Kin structure, ecology and the evolution of social organization in shrimp: A comparative analysis

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1681, 2010, Pages 575-584

  Emmett Duffy, J ^a   Macdonald, Kenneth S ^b  

^a VIRGINIA INSTITUTE OF MARINE SCIENCE   (United States)

^b DIVISION OF INVERTEBRATE ZOOLOGY   (United States)

Author keywords

Cooperative breeding; Ecological constraints; Eusociality; Life history; Phylogeny

Indexed keywords

COMPARATIVE STUDY; COOPERATIVE BREEDING; CRUSTACEAN; EUSOCIALITY; GENETIC STRUCTURE; HOST RANGE; HYPOTHESIS TESTING; KIN SELECTION; LIFE HISTORY THEORY; MARINE ECOSYSTEM; PHYLOGENY; RELATEDNESS; SOCIAL ORGANIZATION; SPONGE;

BELIZE [CENTRAL AMERICA];

ANIMALIA; DECAPODA (CRUSTACEA); HEXAPODA; RATTUS; SYNALPHEUS;

EID: 76249113615     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2009.1483     Document Type: Article

References (62)

1. Agnarsson, I., Aviles, L., Coddington, J. A. & Maddison, W. P. 2006 Sociality in Theridiid spiders: repeated origins of an evolutionary dead end. Evolution 60, 2342-2351. (Pubitemid 44930754)
2. Alexander, R. D., Noonan, K. M. & Crespi, B. J. 1991 The evolution of eusociality. In The biology of the naked mole-rat (eds P. W. Sherman, J. U. M. Jarvis & R. D. Alexander), pp. 3-44. Princeton, NJ: Princeton University Press.
3. Anker, A. & Toth, E. 2008 A preliminary revision of the Synalpheus paraneptunus Coutiere, 1909 species complex (Crustacea: Decapoda: Alpheidae). Zootaxa 1915, 1-28.
4. Arnold, K. E. & Owens, I. P. F. 1999 Cooperative breeding in birds: the role of ecology. Behav. Ecol. 10, 465-471. (doi: 10.1093/beheco/10.5.465)
5. Bourke, A. F. G. & Franks, N. R. 1995 Social evolution in ants. Princeton, NJ: Princeton University Press.
6. Brown, J. L. 1974 Alternate routes to sociality in jays-with a theory for the evolution of altruism and communal breeding. Am. Zool. 14, 63-80.
7. Chapman, T. W., Crespi, B. J., Kranz, B. D. & Schwarz, M. P. 2000 High relatedness and inbreeding at the origin of eusociality in gall-inducing thrips. Proc. Natl Acad. Sci. USA 97, 1648-1650. (doi:10.1073/pnas.020510097)
8. Choe, J. & Crespi, B. J. 1997 The evolution of social behavior in insects and arachnids. Cambridge, UK: Cambridge University Press.
9. Crespi, B. J. 1994 Three conditions for the evolution of eusociality-are they sufficient? Insectes Sociaux 41, 395-400. (doi: 10.1007/BF0l240642)
10. Crespi, B. J. 1996 Comparative analysis of the origins and losses of eusociality: causal mosaics and historical uniqueness. In Phyhgenies and the comparative method in animal behavior (ed. E. P. Martins), pp. 253-287. Oxford, UK: Oxford University Press.
11. Crozier, R. H. & Pamilo, P. 1996 Evolution of social insect colonies. Sex allocation and kin selection. Oxford, UK: Oxford University Press.
12. Didderen, K., Fransen, C. H. J. M. & DeVoogd, N. J. 2006 Observations on sponge-dwelling colonies of Synalpheus (Decapoda, Alpheidae) of Sulawesi, Indonesia. Crustaceana 79, 961-975. (doi:10.1163/1568540067788 15937)
13. Dobkin, S. R. 1965 The first post-embryonic stage of Synalpheus brooksi Coutière. Bull. Mar. Sci. 15, 450-462.
14. Dobkin, S. R. 1969 Abbreviated larval development in caridean shrimps and its significance in the artificial culture of these animals. FAO Fish. Rep. 57, 935-946.
15. Duffy, J. E. 1993 Genetic population-structure in two tropical sponge-dwelling shrimps that differ in dispersal potential. Mar. Biol. 116, 459-470. (doi:10.1007/ BF00350063)
16. Duffy, J. E. 1996a Eusociality in a coral-reef shrimp. Nature 381, 512-514. (doi:10.1038/381512a0)
17. Duffy, J. E. 1996b Synalpheus regalis, new species, a spongedwelling shrimp from the Belize Barrier Reef with comments on host specificity in Synalpheus. J. Crustacean Biol. 16, 564-573. (doi: 10.2307/1548748)
