is about 60% females, suggesting higher mortality of males over females. Both values support sexual selection of males in this species. The method may be applied to other fossil species. We also used the Gompertz allometric equation to study the sexual shape dimorphism of K. hui and found that two sexes had largely homogeneous phenotypes at birth except in the humeral width, contrary to previous suggestions derived from the standard allometric equation.     

Operational sex ratio, sexual conflict and the intensity of sexual selection

Modern sexual selection theory indicates that reproductive costs rather than the operational sex ratio predict the intensity of sexual selection. We investigated sexual selection in the polygynandrous common lizard Lacerta vivipara . This species shows male aggression, causing high mating costs for females when adult sex ratios (ASR) are male-biased. We manipulated ASR in 12 experimental populations and quantified the intensity of sexual selection based on the relationship between reproductive success and body size. In sharp contrast to classical sexual selection theory predictions, positive directional sexual selection on male size was stronger and positive directional selection on female size weaker in female-biased populations than in male-biased populations. Thus, consistent with modern theory, directional sexual selection on male size was weaker in populations with higher female mating costs. This suggests that the costs of breeding, but not the operational sex ratio, correctly predicted the strength of sexual selection.     

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.     

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.     

Paternity success and the direction of sexual selection in a field population of a semelparous marsupial,Antechinus agilis

Antechinus agilis is a small sexually size dimorphic marsupial with a brief annual mating period of 2-3 weeks. All males die after this period, and females give birth to up to 10 young. Mating is thought to be promiscuous, however, there is no field data to confirm this. Using microsatellites, we investigated paternity patterns over two seasons in a wild population. Male weight was significantly positively related to the number of females fertilized and with the number of offspring sired, in both years. Furthermore, selection gradients indicated selection for larger males. Both results suggest that size dimorphism in A. agilis can be explained by sexual selection for larger males. The proportion of offspring sired within litters, did not relate to male size. Therefore, larger males are more successful through higher mating access, not through their sperm outcompeting that of smaller males. As expected from their known ranging behaviour, the number of offspring within litters left unassigned to a father did not depend on the grid location of the mother. Female size did not differ between successful reproducing and unsuccessful females. However, females that weaned offspring had larger heads than females that did not wean offspring. Males did not 'prefer' mating with larger females, nor did assortative mating occur. From our results, the mating system of A. agilis is clearly promiscuous. Selection for larger males occurred in both years, even though in one year the operational sex ratio was highly female biased, suggesting that the potential reproductive rate is a better predictor of the direction of sexual selection in A. agilis.     

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.     

Sexual dimorphism in human skulls. A comparison of sexual dimorphism in different populations

Application and comparison of sex discriminant functions in different populations led to the conclusion that a certain combination and weighting of a few sex dimorphism variables (in this study we only used craniometric variables) can give a good discrimination between male and female individuals, independent of the racial group to which this function is applied. In our study, the sex-discriminatory power of five discriminant functions which were based on different ordination and selection procedures (e.g. professional knowledge, stepwise discriminant analysis, literature) of the cranial variables is compared. These discriminant functions were applied to three different data sets, the first being skull measurements from an Amsterdam series (Europids), the second skull measurements of a Zulu series (Negrids) and the third skull measurements of a Japan series (Mongolids). Our decision as to whether a function is a good or less good sex-discriminating function is determined by the Dt values (these values give an idea about the discriminatory value of the discriminant function when applied to a new test sample), the number of variables necessary to obtain this Dt and the location of the sectioning point (i.e. comparison between the estimation of the sectioning point and the ”real” sectioning point). These discriminant functions were compared withGiles Elliot's (1962, 1963) “race-independent” sex function.     

Female-biased sexual size dimorphism in the yellow-pine chipmunk (Tamias amoenus): sex-specific patterns of annual reproductive success and survival

Sexual size dimorphism is ultimately the result of independent, sex-specific selection on body size. In mammals, male-biased sexual size dimorphism is the predominant pattern, and it is usually attributed to the polygynous mating system prevalent in most mammals. This sole explanation is unsatisfying because selection acts on both sexes simultaneously, therefore any explanation of sexual size dimorphism should explain why one sex is relatively large and the other is small. Using mark-recapture techniques and DNA microsatellite loci to assign parentage, we examined sex-specific patterns of annual reproductive success and survival in the yellow-pine chipmunk (Tamias amoenus), a small mammal with female-biased sexual size dimorphism, to test the hypothesis that the dimorphism was related to sex differences in the relationship between body size and fitness. Chipmunks were monitored and body size components measured over three years in the Kananaskis Valley, Alberta, Canada. Male reproductive success was independent of body size perhaps due to trade-offs in body size associated with behavioral components of male mating success: dominance and running speed. Male survival was consistent with stabilizing selection for overall body size and body size components. The relationship between reproductive success and female body size fluctuated. In two of three years the relationship was positive, whereas in one year the relationship was negative. This may have been the result of differences in environmental conditions among years. Large females require more energy to maintain their soma than small females and may be unable to maintain lactation in the face of challenging environmental conditions. Female survival was positively related to body size, with little evidence for stabilizing selection. Sex differences in the relationship between body size and fitness (reproductive success and survival) were the result of different processes, but were ultimately consistent with female-biased sexual size dimorphism evident in this species.     

Sexual size dimorphism and sexual selection in primates

1. In most animals, females are larger than males. Paradoxically, sexual size dimorphism is biased towards males in most mammalian species. An accepted explanation is that sexual dimorphism in mammals evolved by intramale sexual selection. I tested this hypothesis in primates, by relating sexual size dimorphism to seven proxies of sexual selection intensity: operational sex ratio, mating system, intermale competition, group sex ratio, group size, maximum mating percentage (percentage of observed copulations involving the most successful male), and total paternity (a genetic estimate of the percentage of young sired by the most successful male).
2. I fitted phylogenetic generalised least squares models using sexual size dimorphism as the dependent variable and each of the seven measures of intensity of sexual selection as independent variables. I conducted this comparative analysis with data from 50 extant species of primates, including Homo sapiens, Pan troglodytes, and Gorilla spp.
3. Sexual dimorphism was positively related to the four measures of female monopolisation (operational sex ratio, mating system, intermale competition, and group sex ratio) and in some cases to group size, but was not associated with maximum mating percentage or total paternity. Additional regression analyses indicated that maximum mating percentage and total paternity were negatively associated with group size.
4. These results are predicted by reproductive skew theory: in large groups, males can lose control of the sexual behaviour of the other members of the group or can concede reproductive opportunities to others. The results are also consistent with the evolution of sexual size dimorphism before polygyny, due to the effects of natural, rather than sexual, selection. In birds, the study of molecular paternity showed that variance in male reproductive success is much higher than expected by behaviour. In mammals, recent studies have begun to show the opposite trend, i.e. that intensity of sexual selection is lower than expected by polygyny.
5. Results of this comparative analysis of sexual size dimorphism and sexual selection intensity in primates suggest that the use of intramale sexual selection theory to explain the evolution of polygyny and sexual dimorphism in mammals should be reviewed, and that natural selection should be considered alongside sexual selection as an evolutionary driver of sexual size dimorphism and polygyny in mammals.

     

Male‐biased hermaphrodites in a gynodioecious shrub,Daphne jezoensis

Gynodioecy, a state where female and hermaphrodite plants coexist in populations, has been widely proposed an intermediate stage in the evolutionary pathway from hermaphroditism to dioecy. In the gynodioecy–dioecy pathway, hermaphrodites may gain most of their fitness through male function once females invade populations. To test this prediction, comprehensive studies on sex ratio variation across populations and reproductive characteristics of hermaphrodite and female phenotypes are necessary. This study examined the variation in sex ratio, sex expression, flower and fruit production and sexual dimorphism of morphological traits in a gynodioecious shrub, Daphne jezoensis, over multiple populations and years. Population sex ratio (hermaphrodite:female) was close to 1:1 or slightly hermaphrodite‐biased. Sex type of individual plants was largely fixed, but 15% of plants changed their sex during a 6‐year census. Hermaphrodite plants produced larger flowers and invested 2.5 times more resources in flower production than female plants, but they exhibited remarkably low fruit set (proportion of flowers setting fruits). Female plants produced six times more fruits than hermaphrodite plants. Low fruiting ability of hermaphrodite plants was retained even when hand‐pollination was performed. Fruit production of female plants was restricted by pollen limitation under natural conditions, irrespective of high potential fecundity, and this minimised the difference in resources allocated to reproduction between the sexes. Negative effects of previous flower and fruit production on current reproduction were not apparent in both sexes. This study suggests that gynodioecy in this species is functionally close to a dioecious mating system: smaller flower production with larger fruiting ability in female plants, and larger flower production with little fruiting ability in hermaphrodite plants.     

