Matthias W. Foellmer

Proximate Causes of Rensch’s Rule: Does Sexual Size Dimorphism in Arthropods Result from Sex Differences in Development Time?

A prominent interspecific pattern of sexual size dimorphism (SSD) is Rensch’s rule, according to which male body size is more variable or evolutionarily divergent than female body size. Assuming equal growth rates of males and females, SSD would be entirely mediated, and Rensch’s rule proximately caused, by sexual differences in development times, or sexual bimaturism (SBM), with the larger sex developing for a proportionately longer time. Only a subset of the seven arthropod groups investigated in this study exhibits Rensch’s rule. Furthermore, we found only a weak positive relationship between SSD and SBM overall, suggesting that growth rate differences between the sexes are more important than development time differences in proximately mediating SSD in a wide but by no means comprehensive range of arthropod taxa. Except when protandry is of selective advantage (as in many butterflies, Hymenoptera, and spiders), male development time was equal to (in water striders and beetles) or even longer than (in drosophilid and sepsid flies) that of females. Because all taxa show female‐biased SSD, this implies faster growth of females in general, a pattern markedly different from that of primates and birds (analyzed here for comparison). We discuss three potential explanations for this pattern based on life‐history trade‐offs and sexual selection.

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.

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 females 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.

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.

Does personality explain variation in the probability of sexual cannibalism in the orb-web spider Argiope aurantia?

Sexual cannibalism is often hypothesized to be an extreme manifestation of sexual conflict, yet we still lack a good understanding of the underlying motivation in most species. Hypotheses for the ultimate causes of sexual cannibalism either invoke the behavior as adaptive or mal-adaptive. Adaptive hypotheses consider foraging decisions, mate choice or genetic bet-hedging. Mal-adaptive hypotheses propose that sexual cannibalism is the result of mistaken species identity or the by-product of an aggression syndrome. Here, we test the latter hypothesis, that sexual cannibalism is the result of an aggression syndrome. This hypothesis states that aggressive behavior is favored in the foraging context because females benefit from achieving a large size quickly through an increase in fecundity, and it predicts that individuals that are aggressive foragers are more likely to attack a male and hence are at risk of receiving no or insufficient quantities of sperm. Few tests of this hypothesis are available to date, and only one involved a species with sexual cannibalism occurring after at least some sperm transfer. We test the hypothesis in Argiope aurantia, a species in which females frequently attack males during copulation. We estimated aggressiveness in the foraging context in penultimate and adults females and staged matings using the same females to evaluate whether aggressiveness during the foraging context predicts the likelihood of sexual cannibalism. Indeed, we find that aggressive foragers are more likely to attack their mates, but we conclude that other, possibly adaptive reasons for cannibalism exist as much of the uncertainty in cannibalism occurrence remained unexplained.

Longer Antennae for Romeo: Assessing Effect of Antennae Length on Courtship and Mating Success in Male Crickets, Acheta domesticus (Orthoptera, Gryllidae)

Animals use a variety of chemosensory functions to coordinate behavioral actions, such as sexual recognition and courtship. In particular, many insects use antennae as a vital chemosensory organ to transmit and receive sexual signals that are believed to be crucial in mate recognition and mating in various species of insects. Crickets provide a usable model to test the significance of antennae in insects. The general importance of antennae in male crickets to initiate courtship, ensure copulation, and post-copulatory mate guarding has been documented in studies that performed full antennectomy. Our study is the first to perform partial antennectomy to test the hypothesis that even partial loss due to injury has negative effects on sexual behaviors. We found that partially antennectomized males are not slower than control males in mate recognition and courtship initiation. However, we found that partially antennectomized males take longer to achieve copulation than control males with normal uncut antennae. Our results suggest that male crickets require long, undamaged antennae to efficiently engage in mating behavior and may already incur fitness costs when they lose half of their antennae.

Male mate choice based on chemical cues in the cricket Acheta domesticus (Orthoptera: Gryllidae)

1. Males in many animal species exercise mate choice to maximise their reproductive success, assessing females by characteristics related to reproductive potential, such as mating status, body size, and age. The sensory modalities involved in mate choice are often not firmly demonstrated, but only inferred. This is especially true for chemical cues and signals.

One size fits all? Determinants of sperm transfer in a highly dimorphic orb-web spider.

The evolutionary significance of widespread hypo‐allometric scaling of genital traits in combination with rapid interspecific genital trait divergence has been of key interest to evolutionary biologists for many years and remains poorly understood. Here, we provide a detailed assessment of quantitative genital trait variation in males and females of the sexually highly dimorphic and cannibalistic orb‐weaving spider Argiope aurantia. We then test how this trait variation relates to sperm transfer success. In particular, we test specific predictions of the one‐size‐fits‐all and lock‐and‐key hypotheses for the evolution of genital characters. We use video‐taped staged matings in a controlled environment with subsequent morphological microdissections and sperm count analyses. We find little support for the prediction of the one‐size‐fits‐all hypothesis for the evolution of hypo‐allometric scaling of genital traits, namely that intermediate trait dimensions confer highest sperm transfer success. Likewise, our findings do not support the prediction of the lock‐and‐key hypothesis that a tight fit of male and female genital traits mediates highest sperm transfer success. We do, however, detect directional effects of a number of male and female genital characters on sperm transfer, suggesting that genital trait dimensions are commonly under selection in nature. Importantly, even though females are much larger than males, spermatheca size limits the number of sperm transferred, contradicting a previous hypothesis about the evolutionary consequences of genital size dimorphism in extremely size‐dimorphic taxa. We also find strong positive effects of male body size and copulation duration on the probability of sperm transfer and the number of sperm transferred, with implications for the evolution of extreme sexual size dimorphism and sexual cannibalism in orb weavers.

Sex-Specific Foraging Behaviours and Growth Rates in Juveniles Contribute to the Development of Extreme Sexual Size Dimorphism in a Spider~!2010-03-14~!2010-05-31~!2010-08-13~!

Extreme sexual size dimorphism (SSD) in temperate species is expected to be proximally caused, at least partially, by sex-specific growth rates due to the limited time available for growth and reproduction. Hence sex-specific foraging strategies are predicted to mediate differential growth rates. However, little is known about how sex differences in foraging behaviour and growth trajectories relate to the expression of pronounced SSD. Here we tested for sex-specific foraging strategies and growth rates in juveniles of the highly size dimorphic orb-web spider Argiope aurantia under natural conditions. In a number of web sites, we estimated web height, web size (size of the prey capture area), mesh size, stabilimentum (web decoration) size and length, vegetation density and prey availability. Over four days in the field we also measured spider growth and web site tenacity. Independently of body size, females exhibited faster growth rate than males. When body size and condition were controlled for, we found that females built larger webs, and at sites with greater prey availability compared to males. Males built webs with significantly larger and longer stabilimenta independent of web size. These results indicate that extreme female-biased SSD in A. aurantia is at least partially the result of sex-specific growth rates already in early juvenile stages mediated by sex-specific web design and placement to allow for greater foraging success of females compared to males. We discuss these findings in the context of SSD evolution, and consider whether the sex-specific behaviours detected are more likely consequences or causes of the evolution of extreme SSD.