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.     

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.     

HAVE MALE AND FEMALE GENITALIA COEVOLVED? A PHYLOGENETIC ANALYSIS OF GENITALIC MORPHOLOGY AND SEXUAL SIZE DIMORPHISM IN WEB‐BUILDING SPIDERS (ARANEAE: ARANEOIDEA)

Sexual size dimorphism (SSD) can strongly influence the evolution of reproductive strategies and life history. If SSD is extreme, and other characters (e.g., genitalic size) also increase with size, then functional conflicts may arise between the sexes. Spiders offer an excellent opportunity to investigate this issue because of their wide range of SSD. By using modern phylogenetic methods with 16 species of orb-weaving spiders, we provide strong evidence for the "positive genitalic divergence" model, implying that sexual genitalic dimorphism (SGD) increases as SSD increases. This pattern is supported by an evolutionary mismatch between the absolute sizes of male and female genitalia across species. Indeed, our findings reveal a dramatic reversal from male genitalia that are up to 87x larger than female genitalia in size-monomorphic species to female genitalia that are up to 2.8x larger in extremely size-dimorphic species. We infer that divergence in SGD could limit SSD both in spiders, and potentially in other taxa as well. Further, male and female body size, as well as male and female genitalia size, are decoupled evolutionarily. Finally, we show a negative scaling (hypoallometry) of male and female genitalic morphology within sexes. Evolutionary forces specific to each sex, such as larger female size (increased fecundity) or smaller male size (enhanced mate-searching ability), may be balanced by stabilizing selection on relative genitalic size.     

Competing dwarf males: sexual selection in an orb-weaving spider

Hypotheses for the adaptive significance of extreme female-biased sexual size dimorphism (SSD) generally assume that in dimorphic species males rarely interfere with each other. Here we provide the first multivariate examination of sexual selection because of male-male competition over access to females in a species with 'dwarf' males, the orb-weaving spider Argiope aurantia. Male A. aurantia typically try to mate opportunistically during the female's final moult when she is defenceless. We show that, contrary to previous hypotheses, the local operational sex ratio (males per female on the web) is male-biased most of the season. Both interference and scramble competition occur during opportunistic mating, the former leading to significant selection for large male body size. Male condition and leg length had no effect on mating success independent of size. We discuss these findings in the context of the evolution of extreme female-biased SSD in this clade.     

Selection on male size,leg length and condition during mate search in a sexually highly dimorphic orb-weaving spider

Mate search plays a central role in hypotheses for the adaptive significance of extreme female-biased sexual size dimorphism (SSD) in animals. Spiders (Araneae) are the only free-living terrestrial taxon where extreme SSD is common. The gravity hypothesis states that small body size in males is favoured during mate search in species where males have to climb to reach females, because body length is inversely proportional to achievable speed on vertical structures. However, locomotive performance of males may also depend on relative leg length. Here we examine selection on male body size and leg length during mate search in the highly dimorphic orb-weaving spider Argiope aurantia, using a multivariate approach to distinguish selection targeted at different components of size. Further, we investigate the scaling relationships between male size and energy reserves, and the differential loss of reserves. Adult males do not feed while roving, and a size-dependent differential energy storage capacity may thus affect male performance during mate search. Contrary to predictions, large body size was favoured in one of two populations, and this was due to selection for longer legs. Male size was not under selection in the second population, but we detected direct selection for longer third legs. Males lost energy reserves during mate search, but this was independent of male size and storage capacity scaled isometrically with size. Thus, mate search is unlikely to lead to selection for small male size, but the hypothesis that relatively longer legs in male spiders reflect a search-adapted morphology is supported.     

THE EVOLUTION OF FEMALE-BIASED SEXUAL SIZE DIMORPHISM: A POPULATION-LEVEL COMPARATIVE STUDY IN HORNED LIZARDS (PHRYNOSOMA)

Female-biased sexual size dimorphism is uncommon among vertebrates and traditionally has been attributed to asymmetric selective pressures favoring large fecund females (the fecundity-advantage hypothesis) and/or small mobile males (the small-male advantage hypothesis). I use a phylogenetically based comparative method to address these hypotheses for the evolution and maintenance of sexual size dimorphism among populations of three closely related lizard species (Phrynosoma douglasi, P. ditmarsi, and P. hernandezi). With independent contrasts I estimate evolutionary correlations among female body size, male body size, and sexual size dimorphism (SSD) to determine whether males have become small, females have become large, or both sexes have diverged concurrently in body size during the evolutionary Xhistory of this group. Population differences in degree of SSD are inversely correlated with average male body size, but are not correlated with average female body size. Thus, variation in SSD among populations has occurred predominantly through changes in male size, suggesting that selective pressures on small males may affect degree of SSD in this group. I explore three possible evolutionary mechanisms by which the mean male body size in a population could evolve: changes in size at maturity, changes in the variance of male body sizes, and changes in skewness of male body size distributions. Comparative analyses indicate that population differentiation in male body size is achieved by changes in male size at maturity, without changes in the variance or skewness of male and female size distributions. This study demonstrates the potential of comparative methods at lower taxonomic levels (among populations and closely related species) for studying microevolutionary processes that underlie population differentiation.     

