Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Evolutionary transitions towards eusociality in snapping shrimps


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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

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.


  1. 1

    Rubenstein, D. R. & Abbot, P. Comparative Social Evolution (Cambridge Univ. Press, 2017).

    Book  Google Scholar 

  2. 2

    Duffy, J. E. & Thiel, M. Evolutionary Ecology of Social and Sexual Systems (Oxford Univ. Press, 2007).

    Book  Google Scholar 

  3. 3

    Brown, J. L. Avian communal breeding systems. Annu. Rev. Ecol. Syst. 9, 123–155 (1978).

    Article  Google Scholar 

  4. 4

    Solomon, N. G. & French, J. A. Cooperative Breeding in Mammals (Cambridge Univ. Press, 1997).

    Google Scholar 

  5. 5

    Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W. & Struhsaker, T. T. Primate Societies. (Univ. Chicago Press, 1987).

    Google Scholar 

  6. 6

    Wilson, E. O. Sociobiology. The New Synthesis (Harvard Univ. Press, 1975).

    Google Scholar 

  7. 7

    Vehrencamp, S. L. in Social Behavior and Communication (eds Marler, P. & Vandenbergh, J. G. ) 351–394 (Springer, 1979).

    Book  Google Scholar 

  8. 8

    Sherman, P. W., Lacey, E. A., Reeve, H. K. & Keller, L. The eusociality continuum. Behav. Ecol. 6, 102–108 (1995).

    Article  Google Scholar 

  9. 9

    Lacey, E. A. & Sherman, P. W. Redefining eusociality: concepts, goals and levels of analysis. Ann. Zool. Fenn. 42, 573–577 (2005).

    Google Scholar 

  10. 10

    Rubenstein, D. R., Botero, C. A. & Lacey, E. A. Discrete but variable structure of animal societies leads to the false perception of a social continuum. R. Soc. Open Sci. 3, 160147 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  11. 11

    Duffy, J. E. & Macdonald, K. S. Kin structure, ecology and the evolution of social organization in shrimp: a comparative analysis. Proc. Biol. Sci. 277, 575–584 (2010).

    Article  PubMed  Google Scholar 

  12. 12

    Batra, S. Nests and social behavior of halictine bees of India. Indian J. Entomol. 28, 375–393 (1966).

    Google Scholar 

  13. 13

    Wcislo, W. T. & Tierney, S. M. in Organization of Insect Societies from Genome to Sociocomplexity (eds Gadau, J. & Fewell, J. ) 148–169 (Harvard Univ. Press, 2009).

    Google Scholar 

  14. 14

    Michener, C. D. Comparative social behavior of bees. Annu. Rev. Entomol. 14, 299–342 (1969).

    Article  Google Scholar 

  15. 15

    Boomsma, J. J. Lifetime monogamy and the evolution of eusociality. Phil. Trans. R. Soc. Lond. B 364, 3191–3207 (2009).

    Article  Google Scholar 

  16. 16

    Emlen, S. An evolutionary theory of the family. Proc. Natl Acad. Sci. USA 92, 8092–8099 (1995).

    CAS  Article  PubMed  Google Scholar 

  17. 17

    Boomsma, J. J. et al. Only full-sibling families evolved eusociality. Nature 471, E4–E5 (2011).

    CAS  Article  PubMed  Google Scholar 

  18. 18

    Michener, C. D. The Social Behavior of the Bees. A Comparative Study (Harvard Univ. Press, 1974).

    Google Scholar 

  19. 19

    Bourke, A. F. G. The validity and value of inclusive fitness theory. Proc. R. Soc. B 278, 3313–3320 (2011).

    Article  PubMed  Google Scholar 

  20. 20

    Liao, X., Rong, S. & Queller, D. C. Relatedness, conflict, and the evolution of eusociality. PLoS Biol. 13, e1002098 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  21. 21

    Costa, J. T. & Fitzgerald, T. D. Social terminology revisited: where are we ten years later? Ann. Zool. Fennici 42, 559–564 (2005).

    Google Scholar 

  22. 22

    Crespi, B. J. & Yanega, D. The definition of eusociality. Behav. Ecol. 6, 109–115 (1995).

    Article  Google Scholar 

  23. 23

    Danforth, B. N. Evolution of sociality in a primitively eusocial lineage of bees. Proc. Natl Acad. Sci. USA 99, 286–290 (2002).