18. Duffy, J. E. 2003 The ecology and evolution of eusociality in sponge-dwelling shrimp. In Genes, behaviors, and evolution in social insects (eds T. Kikuchi, S. Higashi & N. Azuma), pp. 217-252. Sapporo, Japan: University of Hokkaido Press.
19. Duffy, J. E. 2007 Ecology and evolution of eusociality in sponge-dwelling shrimp. In Evolutionary ecology of social and sexual systems: crustaceans as model organisms (eds J. E. Duffy & M. Thiel), pp. 387-409. New York, NY: Oxford University Press.
20. Duffy, J. E. & Macdonald, K. S. 1999 Colony structure of the social snapping shrimp Synalpheus filidigitus in Belize. J. Crustacean Biol. 19, 283-292. (doi:10.2307/ 1549235)
21. Duffy, J. E., Morrison, C. L. & Rios, R. 2000 Multiple origins of eusociality among sponge-dwelling shrimps (Synalpheus). Evolution 54, 503-516. (Pubitemid 30263925)
22. Duffy, J. E., Morrison, C. L. & Macdonald, K. S. 2002 Colony defense and behavioral differentiation in the eusocial shrimp Synalpheus regalis. Behav. Ecol. Sociobiol. 51, 488-495. (doi:10.1007/s00265-002-0455-5)
23. Emlen, S. T. 1982 The evolution of helping. I. An ecological constraints model. Am. Nat. 119, 29-39. (doi:10.1086/ 283888)
24. Emlen, S. T. 1991 Evolution of cooperative breeding in birds and mammals. In Behavioural ecology. An evolutionary approach (eds J. R. Krebs & N. B. Davies), 3rd edn. pp. 301-335. Oxford, UK: Blackwell.
25. Faulkes, C. G., Bennett, N. C., Bruford, M. W., O'Brien, H. P., Aguilar, G. H. & Jarvis, J. U. M. 1997 Ecological constraints drive social evolution in the African mole-rats. Proc. R. Soc. Land. B 264, 1619-1627. (doi:10.1098/ rspb. 1997.0226)
26. Felsenstein, J. 1985 Phylogenies and the comparative method. Am. Nat. 125, 1-15. (doi: 10.1086/284325) (Pubitemid 16276188)
27. Fletcher, J. A., Zwick, M., Doebeli, M. & Wilson, D. S. 2006 What's wrong with inclusive fitness? Trends Ecol. Evol. 21, 597-598. (doi:10.1016/j.tree.2006.08.008) (Pubitemid 44528813)
28. Foster, K. R., Wenseleers, T. & Ratnieks, F. L. W. 2006 Kin selection is the key to altruism. Trends Ecol. Evol. 21, 57-60. (doi: 10.1016/j.tree.2005.11.020)
29. Gadagkar, R. 1991 Demographic predisposition to the evolution of eusociality-a hierarchy of models. Proc. Natl Acad. Sci. USA 88, 10 993-10 997. (doi:10.1073/pnas. 88.24.10993)
30. Hamilton, W. D. 1964 The genetical evolution of social behaviour. J. Theor. Biol. 7, 1-52. (doi: 10.1016/00225193(64)90038-4)
31. Hatchwell, B. J. & Komdeur, J. 2000 Ecological constraints, life history traits and the evolution of cooperative breeding. Anim. Behav. 59, 1079-1086. (doi:10.1006/ anbe. 2000.1394) (Pubitemid 30673116)
32. Hughes, W. O. H., Oldroyd, B. P., Beekman, M. & Ratnieks, F. L. W. 2008 Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213-1216. (doi:10.1126/science. 1156108)
33. Hultgren, K. M., MacDonald, K. S. & Duffy, J. E. In press. Sponge-dwelling snapping shrimp of Curaçao, with descriptions of three new species. Zootaxa.
34. Jarvis, J. U. M. & Bennett, N. C. 1993 Eusociality has evolved independently in 2 genera of bathyergid mole-rats-but occurs in no other subterranean mammal. Behav. Ecol. Sociobiol. 33, 253-260. (doi: 10. 1007/BF02027122)
35. Keller, L. & Perrin, N. 1995 Quantifying the level of eusociality. Proc. R. Soc. Lond. B 260, 311-315. (doi:10.1098/ rspb. 1995.0097)
36. Knowlton, N. 1980 Sexual selection and dimorphism in two demes of a symbiotic, pair-bonding snapping shrimp. Evolution 34, 161-173.
37. Lewis, P. O. 2001 A likelihood approach to estimating phylogeny from discrete morphological character data. Syst. Biol. 50, 913-925. (doi:10.1080/10635150 1753462876)
38. Lin, N. & Michener, C. D. 1972 Evolution of sociality in insects. Q. Rev. Biol. 47. (doi: 10.1086/407216)
39. Macdonald, K. S., Ríos, R. & Duffy, J. E. 2006 Biodiversity, host specificity, and dominance by eusocial species among sponge-dwelling alpheid shrimp on the Belize Barrier Reef. Divers. Distrib. 12, 165-178. (doi:10.1111/j.13669516.2005.00213.x) (Pubitemid 43356912)
