Trine Bilde

The Evolution of Sociality in Spiders

Publisher Summary This chapter discusses the occurrence of group living in spiders. Group living has arisen in spiders in basically two different forms. Cooperative or nonterritorial permanent‐social species are the main focus of the chapter. The form of group living in spiders has been termed “colonial” or “communalterritorial.” Colonial species have been likened to foraging flocks of birds and are described as foraging societies. Social spiders can be viewed as an ideal evolutionary experiment with independent replicates, both within and across several families. The designation of species as nonterritorial permanent‐social and nonterritorial periodic‐social applies to groups of traits that generally occur together. The chapter illustrates that, as this terminology is also somewhat unwieldy, for convenience it revert to the commonly used shorthand designations of social and subsocial, for nonterritorial permanent‐social and territorial periodic‐social, respectively.

Spider genomes provide insight into composition and evolution of venom and silk

Spiders are ecologically important predators with complex venom and extraordinarily tough silk that enables capture of large prey. Here we present the assembled genome of the social velvet spider and a draft assembly of the tarantula genome that represent two major taxonomic groups of spiders. The spider genomes are large with short exons and long introns, reminiscent of mammalian genomes. Phylogenetic analyses place spiders and ticks as sister groups supporting polyphyly of the Acari. Complex sets of venom and silk genes/proteins are identified. We find that venom genes evolved by sequential duplication, and that the toxic effect of venom is most likely activated by proteases present in the venom. The set of silk genes reveals a highly dynamic gene evolution, new types of silk genes and proteins, and a novel use of aciniform silk. These insights create new opportunities for pharmacological applications of venom and biomaterial applications of silk.

THE TRANSITION TO SOCIAL INBRED MATING SYSTEMS IN SPIDERS: ROLE OF INBREEDING TOLERANCE IN A SUBSOCIAL PREDECESSOR

Abstract The social spiders are unusual among cooperatively breeding animals in being highly inbred. In contrast, most other social organisms are outbred owing to inbreeding avoidance mechanisms. The social spiders appear to originate from solitary subsocial ancestors, implying a transition from outbreeding to inbreeding mating systems. Such a transition may be constrained by inbreeding avoidance tactics or fitness loss due to inbreeding depression. We examined whether the mating system of a subsocial spider, in a genus with three social congeners, is likely to facilitate or hinder the transition to inbreeding social systems. Populations of subsocial Stegodyphus lineatus are substructured and spiders occur in patches, which may consist of kin groups. We investigated whether male mating dispersal prevents matings within kin groups in natural populations. Approximately half of the marked males that were recovered made short moves (< 5m) and mated within their natal patch. This potential for inbreeding was counterbalanced by a relatively high proportion of immigrant males. In mating experiments, we tested whether inbreeding actually results in lower offspring fitness. Two levels of inbreeding were tested: full sibling versus non-sib matings and matings of individuals within and between naturally occurring patches of spiders. Neither full siblings nor patch mates were discriminated against as mates. Sibling matings had no effect on direct fitness traits such as fecundity, hatching success, time to hatching and survival of the offspring, but negatively affected offspring growth rates and adult body size of both males and females. Neither direct nor indirect fitness measures differed significantly between within patch and between-patch pairs. We tested the relatedness between patch mates and nonpatch mates using DNA fingerprinting (TE-AFLP). Kinship explained 30% of the genetic variation among patches, confirming that patches are often composed of kin. Overall, we found limited male dispersal, lack of kin discrimination, and tolerance to low levels of inbreeding. These results suggest a history of inbreeding which may reduce the frequency of deleterious recessive alleles in the population and promote the evolution of inbreeding tolerance. It is likely that the lack of inbreeding avoidance in subsocial predecessors has facilitated the transition to regular inbreeding social systems.

