A comparative study on the evolution of reversed size dimorphism in monogamous waders

Sexual dimorphism in size is common in birds. Males are usually larger than females, although in some taxa reversed size dimorphism (RSD) predominates. Whilst direct dimorphism is attributed to sexual selection in males giving greater reproductive access to females, the evolutionary causes of RSD are still unclear. Four different hypotheses could explain the evolution of RSD in monogamous birds: (1) The ‘energy storing’ hypothesis suggests that larger females could accumulate more reserves at wintering or refuelling areas to enable an earlier start to egg laying. (2) According to the ‘incubation ability’ hypothesis, RSD has evolved because large females can incubate more efficiently than small ones. (3) The ‘parental role division’ hypothesis suggests that RSD in monogamous waders has evolved in species with parental role division and uniparental male care of the chicks. It is based on the assumption that small male size facilitates food acquisition in terrestrial habitats where chick rearing takes place and that larger females can accumulate more reserves for egg laying in coastal sites. (3) The ‘display agility’ hypothesis suggests that small males perform better in acrobatic displays presumably involved in mate choice and so RSD may have evolved due to female preference for agile males. I tested these hypotheses in monogamous waders using several comparative methods. Given the current knowledge of the phylogeny of this group, the evolutionary history of waders seems only compatible with the hypothesis that RSD has evolved as an adaptation for increasing display performance in males. In addition, the analysis of wing shape showed that males of species with acrobatic flight displays had wings with higher aspect ratio (wing span/²wing area) than non-acrobatic species, which probably increases flight manoeuvrability during acrobatic displays. In species with acrobatic displays males also had a higher aspect ratio than females although no sexual difference was found in non-acrobatic species. These results suggest that acrobatic flight displays could have produced changes in the morphology of some species and suggest the existence of selection favouring higher manoeuvrability in species with acrobatic flight displays. This supports the validity of the mechanisms proposed by the ‘display agility’ hypothesis to explain the evolution of RSD in waders.     

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.     

Sexual selection,sexual dimorphism and plant phylogeny

Summary Darwin examined sexual dimorphism in animals, arguing that sexual selection was important in the evolution of such dimorphism. Sexual dimorphism in plants may have parallel causes and costs.The processes that contribute to sexual dimorphism may also lead to speciation and morphological differences among related species, as argued originally by Darwin. Where sexes are separate and dimorphism is well-developed, males of related animal species (both vertebrate and invertebrate) are often strikingly different from each other, while females may be virtually indistinguishable. A similar pattern may exist in plants: it is frequently the males (of dioecious taxa) or the male portions of the flower (in co-sexual flowers) that apparently have diversified. I suggest that the similarity of pattern may be accounted for by a similarity of process.In addition, sexual selection may have contributed to certain evolutionary trends within the angiosperms and, indeed, to angiosperm radiation.     

Myodocopa (Crustacea: Ostracoda) as models for evolutionary studies of light and vision: multiple origins of bioluminescence and extreme sexual dimorphism

Evolutionists often use phylogeny to examine independent evolutionary events in search of generality. Therefore, groups of organisms rich in such independent character transitions are particularly valuable for the study of evolution. With respect to eyes, vision, and light-related characters, one such group is Ostracoda (Crustacea). Phylogenies of ostracods, derived from DNA sequence data and morphological characters, are presented. These inferred relationships largely agree with previous assessments of ostracod phylogeny, with the exception of paraphyletic Philomedidae. Based on methods of character reconstruction using these inferred relationships, different groups of ostracods probably evolved both bioluminescence and extreme sexual dimorphism (females lack eyes, males have large eyes) multiple times. Furthermore, myodocopid ostracods may have evolved compound eyes independently of other arthropods. For these and other reasons, it is proposed that the Ostracoda are an exceptionally important group for studying the evolution of vision- and light-related characters.     

A biogeographic reversal in sexual size dimorphism along a continental temperature gradient

The magnitude and direction of sexual size dimorphism (SSD) varies greatly across the animal kingdom, reflecting differential selection pressures on the reproductive and/or ecological roles of males and females. If the selection pressures and constraints imposed on body size change along environmental gradients, then SSD will vary geographically in a predictable way. Here, we uncover a biogeographical reversal in SSD of lizards from Central and North America: in warm, low latitude environments, males are larger than females, but at colder, high latitudes, females are larger than males. Comparisons to expectations under a Brownian motion model of SSD evolution indicate that this pattern reflects differences in the evolutionary rates and/or trajectories of sex‐specific body sizes. The SSD gradient we found is strongly related to mean annual temperature, but is independent of species richness and body size differences among species within grid cells, suggesting that the biogeography of SSD reflects gradients in sexual and/or fecundity selection, rather than intersexual niche divergence to minimize intraspecific competition. We demonstrate that the SSD gradient is driven by stronger variation in male size than in female size and is independent of clutch mass. This suggests that gradients in sexual selection and male–male competition, rather than fecundity selection to maximize reproductive output by females in seasonal environments, are predominantly responsible for the gradient.     