40. Macdonald, K. S., Hultgren, K. M. & Duffy, J. E. 2009 Sponge-dwelling snapping shrimp of Discovery Bay, Jamaica, with descriptions of four new species. Zootaxa 2199, 1-57.
41. Maddison, W. P. 1990 A method for testing the correlated evolution of two binary characters: are gains or losses concentrated on certain branches of a phylogenetic tree? Evolution 44, 539-557. (doi: 10.2307/2409434)
42. Maddison, W. P. & Maddison, D. R. 2006 Mesquite: a modular system for evolutionary analysis. Version 1.1. http://mesquiteproject.org.
43. Mathews, L. M. 2007 Evidence for high rates of in-pair paternity in the socially monogamous snapping shrimp Alpheus angulosus. Aquat. Biol. 1, 55-62.
44. Midford, P. E., Garland, T. J. & Maddison, W. P. 2005 PDAP Package of Mesquite. Version 1.07.
45. Morrison, C. L., Rios, R. & Duffy, J. E. 2004 Phylogenetic evidence for an ancient rapid radiation of Caribbean sponge-dwelling snapping shrimps (Synalpheus). Mol. Phylogenet. Evol. 30, 563-581. (doi:10.1016/S10557903(03) 00252-5)
46. Posada, D. & Crandall, K. A. 1998 Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817-818. (doi: 10.1093/bioinformatics/14.9. 817) (Pubitemid 28552116)
47. Queller, D. C. 1989 The evolution of eusociality: reproductive head starts of workers. Proc. Natl Acad. Sci. USA 86, 3224-3226. (doi:10.1073/pnas. 86.9.3224)
48. Queller, D. C. & Strassmann, J. E. 1998 Kin selection and social insects. Bioscience 48, 165-175. (doi:10.2307/ 1313262)
49. Rahman, N., Dunham, D. W. & Govind, C. K. 2003 Social monogamy in the big-clawed snapping shrimp. Alpheus heterochelis. Ethology 109, 457-473. (doi:10.1046/j. 14390310.2003.00885.x)
50. Ríos, R. & Duffy, J. E. 2007 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.
51. Ronquist, F. & Huelsenbeck, J. P. 2003 MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574. (doi:10.1093/bioinformatics/btg180) (Pubitemid 37038874)
52. Rubenstein, D. R. & Lovette, I. J. 2007 Temporal environmental variability drives the evolution of cooperative breeding in birds. Curr. Biol. 17, 1414-1419. (doi:10. 1016/j.cub.2007.07.032)
53. Rubenstein, D. R., McCleery, B. V. & Duffy, J. E. 2008 Microsatellite development suggests evidence of polyploidy in the social sponge-dwelling snapping shrimp Zuzalpheus brooksi. Mol. Ecol. Resources 8, 890-894. (doi:10.1111/j.1755-0998.2008.02100.x)
54. Selander, R. K. 1964 Speciation in wrens of the genus Campylorhynchus. Univ. Calif. Publ. Zool. 74, 1-224.
55. Strassmann, J. E. & Queller, D. C. 2007 Insect societies as divided organisms: the complexities of purpose and cross-purpose. Proc. Natl Acad. Sci. USA 104, 8619-8626. (doi: 10.1073/pnas.0701285104)
56. Strathmann, R. R. 1985 Feeding and nonfeeding larval development and life-history evolution in marineinvertebrates. Annu. Rev. Ecol. Syst. 16, 339-361. (doi:10.1146/annurev.es.16.110185.002011)
57. Tóth, E. & Bauer, R. T. 2007 Gonopore sexing technique allows determination of sex ratios and helper composition in eusocial shrimps. Mar. Biol. 151, 1875-1886. (doi: 10. 1007/s00227-007-0618-z) (Pubitemid 46789081)
58. Tóth, E. & Duffy, J. E. 2005 Coordinated group response to nest intruders in social shrimp. Biol. Lett. 1, 49-52. (doi: 10.1098/rsbl.2004.0237) (Pubitemid 41529981)
59. Wenseleers, T. & Ratnieks, F. L. W. 2006 Comparative analysis of worker reproduction and policing in eusocial hymenoptera supports relatedness theory. Am. Nat. 168, E163-E179. (doi: 10.1086/508619)
60. Wilson, E. O. 1971 The insect societies. Cambridge, MA: Harvard University Press.
61. Wilson, E. O. 2005 Kin selection as the key to altruism: its rise and fall. Soc. Res. 72, 159-166.
62. Wilson, E. O. & Hölldobler, B. 2005 Eusociality: origin and consequences. Proc. Natl Acad. Sci. USA 102, 13 367-13 371. (doi:10.1073/pnas. 0505858102)