Sexual size dimorphism predicts the frequency of sexual cannibalism within and among species of spiders

Sexual cannibalism varies widely among spiders, but no general evolutionary hypothesis has emerged to explain its distribution across taxa. Sexual size dimorphism (SSD) also varies widely among spiders and could affect the vulnerability of males to cannibalistic attacks by females. We tested for a relationship between SSD and sexual cannibalism within and among species of spiders, using a broad taxonomic data set. For most species, cannibalism was more likely when males were much smaller than females. In addition, using phylogenetically controlled and uncontrolled analyses, there was a strong positive relationship between average SSD of a species and the frequency of sexual cannibalism. This is the first evidence that the degree of size difference between males and females is related to the phylogenetic distribution of sexual cannibalism among a broad range of spiders.     

Sexual size dimorphism and phylogeny in North American minnows

Sexual size dimorphism (SSD) is predicted to vary across mating systems. A previous study examined a model of SSD in fishes as it relates to three mating system variables: probability of sperm competition, male territorial guarding, and male-male contest. I tested the ability of these variables to predict SSD in North American freshwater minnows, after controlling for phylogenetic effects by an independent contrasts method. Across 58 species only male territorial guarding was significandy related to SSD in a stepwise multiple regression. When tested for 26 genera and subgenera, both male territorial guarding and male-male contest were significant in the model. The concentrated-changes test revealed that character changes in SSD (from males the same size or smaller than females, to males larger than females) were more concentrated on branches with presence of male guarding (similar results were found for changes in SSD and presence of sperm competition), at the species and genus levels. Both comparative approaches demonstrated that male guarding and male-male contest variables are linked to SSD in minnows.     

Macroevolutionary pattern of sexual size dimorphism in geckos corresponds to intraspecific temperature‐induced variation

Many animal lineages exhibit allometry in sexual size dimorphism (SSD), known as ‘Rensch’s rule’. When applied to the interspecific level, this rule states that males are more evolutionary plastic in body size than females and that male‐biased SSD increases with body size. One of the explanations for the occurrence of Rensch’s rule is the differential‐plasticity hypothesis assuming that higher evolutionary plasticity in males is a consequence of larger sensitivity of male growth to environmental cues. We have confirmed the pattern consistent with Rensch’s rule among species of the gecko genus Paroedura and followed the ontogeny of SSD at three constant temperatures in a male‐larger species (Paroedura picta). In this species, males exhibited larger temperature‐induced phenotypic plasticity in final body size than females, and body size and SSD correlated across temperatures. This result supports the differential‐plasticity hypothesis and points to the role phenotypic plasticity plays in generating of evolutionary novelties.     

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

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

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.     

The Proximate Causes of Sexual Size Dimorphism in Phrynocephalus przewalskii

Sexual size dimorphism (SSD) is a common phenomenon and is a central topic in evolutionary biology. Recently, the importance of pursuing an ontogenetic perspective of SSD has been emphasized, to elucidate the proximate physiological mechanisms leading to its evolution. However, such research has seldom focused on the critical periods when males and females diverge. Using mark-recapture data, we investigated the development of SSD, sex-specific survivorship, and growth rates in Phrynocephalus przewalskii (Agamidae). We demonstrated that both male and female lizards are reproductively mature at age 10–11 months (including 5 months hibernation). Male-biased SSD in snout-vent length (SVL) was only found in adults and was fully expressed at age 11 months (June of the first full season of activity), just after sexual maturation. However, male-biased SSD in tail length (TL), hind-limb length (LL), and head width (HW) were fully expressed at age 9–10 months, just before sexual maturation. Analysis of age-specific linear growth rates identified sexually dimorphic growth during the fifth growth month (age 10–11 months) as the proximate cause of SSD in SVL. The males experienced higher mortality than females in the first 2 years and only survived better than females after SSD was well developed. This suggests that the critical period of divergence in the sizes of male and female P. przewalskii occurs between 10 and 11 months of age (May to June during the first full season of activity), and that the sexual difference in growth during this period is the proximate cause. However, the sexual difference in survivorship cannot explain the male-biased SSD in SVL. Our results indicate that performance-related characteristics, such as TL, HW, and LL diverged earlier than SVL. The physiological mechanisms underlying the different growth patterns of males and females may reflect different energy allocations associated with their different reproductive statuses.     