Predicting the evolution of sexual size dimorphism

11 , Evolution 34 : 292–305) equations for predicting the evolution of sexual size dimorphism (SSD) through frequency‐dependent sexual selection, and frequency‐independent natural selection, were tested against results obtained from a stochastic genetic simulation model. The SSD evolved faster than predicted, due to temporary increases in the genetic variance brought about by directional selection. Predictions for the magnitude of SSD at equilibrium were very accurate for weak sexual selection. With stronger sexual selection the total response was greater than predicted. Large changes in SSD can occur without significant long‐term change in the genetic correlation between the sexes. Our results suggest that genetic correlations constrain both the short‐term and long‐term evolution of SSD less than predicted by the Lande model.     

Testosterone,growth and the evolution of sexual size dimorphism

The integration of macroevolutionary pattern with developmental mechanism presents an outstanding challenge for studies of phenotypic evolution. Here, we use a combination of experimental and comparative data to test whether evolutionary shifts in the direction of sexual size dimorphism (SSD) correspond to underlying changes in the endocrine regulation of growth. First, we combine captive breeding studies with mark‐recapture data to show that male‐biased SSD develops in the brown anole lizard (Anolis sagrei) because males grow significantly faster than females as juveniles and adults. We then use castration surgeries and testosterone implants to show that castration inhibits, and testosterone stimulates, male growth. We conclude by reviewing published testosterone manipulations in other squamate reptiles in the context of evolutionary patterns in SSD. Collectively, these studies reveal that the evolution of SSD has been accompanied by underlying changes in the effect of testosterone on male growth, potentially facilitating the rapid evolution of SSD.     

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.     

A developmental perspective on the evolution of sexual size dimorphism of a moth

Males and females of almost all organisms exhibit sexual differences in body size, a phenomenon called sexual size dimorphism (SSD). How the sexes evolve to be different sizes, despite sharing the same genes that control growth and development, and hence a common genetic architecture, has remained elusive. Here, we show that the genetic architecture (heritabilities and genetic correlations) of the physiological mechanism that regulates size during the last stage of larval development of a moth, differs between the sexes, and thus probably facilitates, rather than hinders, the evolution of SSD. We further show that the endocrine system plays a critical role in generating SSD. Our results demonstrate that knowledge of the genetic architecture underlying the physiological process during development that ultimately produces SSD in adults can elucidate how males and females of organisms evolve to be of different sizes.     

A comparative test of adaptive hypotheses for sexual size dimorphism in lizards

It is commonly argued that sexual size dimorphism (SSD) in lizards has evolved in response to two primary, nonexclusive processes: (1) sexual selection for large male size, which confers an advantage in intrasexual mate competition (intrasexual selection hypothesis), and (2) natural selection for large female size, which confers a fecundity advantage (fecundity advantage hypothesis). However, outside of several well-studied lizard genera, the empirical support for these hypotheses has not been examined with appropriate phylogenetic control. We conducted a comparative phylogenetic analysis to test these hypotheses using literature data from 497 lizard populations representing 302 species and 18 families. As predicted by the intrasexual selection hypothesis, male aggression and territoriality are correlated with SSD, but evolutionary shifts in these categorical variables each explain less than 2% of the inferred evolutionary change in SSD. We found stronger correlations between SSD and continuous estimates of intrasexual selection such as male to female home range ratio and female home range size. These results are consistent with the criticism that categorical variables may obscure much of the actual variation in intrasexual selection intensity needed to explain patterns in SSD. In accordance with the fecundity advantage hypothesis, SSD is correlated with clutch size, reproductive frequency, and reproductive mode (but not fecundity slope, reduced major axis estimator of fecundity slope, length of reproductive season, or latitude). However, evolutionary shifts in clutch size explain less than 8% of the associated change in SSD, which also varies significantly in the absence of evolutionary shifts in reproductive frequency and mode. A multiple regression model retained territoriality and clutch size as significant predictors of SSD, but only 16% of the variation in SSD is explained using these variables. Intrasexual selection for large male size and fecundity selection for large female size have undoubtedly helped to shape patterns of SSD across lizards, but the comparative data at present provide only weak support for these hypotheses as general explanations for SSD in this group. Future work would benefit from the consideration of alternatives to these traditional evolutionary hypotheses, and the elucidation of proximate mechanisms influencing growth and SSD within populations.     

