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Dryad

Impaired immune function accompanies social evolution in spiders

Abstract

An efficient immune system is essential to the survival of many animals. Sociality increases risk of pathogen transmission, which should select for enhanced immune function. However, two hypotheses instead predict a weakened immune function: relaxed selection caused by social immunity/protection, and reduced efficacy of selection due to inbreeding, reproductive skew, and female bias in social species that reduces effective population size and accelerate genetic drift. We assessed the effect of social evolution on immune function in a comparative study of two social spider species and their closely related subsocial sister species (genus Stegodyphus). The haemolymph of social species was less efficient in inhibiting the growth of potentially pathogenic bacteria than that of subsocial species. Reduced efficacy of selection in social species was supported by comparative genomic analysis of immune genes showing substantially elevated non-synonymous substitutions in one of the social species. We propose that this impaired immune function is likely to be a result of reduced efficacy of selection because the evolution of sociality in spiders is accompanied by demographic processes that elevate genetic drift. There may also be positive feedback between pathogen-induced local extinctions and the resulting elevation of genetic drift which further weakens responses to selection by pathogens.