The evolution of worker caste diversity in social insects

American Naturalist

Volumn 167, Issue 3, 2006, Pages 390-400

  Fjerdingstad, Else J ^a,b,c   Crozier, Ross H ^a  

^a JAMES COOK UNIVERSITY   (Australia)

^b Laboratoire d'Ecologie   (France)

^c UPMC University Paris 06   (France)

Author keywords

Colony; Kin selection; Policing; Polyandry and polygyny; Polymorphism

Indexed keywords

EVOLUTION; KIN SELECTION; SOCIAL INSECT; WORKER CASTE;

ANIMAL; ANIMAL BEHAVIOR; ANT; ARTICLE; BODY SIZE; CLASSIFICATION; COMPARATIVE STUDY; EVOLUTION; FEMALE; GENETICS; HISTOLOGY; MALE; PHYLOGENY; PHYSIOLOGY; POPULATION DENSITY; REPRODUCTION; SOCIAL BEHAVIOR; SOCIAL DOMINANCE;

ANIMALS; ANTS; BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION; BODY SIZE; EVOLUTION; FEMALE; HIERARCHY, SOCIAL; MALE; PHYLOGENY; POPULATION DENSITY; REPRODUCTION; SOCIAL BEHAVIOR;

FORMICIDAE; HEXAPODA; INSECTA;

EID: 33645508942     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/499545     Document Type: Article

References (83)