Ecological drivers of body size evolution and sexual size dimorphism in short‐horned grasshoppers (Orthoptera: Acrididae)

Sexual size dimorphism (SSD) is widespread and variable in nature. Although female‐biased SSD predominates among insects, the proximate ecological and evolutionary factors promoting this phenomenon remain largely unstudied. Here, we employ modern phylogenetic comparative methods on eight subfamilies of Iberian grasshoppers (85 species) to examine the validity of different models of evolution of body size and SSD and explore how they are shaped by a suite of ecological variables (habitat specialization, substrate use, altitude) and/or constrained by different evolutionary pressures (female fecundity, strength of sexual selection, length of the breeding season). Body size disparity primarily accumulated late in the history of the group and did not follow a Brownian motion pattern, indicating the existence of directional evolution for this trait. We found support for the converse of Rensch's rule (i.e. females are proportionally bigger than males in large species) across all taxa but not within the two most speciose subfamilies (Gomphocerinae and Oedipodinae), which showed an isometric pattern. Our results do not provide support for the fecundity or sexual selection hypotheses, and we did not find evidence for significant effects of habitat use. Contrary to that expected, we found that species with narrower reproductive window are less dimorphic in size than those that exhibit a longer breeding cycle, suggesting that male protandry cannot solely account for the evolution of female‐biased SSD in Orthoptera. Our study highlights the need to consider alternatives to the classical evolutionary hypotheses when trying to explain why in certain insect groups males remain small.     

Sexual cannibalism, competition, and size dimorphism in the orb-weaving spider Nephila plumipes Latreille (Araneae: Araneoidea)

The degree and direction of sexual dimorphism varies widely,but in several taxa of orb-weaving spiders, including Nephila,males may be less than one-tenth the size of females. This differenceis commonly attributed to selection through precopulation sexualcannibalism: females may either fail to detect very small males,or ignore them as potential prey items. However, there is oftenthe potential for male-male competition in these species becauseseveral males can be found on the web of a single female. Weinvestigated experimentally the effects of sexual cannibalismand male-male competition on male body size and hence sexualdimorphism in the Australian golden orb-weaver (Nephila plumipes).Small males were less likely to be detected and cannibalizedthan larger males. However, larger males excluded small malesfrom the central hub of the web, where mating takes place. Theconflicting effects of sexual cannibalism and male-male competitionmay be responsible for the relatively large variation in malebody size in this species.     

The role of fecundity and sexual selection in the evolution of size and sexual size dimorphism in New World and Old World voles (Rodentia: Arvicolinae)

Evolutionary ecologists dating back to Darwin (1871) have sought to understand why males are larger than females in some species, and why females are the larger sex in others. Although the former is widespread in mammals, rodents and other small mammals usually exhibit low levels of sexual size dimorphism (SSD). Here, we investigate patterns of sexual dimorphism in 34 vole species belonging to the subfamily Arvicolinae in a phylogenetic comparative framework. We address the potential role of sexual selection and fecundity selection in creating sex differences in body size. No support was found for hyperallometric scaling of male body size to female body size. We observed a marginally significant relationship between SSD and the ratio of male to female home range size, with the latter being positively related to the level of intrasexual competition for mates. This suggests that sexual selection favours larger males. Interestingly, we also found that habitat type, but not mating system, constitutes a strong predictor of SSD. Species inhabiting open habitats – where males have extensive home ranges in order to gain access to as many females as possible – exhibit a higher mean dimorphism than species inhabiting closed habitats, where females show strong territoriality and an uniform distribution preventing males to adopt a territorial strategy for gaining copulations. Nonetheless, variation in the strength of sexual selection is not the only selective force shaping SSD in voles; we also found a positive association between female size and litter size across lineages. Assuming this relationship also exists within lineages (i.e. fecundity selection on female size), this suggests an additional role for variation in the strength of fecundity selection shaping interspecific differences in female size, and indirectly in SSD. Therefore our results suggest that different selective processes act on the sizes of males and females, but because larger size is favoured in both sexes, SSD is on average relatively small.     

