Alpheid shrimp represent an abundant and diverse, but poorly characterized, component of the cryptic biodiversity of coral reefs worldwide. Sponge-inhabiting alpheids provide a promising model system for exploring patterns of cryptic reef biodiversity because their habitats (hosts) are discrete and qualitatively distinct units. We tabulated data from 14 years of collections at Carrie Bow Cay, Belize to quantify patterns of diversity, host specificity, and dominance among spongedwelling shrimp ( Synalpheus ), with special attention to eusocial species. From > 600 sampled sponges of 17 species, we recognized at least 36 Synalpheus shrimp species. Of these, 15 (42%) were new to science. Species accumulation curves suggest that we have sampled most of the Synalpheus diversity at Carrie Bow Cay. Diversity of sponge-dwelling Synalpheus was slightly higher in shallow water, probably because of greater habitat diversity, than in deep water. Host specificity was surprisingly high, with > 50% of all shrimp species found in only a single sponge species each, although some shrimp species used as many as six hosts. Cohabitation of individual sponges by multiple shrimp species was rarer than expected by chance, supporting previous distributional and behavioural evidence that competition for hosts is strong and moulds patterns of host association. The fauna of most well-sampled sponge species was dominated, both in numbers of individuals and in frequency of occurrence, by eusocial species. Eusocial shrimp species also inhabited a significantly greater number of sponge species than did non-social shrimp. Consequently, > 65% of shrimp in our quantitative samples belonged to the four eusocial species, and on a per-species basis, eusocial species were 17 times as abundant as non-social species. Our data suggest that the highly diverse sponge-dwelling shrimp assemblage of the Belize Barrier Reef is structured by competition, and that eusociality has allowed a small number of species to dominate the sponge resource.
We review the taxonomy of sponge-dwelling shrimp in the “Gambarelloides species group” within the genus Synalpheus Bate 1888, an informal but widely recognized group that is largely endemic to the western Atlantic and contains the majority of Synalpheus species in that region. The validity of most species described from the western Atlantic is reevaluated based on extensive new material from Carrie Bow Cay, Belize, and on examination of types of most described species. Twenty-eight species, including all those historically considered as part of the Gambarelloides group, are herein removed from Synalpheus and transferred to Zuzalpheus, n. gen., which is diagnosed by two synapomorphies: the dense brush of curved setae on the minor first pereopod, and the mesial lamellae on the coxae of the 3 rd pereopods. Six new species are described (Zuzalpheus dardeaui, Z. elizabethae, Z. idios, Z. kensleyi, Z. ul, Z. yano) and Z. osburni (Schmitt 1933) n. comb. is removed from synonymy with Synalpheus goodei. An identification key to all 34 species of West Atlantic Zuzalpheus is presented, as are known host associations, and color plates of most species.
•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.
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