    CAS  Article  PubMed  Google Scholar 

  24. 24

    Hines, H. M., Hunt, J. H., O’Connor, T. K., Gillespie, J. J. & Cameron, S. A. Multigene phylogeny reveals eusociality evolved twice in vespid wasps. Proc. Natl Acad. Sci. USA 104, 3295–3299 (2007).

    CAS  Article  PubMed  Google Scholar 

  25. 25

    Barden, P. & Grimaldi, D. A. Adaptive radiation in socially advanced stem-group ants from the Cretaceous. Curr. Biol. 26, 515–521 (2016).

    CAS  Article  PubMed  Google Scholar 

  26. 26

    Thorne, B. L. Evolution of eusociality in termites. Annu. Rev. Ecol. Syst. 28, 27–54 (1997).

    Article  Google Scholar 

  27. 27

    Cardinal, S. & Danforth, B. N. The antiquity and evolutionary history of social behavior in bees. PLoS ONE 6, e21086 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. 28

    Tierney, S., Smith, J., Chenoweth, L. & Schwarz, M. Phylogenetics of allodapine bees: a review of social evolution, parasitism and biogeography. Apidologie 39, 3–15 (2008).

    Article  Google Scholar 

  29. 29

    Schwarz, M. P., Richards, M. H. & Danforth, B. N. Changing paradigms in insect social evolution: insights from Halictine and Allodapine bees. Annu. Rev. Entomol. 52, 127–150 (2007).

    CAS  Article  PubMed  Google Scholar 

  30. 30

    Hughes, W. O. H., Oldroyd, B. P., Beekman, M. & Ratnieks, F. L. W. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213–1216 (2008).

    CAS  Article  PubMed  Google Scholar 

  31. 31

    Hultgren, K. M., Duffy, J. E. & Rubenstein, D. R. in Comparative Social Evolution (eds Rubenstein, D. R. & Abbot, P. ) 224–249 (Cambridge Univ. Press, 2017).

    Book  Google Scholar 

  32. 32

    Macdonald, K. S., Ríos, R. & Duffy, J. E. Biodiversity, host specificity, and dominance by eusocial species among sponge-dwelling alpheid shrimp on the Belize Barrier Reef. Divers. Distrib. 12, 165–178 (2006).

    Article  Google Scholar 

  33. 33

    Knowlton, N. Sexual selection and dimorphism in two demes of a symbiotic, pair-bonding snapping shrimp. Evolution 34, 161–173 (1980).

    Article  PubMed  Google Scholar 

  34. 34

    Chak, S. T. C., Duffy, J. E. & Rubenstein, D. R. Reproductive skew drives patterns of sexual dimorphism in sponge-dwelling snapping shrimps. Proc. R. Soc. B 282, 20150342 (2015).

    Article  PubMed  Google Scholar 

  35. 35

    Duffy, J. E. Eusociality in a coral-reef shrimp. Nature 381, 512–514 (1996).

    CAS  Article  Google Scholar 

  36. 36

    Chak, S. T. C., Rubenstein, D. R. & Duffy, J. E. Social control of reproduction and breeding monopolization in the eusocial snapping shrimp Synalpheus elizabethae. Am. Nat. 186, 660–668 (2015).

    Article  PubMed  Google Scholar 

  37. 37

    Duffy, J. E. in Genes, Behavior, and Evolution in Social Insects (eds Kikuchi, T., Azuma, N. & Higashi, S. ) 1–38 (Hokkaido Univ. Press, 2003).

    Google Scholar 

  38. 38

    Keller, L. & Perrin, N. Quantifying the level of eusociality. Proc. R. Soc. B 260, 311–315 (1995).

    Article  Google Scholar 

  39. 39

    Hultgren, K. M. & Duffy, J. E. Phylogenetic community ecology and the role of social dominance in sponge-dwelling shrimp. Ecol. Lett. 15, 704–713 (2012).

    Article  PubMed  Google Scholar 

  40. 40

    Agnarsson, I., Avilés, L., Coddington, J. A., Maddison, W. P. & Funk, D. Sociality in Theridiid spiders: repeated origins of an evolutionary dead end. Evolution 60, 2342–2351 (2006).

    Article  PubMed  Google Scholar 

  41. 41

    Cornwallis, C. K., West, S. A., Davis, K. E. & Griffin, A. S. Promiscuity and the evolutionary transition to complex societies. Nature 466, 969–972 (2010).

