Virginia Settepani

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.

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.

Phylogenetic analysis suggests that sociality is associated with reduced effectiveness of selection

Abstract The evolution of sociality in spiders is associated with female bias, reproductive skew and an inbreeding mating system, factors that cause a reduction in effective population size and increase effects of genetic drift. These factors act to decrease the effectiveness of selection, thereby increasing the fixation probability of deleterious mutations. Comparative studies of closely related species with contrasting social traits and mating systems provide the opportunity to test consequences of low effective population size on the effectiveness of selection empirically. We used phylogenetic analyses of three inbred social spider species and seven outcrossing subsocial species of the genus Stegodyphus, and compared dN/dS ratios and codon usage bias between social Inbreeding and subsocial outcrossing mating systems to assess the effectiveness of selection. The overall results do not differ significantly between the social inbreeding and outcrossing species, but suggest a tendency for lower codon usage bias and higher dN/dS ratios in the social inbreeding species compared with their outcrossing congeners. The differences in dN/dS ratio and codon usage bias between social and subsocial species are modest but consistent with theoretical expectations of reduced effectiveness of selection in species with relatively low effective population size. The modest differences are consistent with relatively recent evolution of social mating systems. Additionally, the short terminal branches and lack of speciation of the social lineages, together with low genetic diversity lend support for the transient state of permanent sociality in spiders.

Evolution of sociality in spiders leads to depleted genomic diversity at both population and species levels

Across several animal taxa, the evolution of sociality involves a suite of characteristics, a “social syndrome,” that includes cooperative breeding, reproductive skew, primary female‐biased sex ratio, and the transition from outcrossing to inbreeding mating system, factors that are expected to reduce effective population size (Ne). This social syndrome may be favoured by short‐term benefits but come with long‐term costs, because the reduction in Ne amplifies loss of genetic diversity by genetic drift, ultimately restricting the potential of populations to respond to environmental change. To investigate the consequences of this social life form on genetic diversity, we used a comparative RAD‐sequencing approach to estimate genomewide diversity in spider species that differ in level of sociality, reproductive skew and mating system. We analysed multiple populations of three independent sister‐species pairs of social inbreeding and subsocial outcrossing Stegodyphus spiders, and a subsocial outgroup. Heterozygosity and within‐population diversity were sixfold to 10‐fold lower in social compared to subsocial species, and demographic modelling revealed a tenfold reduction in Ne of social populations. Species‐wide genetic diversity depends on population divergence and the viability of genetic lineages. Population genomic patterns were consistent with high lineage turnover, which homogenizes the genetic structure that builds up between inbreeding populations, ultimately depleting genetic diversity at the species level. Indeed, species‐wide genetic diversity of social species was 5–8 times lower than that of subsocial species. The repeated evolution of species with this social syndrome is associated with severe loss of genomewide diversity, likely to limit their evolutionary potential.

Evidence for loss of nepotism in the evolution of permanent sociality.

Kin selected benefits of cooperation result in pronounced kin discrimination and nepotism in many social species and favour the evolution of sociality. However, low variability in relatedness among group members, infrequent competitive interactions with non-relatives, and direct benefits of cooperation may relax selection for nepotism. We tested this prediction in a permanently social spider, Stegodyphus dumicola that appears to fulfil these conditions. Sociality is a derived trait, and kin discrimination exists in sub-social closely related congeners and is likely a selective force in the sub-social route to permanent sociality in spiders. We examined whether social spiders show nepotism in cooperative feeding when genetic relatedness among group members was experimentally varied. We found no effect of relatedness on feeding efficiency, growth rate or participation in feeding events. Previous studies on sub-social species showed benefits of communal feeding with kin, indicating nepotistic cooperation. The lack of evidence for nepotism in the social species suggests that kin discrimination has been lost or is irrelevant in communal feeding. Our results are consistent with the hypothesis that the role of nepotism is diminished when cooperation evolves in certain genetic and ecological contexts, e.g. when intra-group genetic relatedness is homogeneous and encounters with competitors are rare.

Temporarily social spiders do not show personality-based task differentiation

Task differentiation in cooperative groups can arise through a wide range of mechanisms. A recent hypothesis, supported by empirical studies of social spiders, suggests that a variation in individual personalities might be one such mechanism. Personality-based task differentiation can either arise as an emergent property of group living based on inherent behavioural variation among individuals, or alternatively it could be an adaptation to permanent sociality favoured by individual fitness benefits arising from increased group efficiency and productivity. We tested whether personality-based task differentiation is present in the temporarily social spider Stegodyphus tentoriicola which represents the ancestral state from which permanent sociality in spiders has evolved. This species is closely related to the permanently social Stegodyphus sarasinorum in which personality-based task differentiation has been documented. We measured individual boldness and investigated individual participation in simulated prey capture events twice per day on 5 consecutive days. We found no evidence for personality-based task differentiation: S. tentoriicola spiders did not exhibit consistent personalities in boldness or consistent task differentiation in prey attack. Our results lend support for the hypothesis that personality-based task differentiation is an adaptation to permanently social living in spiders as their ancestral representative lacks this trait.