Quantifying food limitation of arthropod predators in the field

Abstract A method for quantifying food limitation of arthropod predators in the field is presented and applied to species of ground beetles (Carabidae) and sheet-web spiders (Linyphiidae) from a cereal field. Food limitation is expressed quantitatively as accumulated hunger (=starvation) by transforming 24-h food consumption at 20°C of animals newly collected in the field into days of starvation at 20°C. This is done by means of a reference curve relating 24-h food intake at 20°C to starvation periods (days) at 20°C. Such a reference curve was obtained for the carabid beetle Agonum dorsale in the laboratory. For other species the reference curve was modified with species-specific data. The procedure makes it possible to compare the feeding conditions of different species populations that are part of the same community. Hunger levels in the field for females of A.␣dorsale were equivalent to c. 15 days of starvation in early spring, c. 5 days in June, increasing to c. 10 days in late summer. Two ground beetles occurring during summer also showed increasing hunger levels from June to July, probably the result of a dry summer. Two spider species experienced a hunger level in the range of 4–8 days of starvation.

Kin recognition and cannibalism in a subsocial spider

Evolution of cooperation and group living in spiders from subsocial family groups may be constrained by their cannibalistic nature. A tendency to avoid cannibalizing kin may facilitate tolerance among spiders and implies the ability to identify relatives. We investigated whether the subsocial spider Stegodyphus lineatus discriminates kin by recording cannibalism among juveniles in experiments during which amount of food and size difference among spiders in groups were varied. We hypothesized that family groups should be less cannibalistic than groups of mixed‐parental origin. Further, we tested whether food‐stress would influence cannibalism rates differently in kin and nonkin groups and the effect of relatedness on cannibalism within groups of spiders of variable size compared with those of homogenous size. In groups of six spiders, more spiders were cannibalized in nonsib groups than in sib groups under low food conditions. A tendency for nonkin biased cannibalism in starved spider pairs supported that kin recognition in S. lineatus is expressed when food is limited. Size variance of individuals within well‐fed groups of siblings and unrelated spiders had no influence on cannibalism rates. Apparently, both hunger and high density are important promoters of cannibalism. In addition to inclusive fitness benefits, we suggest that an ability to avoid cannibalizing kin will favour the evolution of cooperation and group living in phylogenetically pre‐adapted solitary species.

The age and evolution of sociality in Stegodyphus spiders: a molecular phylogenetic perspective

Social, cooperative breeding behaviour is rare in spiders and generally characterized by inbreeding, skewed sex ratios and high rates of colony turnover, processes that when combined may reduce genetic variation and lower individual fitness quickly. On these grounds, social spider species have been suggested to be unstable in evolutionary time, and hence sociality a rare phenomenon in spiders. Based on a partial molecular phylogeny of the genus Stegodyphus, we address the hypothesis that social spiders in this genus are evolutionary transient. We estimate the age of the three social species, test whether they represent an ancestral or derived state and assess diversification relative to subsocial congeners. Intraspecific sequence divergence was high in all of the social species, lending no support for the idea that they are young, transient species. The age of the social lineages, constant lineage branching and the likelihood that social species are independently derived suggest that either the social species are ‘caught in sociality’ or they have evolved into cryptic species.

Benefits of cooperation with genetic kin in a subsocial spider

Interaction within groups exploiting a common resource may be prone to cheating by selfish actions that result in disadvantages for all members of the group, including the selfish individuals. Kin selection is one mechanism by which such dilemmas can be resolved This is because selfish acts toward relatives include the cost of lowering indirect fitness benefits that could otherwise be achieved through the propagation of shared genes. Kin selection theory has been proved to be of general importance for the origin of cooperative behaviors, but other driving forces, such as direct fitness benefits, can also promote helping behavior in many cooperatively breeding taxa. Investigating transitional systems is therefore particularly suitable for understanding the influence of kin selection on the initial spread of cooperative behaviors. Here we investigated the role of kinship in cooperative feeding. We used a cross-fostering design to control for genetic relatedness and group membership. Our study animal was the periodic social spider Stegodyphus lineatus, a transitional species that belongs to a genus containing both permanent social and periodic social species. In S. lineatus, the young cooperate in prey capture and feed communally. We provide clear experimental evidence for net benefits of cooperating with kin. Genetic relatedness within groups and not association with familiar individuals directly improved feeding efficiency and growth rates, demonstrating a positive effect of kin cooperation. Hence, in communally feeding spiders, nepotism favors group retention and reduces the conflict between selfish interests and the interests of the group.

Nuptial gifts of male spiders: sensory exploitation of the female's maternal care instinct or foraging motivation?

Nuptial feeding can evolve as sensory traps where the male exploits the females foraging motivation in a sexual context. The nuptial prey gift of the nursery-web spider Pisaura mirabilis is wrapped in white silk, and it has been suggested that males initially exploit the maternal care instinct by producing a nuptial gift that resembles the females eggsac. In mating experiments we examined whether males exploit the females foraging motivation or the females maternal care instinct. We carried out a gift-switching experiment, where males presented an eggsac, a wrapped fly or an unwrapped fly as nuptial gifts. Females fed on eggsacs as well as on prey gifts. Mating success was similar for males with both wrapped and unwrapped gifts, indicating that wrapping per se does not increase male mating success. In a food manipulation experiment, we investigated the effect of the females hunger level on male mating success. Hungry females were more likely to accept a gift and copulate; hence the females hunger state is decisive for male mating success. Our results strongly suggest that the females foraging motivation is the true context for the maintenance of the nuptial gift.

Sexual conflict in the wild : Elevated mating rate reduces female lifetime reproductive success

Sexual conflict over mating rate is suggested to play a pivotal role in male‐female coevolution, and females are predicted to reject superfluous mating attempts. Recent work suggests that direct effects of multiple mating on female fitness are not fully understood. A major concern in studies of sexual conflict is how well the data obtained under controlled laboratory settings relate to natural conditions. We tested the effect of female multiple mating on reproductive success in a natural population of a polyandrous spider, Stegodyphus lineatus. Previous studies show that a male who succeeds in entering a female nest also mates with her; therefore, we used male encounter rate as a proxy of female mating rate. We further elevated female mating rate by introducing males into females’ nests. Female lifetime reproductive success was assessed as the likelihood of successful reproduction, offspring production, and juvenile offspring body mass. Increased mating rate increased the time to oviposition and reduced the likelihood of successful reproduction. Female mating rate negatively affected offspring body mass. Manipulated females produced fewer offspring than control females. The observed patterns imply a net cost of polyandry to females and suggest that natural mating rates can be suboptimal for females under natural conditions.

Individual personalities shape task differentiation in a social spider

Deciphering the mechanisms involved in shaping social structure is key to a deeper understanding of the evolutionary processes leading to sociality. Individual specialization within groups can increase colony efficiency and consequently productivity. Here, we test the hypothesis that within-group variation in individual personalities (i.e. boldness and aggression) can shape task differentiation. The social spider Stegodyphus sarasinorum (Eresidae) showed task differentiation (significant unequal participation) in simulated prey capture events across 10-day behavioural assays in the field, independent of developmental stage (level of maturation), eliminating age polyethism. Participation in prey capture was positively associated with level of boldness but not with aggression. Body size positively correlated with being the first spider to emerge from the colony as a response to prey capture but not with being the first to attack, and dispersal distance from experimental colonies correlated with attacking but not with emerging. This suggests that different behavioural responses to prey capture result from a complex set of individual characteristics. Boldness and aggression correlated positively, but neither was associated with body size, developmental stage or dispersal distance. Hence, we show that personalities shape task differentiation in a social spider independent of age and maturation. Our results suggest that personality measures obtained in solitary, standardized laboratory settings can be reliable predictors of behaviour in a social context in the field. Given the wealth of organisms that show consistent individual behavioural differences, animal personality could play a role in social organization in a diversity of animals.