Sexual dimorphism in leg length among orb-weaving spiders: a possible role for sexual cannibalism

The degree and direction of sexual dimorphism across different species is commonly attributed to differences in the selection pressures acting on males and females. The extent of these differences is especially apparent in species that practise sexual cannibalism, where the female attempts to capture and eat a courting male. Here, we investigate the relationship between sexual dimorphism in size and leg length, sexual cannibalism and courtship behaviour in three taxonomic groups of orb-weaving spiders, using morphological data from 249 species in 36 genera. Females are larger than males in all three taxonomic groups, and males have relatively longer legs than females in both the Araneinae and Tetragnathidae. Across genera within each taxonomic group, male body size is positively correlated with both female body size and male leg length, and female body size is positively correlated with female leg length. Sexual size dimorphism is negatively correlated with relative male leg length within the Araneinae, but not within either the Tetragnathidae or the Gasteracanthinae. There was no negative correlation between sexual size dimorphism and relative female leg length in any taxonomic group. We argue that the relationship between sexual size dimorphism and relative male leg length within the Araneinae may be the result of selection imposed by sexual cannibalism by females.     

Factors influencing the degree of sexual size dimorphism within and among calanoid copepod species

Populations of Diaptomus leptopus (Copepoda: Calanoida) and other calanoid copepods exhibit varying degrees of sexual size dimorphism. We examined whether intraspecific or interspecific variation in dimorphism could be explained by allometry, and we examined the relationship between adult size attained and development rate to determine any relationship between the two. We compared the degree of sexual size dimorphism in D. leptopus and in other calanoid copepods inhabiting temporary and permanent habitats. Allometry did not explain variation in sexual size dimorphism within or among populations or among species. Permanence of habitat affected the degree of dimorphism: dimorphism was greater within and among species inhabiting temporary environments. Non-significant differences in development rate were found among populations and significant differences were found between sexes of D. leptopus when reared under identical laboratory conditions: males developed more rapidly than females but there was no general relationship between development rate and adult size. Potential adaptive hypotheses to explain the differences between populations inhabiting temporary and permanent habitats are discussed.     

Sexual size dimorphism within species increases with body size in insects

Studies examining interspecific differences in sexual size dimorphism (SSD) typically assume that the degree of sexual differences in body size is invariable within species. This work was conducted to assess validity of this assumption. As a result of a systematic literature survey, datasets for 158 insect species were retrieved. Each dataset contained adult or pupal weights of males and females for two or more different subsets, typically originating from different conditions during immature development. For each species, an analysis was conducted to examine dependence of SSD on body size, the latter variable being used as a proxy of environmental quality. A considerable variation in SSD was revealed at the intraspecific level in insects. The results suggest that environmental conditions may strongly affect the degree, though not the direction of SSD within species. In most species, female size appeared to be more sensitive to environmental conditions than male size: with conditions improving, there was a larger relative increase in female than male size. As a consequence, sexual differences in size were shown to increase with increasing body size in species with female-biased SSD (females were the larger sex in more than 80% of the species examined). The results were consistent across different insect orders and ecological subdivisions. Mechanisms leading to intraspecific variation in SSD are discussed. This study underlines the need to consider intraspecific variation in SSD in comparative studies.     

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.

     

Sexual selection and sexual size dimorphism in animals

Sexual selection is often considered as a critical evolutionary force promoting sexual size dimorphism (SSD) in animals. However, empirical evidence for a positive relationship between sexual selection on males and male-biased SSD received mixed support depending on the studied taxonomic group and on the method used to quantify sexual selection. Here, we present a meta-analytic approach accounting for phylogenetic non-independence to test how standardized metrics of the opportunity and strength of pre-copulatory sexual selection relate to SSD across a broad range of animal taxa comprising up to 95 effect sizes from 59 species. We found that SSD based on length measurements was correlated with the sex difference in the opportunity for sexual selection but showed a weak and statistically non-significant relationship with the sex difference in the Bateman gradient. These findings suggest that pre-copulatory sexual selection plays a limited role for the evolution of SSD in a broad phylogenetic context.     

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.     

Optimal climbing speed explains the evolution of extreme sexual size dimorphism in spiders

Several hypotheses have been put forward to explain the evolution of extreme sexual size dimorphism (SSD). Among them, the gravity hypothesis (GH) explains that extreme SSD has evolved in spiders because smaller males have a mating or survival advantage by climbing faster. However, few studies have supported this hypothesis thus far. Using a wide span of spider body sizes, we show that there is an optimal body size (7.4 mm) for climbing and that extreme SSD evolves only in spiders that: (1) live in high‐habitat patches and (2) in which females are larger than the optimal size. We report that the evidence for the GH across studies depends on whether the body size of individuals expands beyond the optimal climbing size. We also present an ad hoc biomechanical model that shows how the higher stride frequency of small animals predicts an optimal body size for climbing.     

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.     

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 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.     

