Phylogeny suggests nondirectional and isometric evolution of sexual size dimorphism in argiopine spiders

Sexual dimorphism describes substantial differences between male and female phenotypes. In spiders, sexual dimorphism research almost exclusively focuses on size, and recent studies have recovered steady evolutionary size increases in females, and independent evolutionary size changes in males. Their discordance is due to negative allometric size patterns caused by different selection pressures on male and female sizes (converse Rensch's rule). Here, we investigated macroevolutionary patterns of sexual size dimorphism (SSD) in Argiopinae, a global lineage of orb‐weaving spiders with varying degrees of SSD. We devised a Bayesian and maximum‐likelihood molecular species‐level phylogeny, and then used it to reconstruct sex‐specific size evolution, to examine general hypotheses and different models of size evolution, to test for sexual size coevolution, and to examine allometric patterns of SSD. Our results, revealing ancestral moderate sizes and SSD, failed to reject the Brownian motion model, which suggests a nondirectional size evolution. Contrary to predictions, male and female sizes were phylogenetically correlated, and SSD evolution was isometric. We interpret these results to question the classical explanations of female‐biased SSD via fecundity, gravity, and differential mortality. In argiopines, SSD evolution may be driven by these or additional selection mechanisms, but perhaps at different phylogenetic scales.     

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

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

Patterns of sexual size dimorphism in stingless bees: Testing Rensch’s rule and potential causes in highly eusocial bees (Hymenoptera: Apidae,Meliponini)

Eusocial insects offer a unique opportunity to analyze the evolution of body size differences between sexes in relation to social environment. The workers, being sterile females, are not subject to selection for reproductive function providing a natural control for parsing the effects of selection on reproductive function (i.e., sexual and fecundity selection) from other kinds of natural selection. Patterns of sexual size dimorphism (SSD) and testing of Rensch's rule controlling for phylogenetic effects were analyzed in the Meliponini or stingless bees. Theory predicts that queens may exhibit higher selection for fecundity in eusocial taxa, but contrary to this, we found mixed patterns of SSD in Meliponini. Non‐Melipona species generally have a female‐biased SSD, while all analyzed species of Melipona showed a male‐biased SSD, indicating that the direction and magnitude of the selective pressures do not operate in the same way for all members of this taxon. The phylogenetic regressions revealed that the rate of divergence has not differed between the two castes of females and the males, that is, stingless bees do not seem to follow Rensch's rule (a slope >1), adding this highly eusocial taxon to the various solitary insect taxa not conforming with it. Noteworthy, when Melipona was removed from the analysis, the phylogenetic regressions for the thorax width of males on queens had a slope significantly smaller than 1, suggesting that the evolutionary divergence has been larger in queens than males, and could be explained by stronger selection on female fecundity only in non‐Melipona species. Our results in the stingless bees question the classical explanation of female‐biased SSD via fecundity and provide a first evidence of a more complex determination of SSD in highly eusocial species. We suggest that in highly eusocial taxa, additional selection mechanisms, possibly related to individual and colonial interests, could influence the evolution of environmentally determined traits such as body 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.     

The evolution of sexual size dimorphism in cottontail rabbits (Sylvilagus,Leporidae)

In mammals, ‘female‐biased’ sexual size dimorphism (SSD), in which females are larger than males, is uncommon. In the present study, we examined Sylvilagus, a purported case of female‐biased SSD, for evolutionary correlations among species between SSD, body‐size, and life‐history variables. We find that: (1) although most species are female‐biased, the degree and direction of SSD vary more than was previously recognized and (2) the degree of SSD decreases with increasing body size. Hence, Sylvilagus provides a new example, unusual for a female‐biased taxon, in which allometry for SSD is consistent with ‘Rensch's Rule’. As a corollary to Rensch's Rule, we observe that changes in SSD in Sylvilagus are typically associated with larger, more significant changes in males than females. Female‐biased SSD could be produced by selection for larger females, smaller males, or both. Although larger female size may be related to high fecundity and the extremely rapid fetal and neonatal growth in Sylvilagus, we find little evidence for a correlation between SSD and various fecundity‐related traits in among‐species comparisons. Smaller male size may confer greater reproductive success through greater mobility and reduced energetic requirements. We propose that a suite of traits (female dispersion, large male home ranges, reduced aggression, and a promiscuous mating system) has favoured smaller males and thus influenced the evolution of SSD in cottontails. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 141–156.     

Evolution of sexual size dimorphism in grouse and allies (Aves: Phasianidae) in relation to mating competition,fecundity demands and resource division

Sexual size dimorphism (SSD) is often assumed to be driven by three major selective processes: (1) sexual selection influencing male size and thus mating success, (2) fecundity selection acting on females and (3) inter‐sexual resource division favouring different size in males and females to reduce competition for resources. Sexual selection should be particularly strong in species that exhibit lek polygyny, since male mating success is highly skewed in such species. We investigated whether these three selective processes are related to SSD evolution in grouse and allies (Phasianidae). Male‐biased SSD increased with body size (Rensch’s rule) and lekking species exhibited more male‐biased SSD than nonlekking ones. Directional phylogenetic analyses indicated that lekking evolved before SSD, but conclusions were highly dependent on the body size traits and chosen model values. There was no relationship between SSD and male display agility, nor did resource division influence SSD. Although clutch mass increased with female body size it was not related to the degree of SSD. Taken together, the results are most consistent with the hypothesis that lekking behaviour led to the evolution of male‐biased SSD in Phasianidae.     

Ecological divergence and sexual selection drive sexual size dimorphism in new world pitvipers (Serpentes: Viperidae)

Hypotheses for the origin and maintenance of sexual size dimorphism (SSD) fall into three primary categories: (i) sexual selection on male size, (ii) fecundity selection on female size and (iii) ecological selection for gender‐specific niche divergence. We investigate the impact of these forces on SSD evolution in New World pitvipers (Crotalinae). We constructed a phylogeny from up to eight genes (seven mitochondrial, one nuclear) for 104 species of NW crotalines. We gathered morphological and ecological data for 82 species for comparative analyses. There is a strong signal of sexual selection on male size driving SSD, but less evidence for fecundity selection on female size across lineages. No support was found for allometric scaling of SSD (Rensch's rule), nor for directional selection for increasing male size (the Fairbairn–Preziosi hypothesis) in NW crotalines. Interestingly, arboreal lineages experience higher rates of SSD evolution and a pronounced shift to female‐biased dimorphism. This suggests that fecundity selection on arboreal females exaggerates ecologically mediated dimorphism, whereas sexual selection drives male size in terrestrial lineages. We find that increasing SSD in both directions (male‐ and female‐biased) decreases speciation rates. In NW crotalines, it appears that increasing magnitudes of ecologically mediated SSD reduce rates of speciation, as divergence accumulates within species among sexes, reducing adaptive divergence between populations leading to speciation.     

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.     

Function‐related Drivers of Skull Morphometric Variation and Sexual Size Dimorphism in a Subterranean Rodent,Plateau Zokor (Eospalax baileyi)

Sexual dimorphism is prevalent in most living organisms. The difference in size between sexes of a given species is generally known as sexual size dimorphism (SSD). The magnitude of the SSD is determined by Rensch's rule where size dimorphism increases with increasing body size when the male is the larger sex and decreases with increasing average body size when the female is the larger sex. The unique underground environment that zokors (Eospalax baileyi) live under in the severe habitat of the Qinghai‐Tibetan Plateau (QTP) could create SSD selection pressures that may or may not be supported by Rensch's rule, making this scientific question worthy of investigation. In this study, we investigated the individual variation between sexes in body size and SSD of plateau zokors using measurements of 19 morphological traits. We also investigated the evolutionary mechanisms underlying SSD in plateau zokors. Moreover, we applied Rensch's rule to all extant zokor species. Our results showed male‐biased SSD in plateau zokors: The body‐ and head‐related measurements were greater in males than in females. Linear regression analysis between body length, body weight, and carcass weight showed significant relationships with some traits such as skull length, lower incisor length, and tympanic bulla width, which might support our prediction that males have faster growth rates than females. Further, the SSD pattern corroborated the assumption of Rensch's rule in plateau zokors but not in the other zokor species. Our findings suggest that the natural underground habitat and behavioral differences between sexes can generate selection pressures on male traits and contribute to the evolution of SSD in plateau zokors.     

Macroecological patterns of sexual size dimorphism in turtles of the world

Sexual size dimorphism (SSD) is a well‐documented phenomenon in both plants and animals; however, the ecological and evolutionary mechanisms that drive and maintain SSD patterns across geographic space at regional and global scales are understudied, especially for reptiles. Our goal was to examine geographic variation of turtle SSD and to explore ecological and environmental correlates using phylogenetic comparative methods. We use published body size data on 135 species from nine turtle families to examine how geographic patterns and the evolution of SSD are influenced by habitat specialization, climate (annual mean temperature and annual precipitation) and climate variability, latitude, or a combination of these predictor variables. We found that geographic variation, magnitude and direction of turtle SSD are best explained by habitat association, annual temperature variance and annual precipitation. Use of semi‐aquatic and terrestrial habitats was associated with male‐biased SSD, whereas use of aquatic habitat was associated with female‐biased SSD. Our results also suggest that greater temperature variability is associated with female‐biased SSD. In contrast, wetter climates are associated with male‐biased SSD compared with arid climates that are associated with female‐biased SSD. We also show support for a global latitudinal trend in SSD, with females being larger than males towards the poles, especially in the families Emydidae and Geoemydidae. Estimates of phylogenetic signal for both SSD and habitat type indicate that closely related species occupy similar habitats and exhibit similar direction and magnitude of SSD. These global patterns of SSD may arise from sex‐specific reproductive behaviour, fecundity and sex‐specific responses to environmental factors that differ among habitats and vary systematically across latitude. Thus, this study adds to our current understanding that while SSD can vary dramatically across and within turtle species under phylogenetic constraints, it may be driven, maintained and exaggerated by habitat type, climate and geographic location.