    CAS  Article  PubMed  Google Scholar 

  42. 42

    Lacey, E. A. & Sherman, P. W. in Cooperative Breeding in Mammals (eds Solomon, N. G. & French, J. A. ) 267–301 (Cambridge Univ. Press, 1997).

    Google Scholar 

  43. 43

    Ríos, R. & Duffy, J. E. A review of the sponge-dwelling snapping shrimp from Carrie Bow Cay, Belize, with description of Zuzalpheus, new genus, and six new species (Crustacea: Decapoda: Alpheidae). Zootaxa 1602, 1–89 (2007).

    Article  Google Scholar 

  44. 44

    Hultgren, K. M., Hurt, C. & Anker, A. Phylogenetic relationships within the snapping shrimp genus Synalpheus (Decapoda: Alpheidae). Mol. Phylogen. Evol. 77, 116–125 (2014).

    Article  Google Scholar 

  45. 45

    Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540–552 (2000).

    CAS  Article  PubMed  Google Scholar 

  46. 46

    Nylander, J. MrModeltest v2 (Evolutionary Biology Centre, Uppsala Univ., 2004).

  47. 47

    Morrison, C. L., Ríos, R. & Duffy, J. E. Phylogenetic evidence for an ancient rapid radiation of Caribbean sponge-dwelling snapping shrimps (Synalpheus). Mol. Phylogenet. Evol. 30, 563–581 (2004).

    CAS  Article  PubMed  Google Scholar 

  48. 48

    Hultgren, K. M. & Duffy, J. E. Multi-locus phylogeny of sponge-dwelling snapping shrimp (Caridea: Alpheidae: Synalpheus) supports morphology-based species concepts. J. Crust. Biol. 31, 352–360 (2011).

    Article  Google Scholar 

  49. 49

    Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  50. 50

    Wiens, J. J. Missing data and the design of phylogenetic analyses. J. Biomed. Inf. 39, 34–42 (2006).

    CAS  Article  Google Scholar 

  51. 51

    Sanderson, M. J. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol. 19, 101–109 (2002).

    CAS  Article  PubMed  Google Scholar 

  52. 52

    Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

    Google Scholar 

  53. 53

    Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).

    Article  Google Scholar 

  54. 54

    Reynolds, A. P., Richards, G., de la Iglesia, B. & Rayward-Smith, V. J. Clustering rules: a comparison of partitioning and hierarchical clustering algorithms. J. Math. Model. Algor. 5, 475–504 (2006).

    Article  Google Scholar 

  55. 55

    Maechler, M., Rousseeuw, P., Struyf, A., Hubert, M. & Hornik, K. Cluster: cluster analysis basics and extensions. R package version 2.0.2 (2015).

  56. 56

    Kaufman, L. & Rousseeuw, P. J. Finding Groups in Data: An Introduction to Cluster Analysis (Wiley, 1999).

    Google Scholar 

  57. 57

    Breiman, L., Friedman, J., Stone, C. & Olshen, R. A. Classification and Regression Trees (CRC, 1984).

    Google Scholar 

  58. 58

    Therneau, T., Atkinson, B. & Ripley, B. rpart: Recursive partitioning and regression trees. R package version 4.1–9 (2015).

    Google Scholar 

  59. 59

    Spiegelhalter, D. J., Best, N. G., Carlin, B. P. & Van Der Linde, A. Bayesian measures of model complexity and fit. J. Roy. Stat. Soc. Ser. B. 64, 583–639 (2002).

    Article  Google Scholar 

  60. 60

    Pennell, M. W. et al. Geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees. Bioinformatics 30, 2216–2218 (2014).

    CAS  Article  PubMed  Google Scholar 

  61. 61

    Garamszegi, L. Z. Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology (Springer, 2014).

    Book  Google Scholar 

  62. 62

    Akaike, H. in Selected Papers of Hirotugu Akaike (eds Parzen, E., Tanabe, K. & Kitagawa, G. ) 199–213 (Springer, 1998).

    Book  Google Scholar 

Download references


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.

Author information




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.

Corresponding author

Correspondence to Solomon Tin Chi Chak.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Chak, S., Duffy, J., Hultgren, K. et al. Evolutionary transitions towards eusociality in snapping shrimps. Nat Ecol Evol 1, 0096 (2017).

Download citation

Further reading


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing