Biological Theory

, Volume 7, Issue 3, pp 204–210 | Cite as

Why are There No Eusocial Fishes?

  • Klaus M. Stiefel
Long Article


Eusociality is the form of animal social organization with a reproductive division of labor, most prominently known from ants and bees. Here I ask the question why this enormously successful form of social organization is missing in the largest and most diverse group of vertebrates, the teleost fishes. I first briefly review the phylogenetic distribution and likely evolutionary origins of eusociality. Then, after an equally very brief review of the diverse life history strategies of teleosts, I conclude that it is not the lack of evolutionary pre-adaptations which is keeping teleosts from becoming eusocial. Rather, I argue, that the absence of eusocial fish is caused by a number of differences between aquatic (chiefly marine) and terrestrial ecosystems: (1) Greater offspring dispersal in aquatic ecosystems reduces the role of kin-selection. (2) Lesser predictability of the environment at larger timescales in marine ecosystems disfavors eusociality. (3) A briefer impact of resource pulses in aquatic ecosystems will cause less evolutionary pressure towards cooperation, and eventually eusociality. Finally, I conclude by predicting that the most likely places to find eusocial fishes will be the deep-water regions of the ocean and the African rift lakes.


Eusociality Evolution Fish Teleost 



I thank Drs. Robert R. Warner and Sasha Mikheyev for helpful discussion and the reviewers of the first version of this manuscript for valuable input and pointers to relevant literature.


