Sexual Size Dimorphism In Spiders Research Articles

Cross-sex genetic correlation does not extend to sexual size dimorphism in spiders.

Males and females are often subjected to different selection pressures for homologous traits, resulting in sex-specific optima. Because organismal attributes usually share their genetic architectures, sex-specific selection may lead to intralocus sexual conflict. Evolution of sexual dimorphism may resolve this conflict, depending on the degree of cross-sex genetic correlation (r MF) and the strength of sex-specific selection. In theory, high r MF implies that sexes largely share the genetic base for a given trait and are consequently sexually monomorphic, while low r MF indicates a sex-specific genetic base and sexual dimorphism. Here, we broadly test this hypothesis on three spider species with varying degrees of female-biased sexual size dimorphism, Larinioides sclopetarius (sexual dimorphism index, SDI = 0.85), Nuctenea umbratica (SDI = 0.60), and Zygiella x-notata (SDI = 0.46). We assess r MF via same-sex and opposite-sex heritability estimates. We find moderate body mass heritability but no obvious patterns in sex-specific heritability. Against the prediction, the degree of sexual size dimorphism is unrelated to the relative strength of same-sex versus opposite-sex heritability. Our results do not support the hypothesis that sexual size dimorphism is negatively associated with r MF. We conclude that sex-specific genetic architecture may not be necessary for the evolution of a sexually dimorphic trait.

Energetics, scaling and sexual size dimorphism of spiders.

The extreme sexual size dimorphism in spiders has motivated studies for many years. In many species the male can be very small relative to the female. There are several hypotheses trying to explain this fact, most of them emphasizing the role of energy in determining spider size. The aim of this paper is to review the role of energy in sexual size dimorphism of spiders, even for those spiders that do not necessarily live in high foliage, using physical and allometric principles. Here we propose that the cost of transport or equivalently energy expenditure and the speed are traits under selection pressure in male spiders, favoring those of smaller size to reduce travel costs. The morphology of the spiders responds to these selective forces depending upon the lifestyle of the spiders. Climbing and bridging spiders must overcome the force of gravity. If bridging allows faster dispersal, small males would have a selective advantage by enjoying more mating opportunities. In wandering spiders with low population density and as a consequence few male-male interactions, high speed and low energy expenditure or cost of transport should be favored by natural selection. Pendulum mechanics show the advantages of long legs in spiders and their relationship with high speed, even in climbing and bridging spiders. Thus small size, compensated by long legs should be the expected morphology for a fast and mobile male spider.

Evolution and maintenance of sexual size dimorphism: aligning phylogenetic and experimental evidence

Integrating the insights derived from both phylogenetic and experimental approaches offers a more complete understanding of evolutionary patterns and processes, yet it is rarely a feature of investigations of the evolutionary significance of trait variation. We combine these approaches to reinterpret the patterns and processes in the evolution of female biased sexual size dimorphism in Nephilidae, a spider lineage characterized by the most extreme sexual size dimorphism among terrestrial animals. We use a molecular phylogeny to reconstruct the size evolution for each sex and reveal a case of “sexually dimorphic gigantism”: both sexes steadily outgrow their ancestral sizes, but the female and male slopes differ, and hence sexual size dimorphism steadily increases. A review of the experimental evidence reveals a predominant net selection for large size in both sexes, consistent with the phylogenetic pattern for females but not for males. Thus, while sexual size dimorphism in spiders most likely originates and is maintained by fecundity selection on females, it is unclear what selection pressures prevent males from becoming as large as females. This integrated approach highlights the dangers of inferring evolutionary significance from experimental studies that isolate the effects of single selection pressures.

Scramble competition for moulting females as a driving force for extreme male dwarfism in spiders

Extreme sexual size dimorphism in spiders is generally assumed to result from female gigantism, male dwarfism or both. However, field evidence demonstrating the existence and nature of these driving mechanisms is still lacking. In this study we performed field monitoring and laboratory manipulations on the giant wood spider, Nephila pilipes, to assess pre- and postcopulatory sexual selection pressures on males. Results of field monitoring showed that females frequently changed web sites and travelled for long distances and consequently the advantage of large males in occupying favourable positions on webs did not guarantee them higher mating opportunities. Most of the mating events occurred during female moulting but there was typically only one male present on a female’s web, indicating a low level of precopulatory maleemale physical competition. Results of staged double-mating experiments using the sterile-male technique showed that sperm competition in N. pilipes followed a mixed-priority pattern. So males able to find a moulting female earlier than their rivals, to monopolize it to transfer more sperm, are favoured. Therefore, scramble competition for suitable but ephemeral penultimate-stage females is one major force driving protandry and maintaining small body size in spiders with extreme sexual dimorphism.

The effects of morphology and substrate diameter on climbing and locomotor performance in male spiders

Summary 1. Spiders are the most sexually size dimorphic terrestrial animals and the evolution of this dimorphism is controversial. Patterns of sexual size dimorphism (SSD) in spiders have been related to individual performance and size. In 2002 Moya‐Laraño, Halaj & Wise proposed the ‘gravity hypothesis’ to explain patterns of sexual size dimorphism in spiders whereby species building webs high in the vegetation are predicted to show greater SSD than those that build lower down. They advocated an advantage in climbing speed in smaller males searching for females in high places. The gravity hypothesis predicts a negative relationship between male size and climbing speed. In 2007 Brandt & Andrade questioned this interpretation and proposed that the pattern of SSD in spiders is better explained by an advantage for larger males of low‐dwelling species to run faster along the ground. 2. We induced male spiders to run a standard distance up vertical poles of different diameters to examine the predicted relationship between size and climbing speed. We tested two species of extremely size‐dimorphic orb‐web spiders, Argiope keyserlingi and Nephila plumipes, that differ in the height at which females tend to build webs, and one species of jumping spider, Jacksonoides queenslandica, with low levels of size dimorphism. We also examined morphological determinants of horizontal motility by inducing males to run along a raceway. 3. Substrate diameter was consistently found to influence climbing performance. In N. plumipes, climbing speed was slowest on the widest diameter substrate. In A. keyserlingi, size‐adjusted leg length and substrate diameter interacted to determine climbing speed, while in J. queenslandica, there was an interaction between body size and substrate diameter on climbing speed. In the effect of substrate diameter, we have identified a potential bias in previous tests of the gravity hypothesis. 4. Our results do not support the prediction of the gravity hypothesis. There was no evidence of a negative relationship between body size and climbing speed in the two orb‐web species with high levels of SSD. Our results are also not consistent with a recent modification of the gravity hypothesis that suggests a curvilinear relationship between climbing speed and size. 5. Body size was positively associated with maximum running speed only in the cursorial hunter J. queenslandica. For this spider, results are more consistent with Brandt & Andrade’s explanation for variation in SSD in spiders, that larger males are selected for superior running ability in low‐dwelling species, rather than selection for smaller size for climbing to females in high‐dwelling species.

Introducing the refined gravity hypothesis of extreme sexual size dimorphism.

BackgroundExplanations for the evolution of female-biased, extreme Sexual Size Dimorphism (SSD), which has puzzled researchers since Darwin, are still controversial. Here we propose an extension of the Gravity Hypothesis (i.e., the GH, which postulates a climbing advantage for small males) that in conjunction with the fecundity hypothesis appears to have the most general power to explain the evolution of SSD in spiders so far. In this "Bridging GH" we propose that bridging locomotion (i.e., walking upside-down under own-made silk bridges) may be behind the evolution of extreme SSD. A biomechanical model shows that there is a physical constraint for large spiders to bridge. This should lead to a trade-off between other traits and dispersal in which bridging would favor smaller sizes and other selective forces (e.g. fecundity selection in females) would favor larger sizes. If bridging allows faster dispersal, small males would have a selective advantage by enjoying more mating opportunities. We predicted that both large males and females would show a lower propensity to bridge, and that SSD would be negatively correlated with sexual dimorphism in bridging propensity. To test these hypotheses we experimentally induced bridging in males and females of 13 species of spiders belonging to the two clades in which bridging locomotion has evolved independently and in which most of the cases of extreme SSD in spiders are found.ResultsWe found that 1) as the degree of SSD increased and females became larger, females tended to bridge less relative to males, and that 2) smaller males and females show a higher propensity to bridge.ConclusionsPhysical constraints make bridging inefficient for large spiders. Thus, in species where bridging is a very common mode of locomotion, small males, by being more efficient at bridging, will be competitively superior and enjoy more mating opportunities. This "Bridging GH" helps to solve the controversial question of what keeps males small and also contributes to explain the wide range of SSD in spiders, as those spider species in which extreme SSD has not evolved but still live in tall vegetation, do not use bridging locomotion to disperse.

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.

Mass-mediated sex differences in climbing patterns support the gravity hypothesis of sexual size dimorphism

Abstract. The gravity hypothesis of sexual size dimorphism can explain the patterns of extreme sexual size dimorphism in spiders (males smaller than females) because small males climb faster and therefore may be better at reaching females that live in high habitats. Recently, the main prediction of a negative relationship between climbing speed and body size in spiders has been called into question. Here we induced males and females of the spider Leucauge venusta (Tetragnathidae) to run on vertical surfaces and found partial support for the gravity hypothesis. As predicted, males climb faster than females and we demonstrated that this effect is an indirect effect mediated by the negative relationship between body mass and climbing speed. We validate our results using simulated data showing that there is enough statistical efficiency in our data set to support our conclusions. We distinguished between direct and indirect effects (through mass) on sex differences in climbing speed by means of path analysis. Thus, we provide empirical evidence that by being smaller, males are able to climb faster than females. However, we found only a barely significant negative relationship between climbing speed and body size when only males were considered. Reasons for such results are discussed within the text.