The origins of sexual dimorphism in body size in ungulates

Jarman (1974) proposed a series of relationships between habitat use, food dispersion, and social behavior and hypothesized a series of evolutionary steps leading to sexual dimorphism in body size through sexual selection in African antelope species. The hypothesis states that sexual size dimorphism evolved in a three-step process. Initially, ancestral monomorphic and monogamous ungulate species occupying closed habitats radiated into open grassland habitats. Polygynous mating systems then rapidly evolved in response to the aggregation of males and females, perhaps in relation to the clumped distribution of food resources in open habitats. Subsequently, size dimorphism evolved in those species occupying open habitats, but not in species that remained in closed habitats or retained monogamy. This hypothesis has played an important role in explaining the origins of sexual dimorphism in mammals. However, the temporal sequence of the events that Jarman proposed has never been demonstrated. Here we use a phylogeny of extant ungulate species, along with maximum-likelihood statistical techniques, to provide a test of Jarman's hypothesis.     

Directional changes in sexual size dimorphism in shorebirds, gulls and alcids

The Charadrii (shorebirds, gulls and alcids) are one of the most diverse avian groups from the point of view of sexual size dimorphism, exhibiting extremes in both male-biased and female-biased dimorphism, as well as monomorphism. In this study we use phylogenetic comparative analyses to investigate how size dimorphism has changed over evolutionary time, distinguishing between changes that have occurred in females and in males. Independent contrasts analyses show that both body mass and wing length have been more variable in males than in females. Directional analyses show that male-biased dimorphism has increased after inferred transitions towards more polygynous mating systems. There have been analogous increases in female-biased dimorphism after transitions towards more socially polyandrous mating systems. Changes in dimorphism in both directions are attributable to male body size changing more than female body size. We suggest that this might be because females are under stronger natural selection constraints related to fecundity. Taken together, our results suggest that the observed variation in dimorphism of Charadrii can be best explained by male body size responding more sensitively to variable sexual selection than female body size.     

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.     

Sexual selection, sexual size dimorphism and Rensch's rule in Odonata

Odonata (dragonflies and damselflies) exhibit a range of sexual size dimorphism (SSD) that includes species with male-biased (males > females) or female-biased SSD (males < females) and species exhibiting nonterritorial or territorial mating strategies. Here, we use phylogenetic comparative analyses to investigate the influence of sexual selection on SSD in both suborders: dragonflies (Anisoptera) and damselflies (Zygoptera). First, we show that damselflies have male-biased SSD, and exhibit an allometric relationship between body size and SSD, that is consistent with Rensch's rule. Second, SSD of dragonflies is not different from unit, and this suborder does not exhibit Rensch's rule. Third, we test the influence of sexual selection on SSD using proxy variables of territorial mating strategy and male agility. Using generalized least squares to account for phylogenetic relationships between species, we show that male-biased SSD increases with territoriality in damselflies, but not in dragonflies. Finally, we show that nonagile territorial odonates exhibit male-biased SSD, whereas male agility is not related to SSD in nonterritorial odonates. These results suggest that sexual selection acting on male sizes influences SSD in Odonata. Taken together, our results, along with avian studies (bustards and shorebirds), suggest that male agility influences SSD, although this influence is modulated by territorial mating strategy and thus the likely advantage of being large. Other evolutionary processes, such as fecundity selection and viability selection, however, need further investigation.     

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.     

Sexual size dimorphism is not associated with the evolution of parental care in frogs

Sex differences in parental care are thought to arise from differential selection on the sexes. Sexual dimorphism, including sexual size dimorphism (SSD), is often used as a proxy for sexual selection on males. Some studies have found an association between male‐biased SSD (i.e., males larger than females) and the loss of paternal care. While the relationship between sexual selection on males and parental care evolution has been studied extensively, the relationship between female‐biased SSD (i.e., females larger than males) and the evolution of parental care has received very little attention. Thus, we have little knowledge of whether female‐biased SSD coevolves with parental care. In species displaying female‐biased SSD, we might expect dimorphism to be associated with the evolution of paternal care or perhaps the loss of maternal care. Here, drawing on data for 99 extant frog species, we use comparative methods to evaluate how parental care and female‐biased SSD have evolved over time. Generally, we find no significant correlation between the evolution of parental care and female‐biased SSD in frogs. This suggests that differential selection on body size between the sexes is unlikely to have driven the evolution of parental care in these clades and questions whether we should expect sexual dimorphism to exhibit a general relationship with the evolution of sex differences in parental care.     