  1. Alexander RD, Noonan KM, Crespi B (1991) The evolution of eusociality. In: Sherman PW, Jarvis J, Alexander RD (eds) The Biology of the naked mole rat. Princeton University Press, PrincetonGoogle Scholar
  2. Bergmüller R, Johnstone RA, Russell AF, Bshary R (2007) Integrating cooperative breeding into theoretical concepts of cooperation. Behav Processes 76:61–72Google Scholar
  3. Boomsma JJ (2007) Kin selection versus sexual selection: why the ends do not meet. Current Biol 17(16):R673–R683Google Scholar
  4. Boomsma JJ, Beekman M, Cornwallis CK, Griffin AS, Holman L, Hughes WO, Keller L, Oldroyd BP, Ratnieks FL (2011) Only full-sibling families evolved eusociality. Nature 471(7339):E4–E5Google Scholar
  5. Bourke AFG (2011) Principles of Social Evolution, 1st edn. Oxford University Press, USAGoogle Scholar
  6. Brown GE, Brown JA (1996) Kin discrimination in salmonids. Rev Fish Biol Fisheries 6(2):201–219CrossRefGoogle Scholar
  7. Bruintjes R, Taborsky M (2011) Size-dependent task specialization in a cooperative cichlid in response to experimental variation of demand. Anim Behav 81(2):387–394CrossRefGoogle Scholar
  8. Burland TM, Bennett NC, Jarvis JUM, Faulkes CG (2002) Eusociality in African Mole-rats: new insights from patterns of genetic relatedness in the Damaraland mole-rat (Cryptomys Damarensis). Proceedings of the Royal Society of London. Series B: biological sciences, 269(1495):1025–1030, 22 May 2002Google Scholar
  9. Carr Mark H, Neigel JE, Estes JA, Andelman S, Warner RR, Largier JL (2003) Comparing marine and terrestrial ecosystems: implications for the design of coastal marine reserves. Ecol Appl 13(1):S90–S107CrossRefGoogle Scholar
  10. Crespi BJ (1994) Three conditions for the evolution of eusociality: are they sufficient? Insectes Soc 41(4):395–400CrossRefGoogle Scholar
  11. Crow KD, Stadler PF, Lynch VJ, Amemiya C, Wagner GP (2006) The “fish-specific” hox cluster duplication is coincident with the origin of teleosts. Mol Biol Evol 23(1):121–136CrossRefGoogle Scholar
  12. Crozier RH (2008) Advanced eusociality, kin selection and male haploidy. Aust J Entomology 47(1):2–8CrossRefGoogle Scholar
  13. Duffy JE (1996) Eusociality in a coral-reef shrimp. Nature 381(6582):512–514CrossRefGoogle Scholar
  14. Duffy JE (2002) The ecology and evolution of eusociality in sponge-dwelling shrimp. In: Kikuchi T (ed) Genes, behavior, and evolution in social insects. University of Hokkaido Press, SapporoGoogle Scholar
  15. Duffy JE, Macdonald KS (2010) Kin structure, ecology and the evolution of social organization in shrimp: a comparative analysis. Proceedings of the Royal Society B: Biological Sciences, 277(1681):575–584, 22 Feb 2010Google Scholar
  16. Froese R, Pauly D (2002) FishBase. World Wide Web electronic publication. Accessed 1 June 2012
  17. Fromhage L, Kokko H (2011) Monogamy and haplodiploidy act in synergy to promote the evolution of eusociality. Nature Commun 2:397CrossRefGoogle Scholar
  18. Gardner A, Alpedrinha J, West Stuart A (2012) Haplodiploidy and the evolution of eusociality: split sex ratios. Am Nat 179(2):240–256CrossRefGoogle Scholar
  19. Goodwin NB, Dulvy NK, Reynolds JD (2002) Life-history correlates of the evolution of live bearing in fishes. Philos Trans R Soc B Biol Sci 357(1419):259–267CrossRefGoogle Scholar
  20. Grutter, Alexandra, Cribb, Thomas, Fargher, Bronwyn, Kuris, Armand, McCormick, Mark Robert Warner, Robert (2012) The larval fish pelagic phase: a sanctuary from harmful parasites?. In: Abstracts of the international coral reef symposium, Cairns, 2012Google Scholar
  21. Hamilton WD (1964a) The genetical evolution of social behaviour. I. J Theor Biol 7(1):1–16CrossRefGoogle Scholar
  22. Hamilton WD (1964b) The genetical evolution of social behaviour. II. J Theor Biol 7(1):17–52CrossRefGoogle Scholar
  23. Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31(2):295–311CrossRefGoogle Scholar
  24. Hughes WOH, Oldroyd BP, Beekman M, Ratnieks FLW (2008) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320(5880):1213–1216CrossRefGoogle Scholar
  25. Jarvis JU (1981) Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212(4494):571–573CrossRefGoogle Scholar
  26. Jeanson R, Kukuk PF, Fewell JH (2005) Emergence of division of labour in halictine bees: contributions of social interactions and behavioural variance. Animal Behav 70(5):1183–1193CrossRefGoogle Scholar
  27. Keller L, Nicolas P (1995) Quantifying the level of eusociality. Proceedings: biological sciences, 260(1359):311–315, 22 Jun 1995Google Scholar
  28. Lehmann L, Rousset F (2010) How life history and demography promote or inhibit the evolution of helping behaviours. Philosophical transactions of the Royal Society B: biological sciences 365(1553):2599–2617, 12 Sep 2010Google Scholar
  29. Malte A (1984) The evolution of eusociality. Annu Rev Ecol Syst 15:165–189Google Scholar
  30. Mann KD, Turnell ER, Atema J, Gerlach G (2003) Kin recognition in juvenile zebrafish (Danio rerio) based on olfactory cues. Biol Bull 205(2):224–225CrossRefGoogle Scholar
  31. Neafsey DE, Palumbi SR (2003) Genome size evolution in pufferfish: a comparative analysis of diodontid and tetraodontid pufferfish genomes. Genome Res 13(5):21–830CrossRefGoogle Scholar
  32. Nowak MA, Tarnita CE, Wilson EO (2010) The evolution of eusociality. Nature 466(7310):1057–1062CrossRefGoogle Scholar
  33. Nowlin WH, Vanni MJ, Yang LH (2008) Comparing resource pulses in aquatic and terrestrial ecosystems. Ecology 89(3):647–659CrossRefGoogle Scholar
  34. Planes S, Jones GP, Thorrold SR (2009) Larval dispersal connects fish populations in a network of marine protected areas. In: Proceedings of the National Academy of Sciences 106(14):5693–5697, 7 Apr 2009Google Scholar
  35. Queller DC (1994) Genetic relatedness in viscous populations. Evol Ecol 8(1):70–73CrossRefGoogle Scholar
  36. Queller DC (1989) The evolution of eusociality: reproductive head starts of workers. In: Proceedings of the National Academy of Sciences, 86(9):3224–3226, 1 May 1989Google Scholar
  37. Ralph B, Johnstone RA, Russell AF, Bshary R (2007) Integrating cooperative breeding into theoretical concepts of cooperation. Behav Process 76(2):61–72CrossRefGoogle Scholar
  38. Robertson DR (1973) Field observations on the reproductive behaviour of a pomacentrid fish, Acanthochromis polyacanthus. Zeitschrift Für Tierpsychologie 32(3):319–324CrossRefGoogle Scholar
  39. Siegel DA, Mitarai S, Costello CJ, Gaines SD, Kendall BE, Warner RR, and Winters KB (2008) The stochastic nature of larval connectivity among nearshore marine populations. Proceedings of the National Academy of Sciences, 105(26):8974–8979, 1 July 2008Google Scholar
  40. Smith CR, Baco AR (2003) Ecology of whale falls at the deep-sea floor. In: Oceanography and marine biology: an annual review, vol 41, pp 311–354Google Scholar
  41. Spanier E, Cobb JS, James M-J (1993) Why are there no reports of eusocial marine crustaceans? Oikos 67(3):573–576CrossRefGoogle Scholar
  42. Steele John H (1985) A comparison of terrestrial and marine ecological systems. Nature 313(6001):355–358CrossRefGoogle Scholar
  43. Taborsky M (1994) Sneakers, satellites, and helpers: parasitic and cooperative behavior in fish reproduction. In: Advances in the study of behavior, vol 23. Academic Press, London, pp 1–100Google Scholar
  44. Thorne BL (1997) Evolution of eusociality in termites. Annu Rev Ecol Syst 28:27–54CrossRefGoogle Scholar
  45. Vasseur DA, Yodzis P (2004) The color of environmental noise. Ecology 85(4):1146–1152CrossRefGoogle Scholar
  46. Vollrath F (1986) Eusociality and extraordinary sex ratios in the spider Anelosimus eximius (Araneae: theridiidae). Behav Ecol Sociobiol 18(4):283–287CrossRefGoogle Scholar
  47. Wade MJ (2001) Maternal gene effects and the evolution of sociality in haplo-diploid organisms. Evolution 55(3):453–458CrossRefGoogle Scholar
  48. Warner RR (1975) The adaptive significance of sequential hermaphroditism in animals. Am Nat 109(965):61–82CrossRefGoogle Scholar
  49. Warner RR, Swearer SE (1991) Social control of sex change in the bluehead wrasse, Thalassoma bifasciatum (Pisces: Labridae). Biol Bulletin 181(2):199–204CrossRefGoogle Scholar
  50. Watson JR, Mitarai S, Siegel DA, Caselle JE, Dong C, McWilliams JC (2010) Realized and potential larval connectivity in the Southern California Bight. Mar Ecol Prog Ser 401:31–48CrossRefGoogle Scholar
  51. Wcislo WT (1997) Social interactions and behavioral context in a largely solitary bee, Lasioglossum (Dialictus) (Hymenoptera, Halictidae). Insectes Soc 44(3):199–208CrossRefGoogle Scholar
  52. West SA, Griffin AS, Gardner A (2007) Evolutionary explanations for cooperation. Curr Biol 17(16):R661–R672CrossRefGoogle Scholar
  53. Whiteman EA, Côté IM (2004) Monogamy in marine fishes. Biol Rev 79(2):351–375CrossRefGoogle Scholar
  54. Wilson EO (1971) The Insect Societies. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  55. Wilson EO (2008) One giant leap: how insects achieved altruism and colonial life. Bioscience 58(1):17–25CrossRefGoogle Scholar
  56. Wilson EO, Hölldobler B (2005) Eusociality: origin and consequences. Proceedings of the National Academy of Sciences of the United States of America. 102(38):13367–13371, 20 Sep 2005Google Scholar
  57. Wong M, Balshine S (2011) The evolution of cooperative breeding in the African cichlid fish, Neolamprologus pulcher. Biol Rev 86(2):511–530CrossRefGoogle Scholar

Copyright information

© Konrad Lorenz Institute for Evolution and Cognition Research 2012

Authors and Affiliations

  1. 1.University of Western SydneyMARCS Institute, Bioelectronics and NeurosciencePenrithAustralia

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