What is the matter with the gravity hypothesis?

Although gravity undoubtedly exerts substantial effects on locomotor performance, we dispute the arguments made in defence of the Gravity Hypothesis (GH) in Moya-Laraño et al.'s Forum contribution. Moya-Laraño et al. presented a list of supposed errors in rebuttal of our paper (Brandt & Andrade 2007), yet failed to address core questions we raised as objections to the GH for sexual size dimorphism (SSD): (i) Why should muscle cross-sectional area be proportional to power? (ii) Why do so many studies fail to find a size-dependent decline in mass specific power? (iii) Why are there no studies showing an inverse relationship between size and climbing speed? In the absence of satisfactory answers to these questions, we remain unconvinced that the GH is a good explanation for patterns of sexual size dimorphism in spiders. Below, we counter some of the major points in their rebuttal. First, Moya-Laraño et al. argue that because muscles can activate a variable percentage of their fibres, our assumption that force should be proportional to muscle cross-sectional area is not realistic. However, the assumption that power output limits climbing speed, an assumption shared by both models, implies maximal muscle performance, which requires activation of all muscle fibres. The scaling of maximum force to muscle cross-sectional area arises from the parallel arrangement of muscle fibres and the serial arrangement of sarcomeres, as outlined in any modern physiology textbook (e.g. Randall, Burggren & French 2002, pp. 368–369). Moya-Laraño et al. are aware of this, since they write: ‘the force produced per muscle cross section has been shown to be constant across a wide range of body sizes and animal taxa (Medler 2002)’. Second, they argue that muscle power output should show an inverse relationship with size, as predicted by the GH. Medler's (2002) meta-analysis found that muscle contraction velocity is inversely related to size. Given that power is a product of force and contraction velocity, Moya-Laraño et al. proposed that power output should decline with size. However, both force and velocity change dynamically during the cyclical contractions typical of active locomotor muscles, complicating predictions about the scaling of power output. Importantly, power output is restricted to the period of active muscle contraction (Josephson 1993). As animal size decreases, muscle contraction frequencies increase, and the active contraction phase occupies an ever smaller proportion of the contraction cycle, thereby preventing power output from increasing as size decreases (Schilder & Marden 2004). Regardless of predictive models, empirical studies repeatedly find that, contrary to the GH, mass-specific mechanical power output does not vary with size (Marden 1987; Johnson et al. 1993; Full 1997; Schilder & Marden 2004). Third, Moya-Laraño et al. argue that their model is supported by a recent multi-species study in which climbing speed exhibits a curvilinear relationship with size, with a maximum at 42·5 mg (Foellmer & Moya-Laraño 2007). However, these results are not consistent with the inverse relationship predicted by the GH. Moreover, this analysis included uncontrolled variables likely to influence climbing speed, such as variation in reproductive status, sex, instar and phylogenetic relationships. For example, the heaviest individuals in their sample comprised gravid females, which are likely to be slow climbers due to the weight of eggs they carry. If we accept the suggestion that optimal climbing speed arises at 42·5 mg, then we are left with no explanation for SSD in species in which the females are larger than the optimal climbing size and males are considerably smaller than the optimum, as seen in many high habitat species, (Foellmer & Moya-Laraño 2007). Similarly, in species with females smaller than the optimal climbing size, males should be selected to be larger than females. Such male-biased SSD in spiders is very rare (Foellmer & Moya-Laraño 2007). Finally, the authors suggest that a lack of sufficient variation could account for our failure to detect an inverse relationship between body size and climbing speed. However, this claim ignores the substantial size variation in our two samples: CVbody mass = 32% and 52%, variation that allowed us to detect a significant positive effect of size on horizontal running speed. The GH (Moya-Laraño, Halaj & Wise 2002) is based on an erroneous biomechanical model, runs counter to numerous empirical studies in which mass-specific mechanical power output was found to be independent of size, and its prediction that climbing speed should be inversely related to size has no empirical support. We therefore maintain that selection for vertical climbing speed in males cannot account for patterns of SSD in spiders.

Testing the gravity hypothesis of sexual size dimorphism: are small males faster climbers?