A phylogeny of the high-elevation Tibetan megophryid frogs and evidence for the multiple origins of reversed sexual size dimorphism

A molecular phylogeny of the high-elevation Tibetan megophryid frogs was reconstructed using mitochondrial and nuclear gene sequences. Both parsimony and Bayesian analysis produced similar tree topologies, which identified the genus Leptobrachium as a sister group to Vibrissaphora , and the genera Oreolalax and Scutiger as monophyletic groups. Within the latter two genera, several species groups were also clearly recognized. At least 13 megophryids display reversed sexual size dimorphism (RSSD), where males are equal to or larger than females. According to our phylogenetic hypothesis, RSSD may have independently evolved at least five times or as many as seven times in this group. The multiple origins of RSSD within this group provide an excellent opportunity for studying the relationship between body size sexual dimorphism and other life-history traits and for determining the costs and benefits of RSSD.     

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.     

The eunuch phenomenon: adaptive evolution of genital emasculation in sexually dimorphic spiders

Under natural and sexual selection traits often evolve that secure paternity or maternity through self‐sacrifice to predators, rivals, offspring, or partners. Emasculation—males removing their genitals—is an unusual example of such behaviours. Known only in insects and spiders, the phenomenon's adaptiveness is difficult to explain, yet its repeated origins and association with sexual size dimorphism (SSD) and sexual cannibalism suggest an adaptive significance. In spiders, emasculation of paired male sperm‐transferring organs — secondary genitals — (hereafter, palps), results in ‘eunuchs’. This behaviour has been hypothesized to be adaptive because (i) males plug female genitals with their severed palps (plugging hypothesis), (ii) males remove their palps to become better fighters in male–male contests (better‐fighter hypothesis), perhaps reaching higher agility due to reduced total body mass (gloves‐off hypothesis), and (iii) males achieve prolonged sperm transfer through severed genitals (remote‐copulation hypothesis). Prior research has provided evidence in support of these hypotheses in some orb‐weaving spiders but these explanations are far from general. Seeking broad macroevolutionary patterns of spider emasculation, we review the known occurrences, weigh the evidence in support of the hypotheses in each known case, and redefine more precisely the particular cases of emasculation depending on its timing in relation to maturation and mating: ‘pre‐maturation’, ‘mating’, and ‘post‐mating’. We use a genus‐level spider phylogeny to explore emasculation evolution and to investigate potential evolutionary linkage between emasculation, SSD, lesser genital damage (embolic breakage), and sexual cannibalism (females consuming their mates). We find a complex pattern of spider emasculation evolution, all cases confined to Araneoidea: emasculation evolved at least five and up to 11 times, was lost at least four times, and became further modified at least once. We also find emasculation, as well as lesser genital damage and sexual cannibalism, to be significantly associated with SSD. These behavioural and morphological traits thus likely co‐evolve in spiders. Emasculation can be seen as an extreme form of genital mutilation, or even a terminal investment strategy linked to the evolution of monogyny. However, as different emasculation cases in araneoid spiders are neither homologous nor biologically identical, and may or may not serve as paternity protection, the direct link to monogyny is not clear cut. Understanding better the phylogenetic patterns of emasculation and its constituent morphologies and behaviours, a clearer picture of the intricate interplay of natural and sexual selection may arise. With the here improved evolutionary resolution of spider eunuch behaviour, we can more specifically tie the evidence from adaptive hypotheses to independent cases, and propose promising avenues for further research of spider eunuchs, and of the evolution of monogyny.     

宁波滑蜥两性异形和雌性繁殖

蜥蜴的雌性繁殖特征对理解两性异形的进化原因起着重要作用。于2011年4月在安徽滁州采集宁波滑蜥(Scincella modesta),定量研究该种形态特征的两性异形和雌性繁殖特征,检验成体形态特征两性异形与雌性繁殖的相关性。研究共采集43条(17♀♀,26♂♂)宁波滑蜥,雄性和雌性个体的最大体长分别为47.4 mm和46.6 mm。雌雄两性在体长和头宽上没有差异,而在腹长和头长上差异显著,雄性有较大的头长,雌性有较大的腹长。宁波滑蜥年产单窝卵。窝卵数和窝卵重与雌体体长及腹长呈正相关,卵重与雌体体长无相关性。窝卵数及卵重的变异系数分别为0.20和0.12。卵长径与窝卵数呈负相关,而卵短径与窝卵数无关。雌体主要通过增加窝卵数来增加繁殖输出。这些结果表明,宁波滑蜥是雌雄个体大小同形的两性异形模式,性选择使得雄性有着较大的头长,以具有较高的交配成功率,生育力选择使得雌性有着较大的腹长,以具有较大的生育力和繁殖输出。     

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.