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

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

Craniofacial sexual dimorphism in a Northern-Greek pre-pubertal population

Craniofacial sexual dimorphism on size and shape in a prepubertal (6–12 years of age) population of northern Greece has been studied by means of both univariate and multivariate analysis. The structure of population was limiting the influence of environmental and genetic factors. Even though there have been observed statistical significant differences between the sexes in most of the variables it has not been concluded any sexual dimorphism in the morphology of the craniofacial area.     

Polyploidization and sexual dimorphism of floral traits in a subdioecious population of Dasiphora glabra

银露梅亚雌雄异株种群的多倍化和花特征性二态 性二态是性别分离植物的常见性状,对植物的雌性和雄性功能可能产生不同的影响。本文以青藏高原特有植物银露梅(Dasiphora glabra)为研究对象,利用银露梅同时存在两性、雌性和雄性植株的种群,探讨银露梅与传粉相关的花特征性二态现象及其对传粉者访问、花粉流和结实的影响。另外,本文还利用流式细胞仪检查了两性植株、雄性植株和雌性植株之间基因组大小的差异。研究结果表明：银露梅雌性植株和雄性植株数量约占种群中植株总数量的40%,表明银露梅两性植株数量多于雄性和雌性的植株数量。两性植株的花数量显著多于雄性和雌性植株的花数量。雄花的花大小显著大于雌花和两性花的花大小。雄花的花粉数量与两性花的花粉数量没有差异,但是雌花的胚珠数量显著高于两性花的胚珠数量。双翅目的蝇类是银露梅最主要的访花者,尽管访花者偏好访问更大的花,但是在花间连续访问对大花没有表现出偏好。模拟花粉流实验表明,两性植株和雄性植株的有效花粉转移都很低,从而导致较低的结实率。雌性植株和雄性植株的DNA含量约为两性植株的4倍,并且单性植株和两性植株之间相互授粉不能结实。以上结果表明,与两性花相比,雌花和雄花在与传粉相关的花特征二态性上分别在雌性和雄性功能上表现出优势,但这种优势在很大程度上被低效的花粉转移所掩盖。银露梅的雌性植株和雄性植株经历了多倍化事件,导致与两性植株之间存在繁殖隔离,从而维持了3种性别植株的共存。     

Proximate causes of sexual size dimorphism in Colorado pikeminnow, a long‐lived cyprinid

Evidence for sexual size dimorphism (SSD) and its possible causes were examined in the endangered Colorado pikeminnow Ptychocheilus lucius, a large, piscivorous, cyprinid endemic to the Colorado River system of North America. Individuals representing 18–24% of the upper Colorado River population were captured, measured, sexed and released in 1999 and 2000. Differing male and female total length‐(L_T) frequency distributions revealed SSD with females having greater mean and maximum sizes than males. Although both sexes exhibit indeterminate post‐maturity growth, growth trajectories differed. The point of trajectory divergence was not established, but slowed male growth might coincide with the onset of maturation. Differing growth rate was the dominant proximate cause of SSD, accounting for an estimated 61% of the observed difference in mean adult L_T. The degree of SSD in adults, however, was also related to two other factors. Evidence suggests males become sexually active at a smaller size and earlier age than females; a 2 year difference, suggested here, accounted for an estimated 12% of the between‐sex difference in mean adult L_T. Temporal shifts in gender‐specific survival accounted for an additional 27% of the observed between‐sex difference in mean adult L_T. Estimated age distributions indicated a higher number of older females than older males and more younger males than younger females in the population during the period of sampling. Dissimilarity of age distributions was an unexpected result because the male : female population sex ratio was 1 : 1 and estimates of long‐term annual survival for adult males and females were equal (88%). Future assessments of SSD in this population are apt to vary depending on the prior history of short‐term gender‐specific survival. Without recognizing SSD, non‐gender‐specific growth curves overestimate mean age of adult females and underestimate mean age of adult males of given L_T. Assuming age 8 years for first reproduction in males and age 10 years for females, the adult male : female ratio was estimated as 1·1 : 1 and mean adult age, or generation time, was estimated as 16·4 years for males and 18·4 years for females.     

A statistical analysis of the literature on sexual dimorphism in primates

The annotated bibliography on sexual dimorphism in primates compiled by the authors was analysed considering the distribution of entries by keytitles, keywords, kind of periodicals and years of publication. A growing interest in this field was observed especially since the 1970s, but a relative scarcity of basic methodological papers was found. Articles on extant human populations and on living nonhuman primates are much more frequent than works on fossil primates and ancient humans.