Summary Moya‐Laraño et al. (2002; Evolution 56, 420–425) showed that female‐biased sexual size dimorphism is more pronounced in tree‐dwelling spider species than in species inhabiting lower‐lying substrates. They proposed the Gravity Hypothesis for sexual size dimorphism: small size should be advantageous for males in habitats where successful mate searching requires climbing, because mass‐specific power and hence the speed of climbing against gravity, must decrease with increasing size. Their biomechanical model is based on a false premise, that the cross‐sectional area of a muscle determines its power output. In fact, muscle power is proportional to muscle volume, and hence mass‐specific power should be independent of size. We therefore predict, contrary to the Gravity Hypothesis, that climbing speed should be independent of body size. We tested these contrasting predictions using adult male Western black widow spiders Latrodectus hesperus, a species in which males span a broad range of sizes. In accordance with our prediction, and contrary to the Gravity Hypothesis, we found no relationship between vertical climbing speed and any of a series of size measures, whereas on a horizontal surface, speed was positively related to size. Our results, as well as the error we exposed in the biomechanical model underlying the Gravity Hypothesis, indicate that selection for vertical climbing speed in males cannot account for patterns of sexual size dimorphism in spiders.

SEXUAL SIZE DIMORPHISM AND REPRODUCTIVE INVESTMENT BY FEMALE SPIDERS: A COMPARATIVE ANALYSIS.

We investigate the association between female reproductive investment, absolute size, and sexual size dimorphism in spiders to test the predictions of the fecundity-advantage hypothesis. The relationships between absolute size and sexual size dimorphism and aspects of female reproductive output are examined in comparative analyses using phylogenetically independent contrasts. We provide support for the idea that allometry for sexual dimorphism is the result of variation in female size more so than male size. Regression analyses suggest selection for increased fecundity in females. We argue that fecundity selection provides the only general explanation for the evolution of sexual size dimorphism in spiders.

No association between sexual size dimorphism and life histories in spiders

In spiders, females are commonly larger than males. The majority of hypotheses that attempt to explain sexual size dimorphism in spiders concentrate on reduction in male size, although there is evidence to suggest that the independent evolution of marked sexual size dimorphism and reversion to a less extreme dimorphic state has occurred several times. Recent debate has centred on two conflicting hypotheses involving male dwarfism and increased female size through fecundity selection, and has focused on the golden orb-weaving spider, Nephila clavipes (Tetragnathidae), and its relatives. In Nephila, males are tiny in comparison to females, however, other orb-web spiders do not show such extremes in dimorphism. Here, we incorporate phylogeny into a comparative investigation of the patterns of sexual dimorphism predicted by the hypothesis of male dwarfism via sex-linked differential mortality during mate searching and note an absence of supporting evidence. There was no evidence of the predicted association between male and female size and sexual size dimorphism with life histories, exemplified by variation in predatory strategies, in spiders.

Multivariate morphometrics and sexual dimorphism in the orb-web spider Metellina segmentata (Clerck, 1757) (Araneae, Metidae)

Sexual dimorphism in body size and leg length was investigated in a common orb-weaving spider of Ireland and northern Europe, Metellina segmentata (Clerck, 1757) (Araneae, Metidae). Univariate and multivariate analyses of sexual dimorphism revealed that a greater proportion of between sex variation (sexual dimorphism) was attributable to variation in shape than in size. Significant differences were found in the scores for males and females for the first two principal components. PC1 (shape) accounted for 44.25% of the variation and PC2 (size) 13.01% of the variation. Although M. segmentata has been attributed with minimal sexual size dimorphism, females were markedly heavier, possibly a reflection of differential reproductive investment between the sexes, but males had markedly longer legs and broader prosoma. The results are discussed with regard to existing theories of natural and sexual selection, particularly those concerning sexual cannibalism and differential life history traits in males and females. Models that attempt to explain the evolution of sexual size dimorphism in spiders and of the web builders in particular, fail to account for the multivariate nature of dimorphism, especially with respect to shape.

Multivariate morphometrics and sexual dimorphism in the orb-web spider Metellina segmentata (Clerck, 1757) (Araneae, Metidae)

Sexual dimorphism in body size and leg length was investigated in a common orb-weaving spider of Ireland and northern Europe, Metellina segmentata (Clerck, 1757) (Araneae, Metidae). Univariate and multivariate analyses of sexual dimorphism revealed that a greater proportion of between sex variation (sexual dimorphism) was attributable to variation in shape than in size. Significant differences were found in the scores for males and females for the first two principal components. PC1 (shape) accounted for 44.25% of the variation and PC2 (size) 13.01% of the variation. Although M. segmentata has been attributed with minimal sexual size dimorphism, females were markedly heavier, possibly a reflection of differential reproductive investment between the sexes, but males had markedly longer legs and broader prosoma. The results are discussed with regard to existing theories of natural and sexual selection, particularly those concerning sexual cannibalism and differential life history traits in males and females. Models that attempt to explain the evolution of sexual size dimorphism in spiders and of the web builders in particular, fail to account for the multivariate nature of dimorphism, especially with respect to shape.