Multiple Origins of Eusociality Among Sponge-Dwelling Shrimps (Synalpheus)

Abstract

•As the most extreme expression of apparent altruism in nature, eusociality has long posed a central paradox for behavioral and evolutionary ecology. Because eusociality has arisen rarely among animals, understanding the selective 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 shrimps (Synalpheus) with colony organization ranging from asocial pair-bonding through eusociality. We then used phylogenetically independent contrasts to test whether sociality was associated with evidence of enhanced competitive ability, as suggested by hypotheses invoking an advantage of cooperation in crowded habitats. The molecular, morphological , and combined data each strongly supported three independent origins of monogynous, multigenerational (eusocial) colony organization within this genus. Phylogenetically independent contrasts confirmed that highly social taxa, with strong reproductive skew, have significantly higher relative abundance within the host sponge than do less social taxa, a result that was robust to uncertainty in tree topology and varying models of character change. A similar tendency for highly social species to share their sponge with fewer congener species was suggestive, but not significant. Because unoccupied habitat appears to be limiting for many sponge-dwelling shrimp species, these data are consistent with hypotheses that cooperative social groups enjoy a competitive advantage over less organized groups or individuals, where independent establishment is difficult, and that enemy pressure is of central importance in the evolution of animal sociality.

Eusociality: Origin and consequences

“…Other eusocial species, those outside the Hymenoptera, have descended from species adapted to unusually well protected microhabitats that can be most effectively used and defended by groups. They include green-wood borings (the ambrosia beetle Austroplatypus) (41), plant galls (aphids and thrips) (42,43), and, in the one known example among crustaceans, cavities in sponges (Synalpheus snapping shrimps) (44).…”

Morphological Phylogeny of Alpheid Shrimps: Parallel Preadaptation and the Origin of a Key Morphological Innovation, the Snapping Claw

“…Many alpheids live in permanent symbiosis with other organisms, including sponges, cnidarians, molluscs, echinoderms, other crustaceans, echiurans, and gobiid fishes (Bruce 1976;Karplus 1987;Dworschak et al 2000;Anker et al 2001Marin et al 2005). Many aspects of these associations, such as interspecific communication (Vannini 1985;Karplus 1987), protandric hermaphroditism (Nakashima 1987;Gherardi and Calloni 1993), host protection (Glynn 1983), and eusociality (Duffy et al 2000) make alpheids particularly interesting to field and behavioral biologists.…”

Group Structure and Stability in Social Aggregations of White's Skink,Egernia whitii

“…Goossens et al 1998;Cockburn 2003), to highly social or eusocial colonies (e.g. Jarvis et al 1994;Duffy et al 2000). In particular, social systems involving cohesive and temporally stable social aggregations have arisen independently in many vertebrate taxa.…”