Multiple origins of eusociality among sponge-dwelling shrimps (Synalpheus)

As the most extreme expression of apparent altruism in nature, eusociality has long posed a central paradox for behavioral and evolutionary ecology. B ecause eusociality has arisen rarely among animals, understanding the selec tive pressures important in early stages of its evolution remains elusive. Employing a historical approach to this problem, we used morphology and DNA sequences to reconstruct the phylogeny of 13 species of sponge-dwelling sh rimps (Synalpheus) with colony organization ranging from asocial pair-bondi ng through eusociality. We then used phylogenetically independent contrasts to test whether sociality was associated with evidence of enhanced competi tive ability, as suggested by hypotheses invoking an advantage of cooperati on in crowded habitats. The molecular, morphological, and combined data eac h strongly supported three independent origins of monogynous, multigenerati onal (eusocial) colony organization within this genus. Phylogenetically ind ependent contrasts confirmed that highly social taxa, with strong reproduct ive skew, have significantly higher relative abundance within the host spon ge than do less social taxa, a result that was robust to uncertainty in tre e topology and varying models of character change. A similar tendency for h ighly social species to share their sponge with fewer congener species was suggestive, but not significant. Because unoccupied habitat appears to be l imiting for many sponge-dwelling shrimp species, these data are consistent with hypotheses that cooperative social groups enjoy a competitive advantag e over less organized groups or individuals, where independent establishmen t is difficult, and that enemy pressure is of central importance in the evo lution of animal sociality.