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Evolutionary transitions towards eusociality in snapping shrimps

Abstract

Animal social organization varies from complex societies where reproduction is dominated by a single individual (eusociality) to those where reproduction is more evenly distributed among group members (communal breeding). Yet, how simple groups transition evolutionarily to more complex societies remains unclear. Competing hypotheses suggest that eusociality and communal breeding are alternative evolutionary endpoints, or that communal breeding is an intermediate stage in the transition towards eusociality. We tested these alternative hypotheses in sponge-dwelling shrimps, Synalpheus spp. Although species varied continuously in reproductive skew, they clustered into pair-forming, communal and eusocial categories based on several demographic traits. Evolutionary transition models suggested that eusocial and communal species are discrete evolutionary endpoints that evolved independently from pair-forming ancestors along alternative paths. This ‘family-centred’ origin of eusociality parallels observations in insects and vertebrates, reinforcing the role of kin selection in the evolution of eusociality and suggesting a general model of animal social evolution.

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Figure 1: Demographic classification of social states in Synalpheus shrimp.
Figure 2: Demographic properties of pair-forming, communal and eusocial species.
Figure 3: Comparison of three models of continuous social trait evolution among pair-forming (P), communal (C) and eusocial (E) species.
Figure 4: Phylogeny of social evolution in Synalpheus.

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Acknowledgements

We thank K. W. Leong, K. MacDonald III, C. L. Morrison, E. Tóth, J. Kealey, S. Bornbusch, M. Chang, and D. Hall for assisting in field collection. S.T.C.C. was funded by the Smithsonian Tropical Research Institute Short-Term Fellowship Program. J.E.D. and S.T.C.C. were funded by the US National Science Foundation to J.E.D. (DEB 92-01566, DEB 98–15785, IBN-0131931, IOS-1121716). K.M.H. was supported by the National Geographic Society (Research and Exploration Grant no. 8312- 07) and by the Murdock Charitable Trust. D.R.R. was supported by the US National Science Foundation (IOS-1121435, IOS-1257530, IOS-1439985). This work benefited substantially from the Smithsonian Institution’s Caribbean Coral Reef Ecosystem Program and is CCRE contribution no. 994. This Article is contribution 3610 of the Virginia Institute of Marine Science, College of William and Mary.

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S.T.C.C., J.E.D., K.M.H. and D.R.R. collected field samples. S.T.C.C. carried out the statistical analyses and drafted the manuscript; S.T.C.C., J.E.D., K.M.H. and D.R.R. conceived of the study, designed the study, coordinated the study and helped draft the manuscript. All authors gave final approval for publication.

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Correspondence to Solomon Tin Chi Chak.

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Supplementary Methods; Supplementary Figure 1; Supplementary Tables 1–9. (PDF 357 kb)

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Chak, S., Duffy, J., Hultgren, K. et al. Evolutionary transitions towards eusociality in snapping shrimps. Nat Ecol Evol 1, 0096 (2017). https://doi.org/10.1038/s41559-017-0096

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