Sexual size dimorphism predicts the frequency of multiple mating in the sex-role reversed pipefish Syngnathus typhle

The sex-role reversed pipefish Syngnathus typhle is a member of the Syngnathidae, a family of fishes in which males brood embryos on their body surface. As in most ectotherms, embryonic development is highly temperature dependent in syngnathids and male brooding periods are extended when water temperatures are reduced. The influence of temperature on reproduction is expected to effectively truncate the breeding season and reduce fecundity in cold waters, potentially enhancing the opportunity for both fecundity and sexual selection. We studied spatial variation in the morphology and reproductive biology of S. typhle in five European populations which vary in latitude and water temperature. Microsatellite analyses indicated that the average number of male mates per population ranged between 1.3 and 3.7. The frequency of multiple mating by males was negatively correlated with the degree of sexual size dimorphism in each population, suggesting that disproportionate increases in female fecundity may be able to compensate for increased male brood pouch capacity. Both sexes were larger and males had an increased brood size where water temperatures during the breeding season were lower. Morphological variation among populations may be mediated by differences in fecundity selection associated with different optimal reproductive strategies in cold and warm water environments.     

Sexual selection explains Rensch's rule of allometry for sexual size dimorphism

In 1950, Rensch first described that in groups of related species, sexual size dimorphism is more pronounced in larger species. This widespread and fundamental allometric relationship is now commonly referred to as 'Rensch's rule'. However, despite numerous recent studies, we still do not have a general explanation for this allometry. Here we report that patterns of allometry in over 5300 bird species demonstrate that Rensch's rule is driven by a correlated evolutionary change in females to directional sexual selection on males. First, in detailed multivariate analysis, the strength of sexual selection was, by far, the strongest predictor of allometry. This was found to be the case even after controlling for numerous potential confounding factors, such as overall size, degree of ornamentation, phylogenetic history and the range and degree of size dimorphism. Second, in groups where sexual selection is stronger in females, allometry consistently goes in the opposite direction to Rensch's rule. Taken together, these results provide the first clear solution to the long-standing evolutionary problem of allometry for sexual size dimorphism: sexual selection causes size dimorphism to correlate with species size.     

The evolution of fecundity is associated with female body size but not female‐biased sexual size dimorphism among frogs

Sexual size dimorphism (SSD) is one of the most common ways in which males and females differ. Male‐biased SSD (when males are larger) is often attributed to sexual selection favouring large males. When females are larger (female‐biased SSD), it is often argued that natural selection favouring increased fecundity (i.e. larger clutches or eggs) has coevolved with larger female body size. Using comparative phylogenetic and multispecies regression model selection approaches, we test the hypothesis that among‐species variation in female fecundity is associated with the evolution of female‐biased SSD. We also ask whether the hypothesized relationship between SSD and fecundity is relaxed upon the evolution of parental care. Our results suggest a strong relationship between the evolution of fecundity and body size, but we find no significant relationship between fecundity and SSD. Similarly, there does not appear to be a relationship between fecundity and the presence or absence of parental care among species. Thus, although female body size and fecundity coevolve, selection for increased fecundity as an explanation for female‐biased SSD is inconsistent with our analyses. We caution that a relationship between female body size and fecundity is insufficient evidence for fecundity selection driving the evolution of female‐biased SSD.     

Correlates of sexual dimorphism in primates: Ecological and size variables

The effects of a series of ecological and size factors on the degree of sexual dimorphism in body weight and canine size were studied among subsets of 70 primate species. Variation in body-weight dimorphism can be almost entirely attributed to body weight (83% of variance R² of weight dimorphism). Much smaller amounts of the variation can be attributed to mating system (R² =6.8%,polygynous species being more dimorphic than monogamous ones) and diet (R² = 2.5%,frugivorous species being more dimorphic than folivorous ones). Habitat (arboreal vs. terrestrial) and activity rhythm (nocturnal vs. diurnal) have only an indirect effect on weight dimorphism. Variation in canine-size dimorphism can be explained in terms of canine size (R² =49%),activity rhythm (R² = 20%,diurnal species being more dimorphic than nocturnal ones), and mating system (R² = 10%).Habitat and diet do not play a significant role in canine-size dimorphism. The unexpectedly high contribution of size to sexual dimorphism coupled with the observation of increased sexual dimorphism with increased size leads us to formulate a new selection model for the evolution of sexual dimorphism. We suggest that if there is selection for size increase, whatever its cause, directional selection in both males and females will lead to an increase in sexual dimorphism based on differences in genetic variance between the sexes. Sexual selection, resource division between the sexes, or lopsided reproductive selection need not play a role in such a model.