Sexual size dimorphism and sexual selection in turtles (order testudines)

Summary This paper combines published and original data on sexual size dimorphism, reproductive behavior, and habitat types in turtles. Our major finding is that observed patterns of sexual size dimorphism correlate with habitat type and male mating strategy. (1) In most terrestrial species, males engage in combat with each other. Males typically grow larger than females. (2) In semiaquatic and bottom-walking aquatic species, male combat is less common, but males often forcibly inseminate females. As in terrestrial species, males are usually larger than females. (3) In truly aquatic species, male combat and forcible insemination are rare. Instead, males utilize elaborate precoital displays, and female choice is highly important. Males are usually smaller than females.We interpret these correlations between sexual behavior and size dimorphism in terms of sexual selection theory: males are larger than females when large male size evolves as an adaptation to increase success in male combat, or to enable forcible insemination of females. In contrast, males are usually smaller than females where small size in males evolves to increase mobility (and hence, ability to locate females), or because selection for increased fecundity may result in increased female size. In turtle species with male combat or forcible insemination, the degree of male size superiority increases with mean species body size.     

Sexual dimorphism in chelicerae size in three species of nuptial-gift spiders: a discussion of possible functions and driving selective forces

Positive allometric patterns observed for intersexual signalling characters are related to directional sexual selection, and supported by theoretical and empirical data. Recent models have shown that positive allometry may not hold as a rule if the influence of natural selection is added to the model. Here we tested these models applying traditional morphometrical techniques for the analysis of chelicerae sexual dimorphism and allometric patterns within the genus Paratrechalea : Paratrechalea azul , Paratrechalea galianoae and Paratrechalea ornata . Spider chelicerae are basically used for prey capture, but males of Paratrechalea also use the chelicerae to offer a nuptial gift during courtship, also presenting a clear size and colour sexual dimorphism supporting a possible role as a signal. Chelicerae size was male biased for all the variables studied and showed an isometric pattern, while females showed a higher variation. Our findings are in accordance with models of viability-related function for prey capture, questioning some statements proposed by the positive allometry model.     

Sexual size dimorphism in species with asymptotic growth after maturity

If animals mature at small sizes and then grow to larger asymptotic sizes, many factors can affect male and female size distributions. Standard growth equations can be used to study the processes affecting sexual size dimorphism in species with asymptotic growth after maturity. This paper first outlines the effects of sex differences in growth and maturation patterns on the direction and degree of sexual dimorphism. The next section considers the effects of variation in age structure or growth rates on adult body sizes and sexual size dimorphism. Field data from a crustacean, fish, lizard and mammal show how information on a species' growth and maturation patterns can be used to predict the relationships between male size, female size and sexual size dimorphism expected if a series of samples from the same population simply differed with respect to their ages or growth rates. The last section considers ecological or behavioural factors with different effects on the growth, maturation, survival or movement patterns of the two sexes. This study supports earlier suggestions that information on growth and maturation patterns may be useful, if not essential, for comparative studies of sexual size dimorphism in taxa with asymptotic growth after maturity.     

The phylogenetic basis of sexual size dimorphism in orb-weaving spiders (Araneae,Orbiculariae)

Extreme sexual body size dimorphism (SSD), in which males are only a small fraction of the size of the females, occurs only in a few, mostly marine, taxonomic groups. Spiders are the only terrestrial group in which small males are relatively common, particularly among orb-weavers (especially in the families Tetragnathidae and Araneidae) and crab spiders (Thomisidae). We used a taxonomic sample of 80 genera to study the phylogenetic patterns (origins and reversals) of SSD in orb-weaving spiders (Orbiculariae). We collected and compiled male and female size data (adult body length) for 536 species. Size data were treated as a continuous character, and ancestral sizes, for males and females separately, were reconstructed by using Wagner parsimony on a cladogram for the 80 genera used in this study. Of these 80 genera, 24 were female-biased dimorphic (twice or more the body length of the male); the remaining 56 genera were monomorphic. Under parsimony only four independent origins of dimorphism are required: in the theridiid genus Tidarren, in the distal nephilines, in the "argiopoid clade," and in the araneid genus Kaira. Dimorphism has reversed to monomorphism at least seven times, all of them within the large "argiopoid clade." The four independent origins of dimorphism represent two separate instances of an increase in female size coupled with a decrease of male size (involving only two genera), and two separate instances of an increase in female size with male size either remaining the same or increasing, but not as much as females (involving 30 genera). In orb-weaving spiders, far more taxa are sexually dimorphic as a result of female size increase (22 genera) than as a result of male size decrease (two genera). SSD in orb-weaving spiders encompasses several independent evolutionary histories that together suggest a variety of evolutionary pathways. This multiplicity strongly refutes all efforts thus far to find a general explanation for either the origin or maintenance (or both) of SSD, because the different pathways very likely will require distinctly different, possibly unique, explanations. Each pattern must be understood historically before its origin and maintenance can be explained in ecological and evolutionary terms. The most frequently cited example of male dwarfism in spiders, the golden orb-weaving spider genus Nephila (Tetragnathidae), is in fact a case of female giantism, not male dwarfism.     

Statistics of sexual size dimorphism

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