1. Abouheif, E., and G. A. Wray. 2002. Evolution of the gene network underlying wing polyphenism in ants. Science 297:249-252.
2. Anderson, C., and F. L. W. Ratnieks. 1999a. Task partitioning in insect societies. Insectes Sociaux 46:95-108.
3. _. 1999b. Task partitioning in insect societies. I. Effect of colony size on queueing delay and colony ergonomic efficiency. American Naturalist 154:521-535.
4. Beshers, S. N., and J. F. A. Traniello. 1994. The adaptiveness of worker demography in the attine ant Trachymyrmex septentrionalis. Ecology 75:763-775.
5. Bourke, A. F. G. 1988. Worker reproduction in the higher eusocial Hymenoptera. Quarterly Review of Biology 63:291-311.
6. _. 1999. Colony size, social complexity and reproductive conflict in social insects. Journal of Evolutionary Biology 12:245-257.
7. Bourke, A. F. G., and N. R. Franks. 1995. Social evolution in ants. Princeton University Press, Princeton, NJ.
8. Breed, M. D., and J. M. Harrison. 1988. Worker size, ovary development and division of labour in the giant tropical ant, Paraponera clavata (Hymenoptera: Formicidae). Journal of the Kansas Entomological Society 61:285-291.
9. Brown, M. J. F., and P. Schmid-Hempel. 2003. The evolution of female multiple mating in social Hymenoptera. Evolution 27: 2067-2081.
10. Brown, J. J., and J. F. A. Traniello. 1998. Regulation of brood-care behavior in the dimorphic castes of the ant Pheidole morrisi (Hymenoptera: Formicidae): effects of caste ratio, colony size, and colony needs. Journal of Insect Behavior 11:209-219.
11. Calabi, P., and J. F. A. Traniello. 1989a. Behavioral flexibility in age castes of the ant Pheidole dentata. Journal of Insect Behavior 2: 663-678.
12. _. 1989b. Social organization in the ant Pheidole dentata: physical and temporal caste ratios lack ecological correlates. Behavioral Ecology and Sociobiology 24:69-78.
13. Chiotis, M., L. S. Jermin, and R. H. Crozier. 2000. A molecular framework for the phylogeny of the ant subfamily Dolichoderinae. Molecular Phylogenetics and Evolution 17:108-116.
14. Cnaani, J., G. E. Robinson, and A. Hefetz. 2000. The critical period for caste determination in Bombus terrestris and its juvenile hormone correlates. Journal of Comparative Physiology 186:1089-1094.
15. Crozier, R. H., and E. J. Fjerdingstad. 2001. Polyandry in social Hymenoptera: disunity in diversity? Annales Zoologici Fennici 38:267-285.
16. Crozier, R. H., and R. E. Page. 1985. On being the right size: male contributions and multiple mating in social Hymenoptera. Behavioral Ecology and Sociobiology 18:105-115
17. Crozier, R. H., and P. Pamilo. 1996. Evolution of social insect colonies: sex allocation and kin selection. Oxford University Press, Oxford.
18. Dejean, A., and R. Feneron. 1996. Polymorphism and oligogyny in the ponerine ant Centromyrmex bequaerti (Formicidae: Ponerinae). Insectes Sociaux 43:87-99.
19. Detrain, C., and J. M. Pasteels. 1991. Caste differences in behavioral thresholds as a basis for polyethism during food recruitment in the ant Pheidole pallidula Nyl. (Hymenoptera: Formicidae). Journal of Insect Behavior 4:157-176.
20. _. 1992. Caste polyethism and collective defense in the ant Pheidole pallidula the outcome of quantitative differences in recruitment. Behavioral Ecology and Sociobiology 29:405-412.
21. Diaz-Uriarte, R., and T. Garland Jr. 1998. Effects of branch length error on the performance of phylogenetically independent contrasts. Systematic Biology 47:654-672.
22. Dietemann, V., B. Hölldobler, and C. Peeters. 2002. Caste specialization and differentiation in reproductive potential in the phylogenetically primitive ant Myrmecia gulosa. Insectes Sociaux 49:289-298.
23. Dijkstra, M. B., D. R. Nash, and J. J. Boomsma. 2005. Self-restraint and sterility in workers of Acromyrmex and Atta leafcutter ants. Insectes Sociaux 51:67-76.
24. Engels, W., and A. Buschinger. 1990. Social insects: an evolutionary approach to castes and reproduction. Springer, Berlin.
25. Evans, J. D., and D. E. Wheeler. 1999. Differential gene expression between developing queens and workers in the honey bee, Apis mellifera. Proceedings of the National Academy of Sciences of the USA 96:5575-5580.
26. _. 2000. Expression profiles during honeybee caste determination. Genome Biology 2:1-6.
27. _. 2001. Gene expression and the evolution of insect polyphenisms. Bioessays 23:62-68.
28. Feener, D. H., Jr., J. R. B. Lighton, and G. A. Bartholomew. 1988. Curvilinear allometry, energetics and foraging ecology: a comparison of leaf-cutting ants and army ants. Functional Ecology 2:509-520.
29. Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125:1-15.
30. Fersch, R., A. Buschinger, and J. Heinze. 2000. Queen polymorphism in the Australian ant Monomorium sp. 10. Insectes Sociaux 47:280-284.
31. Ferster, B., and J. F. A. Traniello. 1995. Polymorphism and foraging behavior in Pogonomyrmex badius (Hymenoptera: Formicidae): worker size, foraging distance, and load size associations. Environmental Entomology 24:673-678.
32. Fraser, V. S., B. Kaufmann, B. P. Oldroyd, and R. H. Crozier. 1999. Genetic influence on caste in the ant Camponotus consobrinus. Behavioral Ecology and Sociobiology 47:188-194.
33. Frumhoff, P. C., and P. S. Ward. 1992. Individual-level selection, colony-level selection and the association between polygyny and worker monomorphism in ants. American Naturalist 139:559-590.
34. Fuchs, S., and R. F. A. Moritz. 1999. Evolution of extreme polyandry in the honeybee Apis mellifera L. Behavioral Ecology and Sociobiology 45:269-275.
35. Garland, T., Jr., P. H. Harvey, and A. R. Ives. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology 41:18-32.
36. Gobin, B., and F. Ito. 2003. Suma wrestling in ants: major workers fight over male production in Acanthomyrmex ferox. Naturwissenschaften 90:318-321.
37. Hamilton, W. D. 1964. The genetical evolution of social behaviour. I, II. Journal of Theoretical Biology 7:1-52.
38. Hammond, R. L., and L. Keller. 2004. Conflict over male parentage in social insects. PLoS Biology 2:1472-1482.
39. Hasegawa, E. 1993. Caste specialization of food storage in the dimorphic ant Colobopsis nipponicus (Wheeler). Insectes Sociaux 40:261-271.
40. _. 1997. The optimal caste ratio in polymorphic ants: estimation and empirical evidence. American Naturalist 149:706-722.
41. Haskins, C. P., and R. M. Whelden. 1965. "Queenlessness," worker sibship, and colony versus population structure in the formicid genus Rhytidoponera. Psyche 72:87-112.
42. Heinze, J., S. Foitzik, B. Oberstadt, O. Ruppell, and B. Hölldobler. 1999. A female caste specialized for the production of unfertilized eggs in the ant Crematogaster smithi. Naturwissenschaften 86:93-95.
43. Hölldobler, B., and E. O. Wilson. 1990. The ants. Harvard University Press, Cambridge, MA.
44. Hughes, W. O. H., S. Sumner, S. Van Borm, and J. J. Boomsma 2003. Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants. Proceedings of the National Academy of Sciences of the USA 100:9394-9397.
45. Ito, F., N. Sugiura, and S. Higashi. 1994. Worker polymorphism in the red-head bulldog ant (Hymenoptera: Formicidae), with the description of nest structure and colony composition. Annals of the Entomological Society of America 87:337-341.
46. Johnson, R. N., P.-M. Agapow, and R. H. Crozier. 2003. A tree island approach to inferring the phylogeny in the ant subfamily Formicinae, with especial reference to the evolution of weaving. Molecular Phylogenetics and Evolution 29:317-330.
47. Keller, L., and L. Passera. 1989. Size and fat content of gynes in relation to the mode of colony founding in ants. Hymenoptera: Formicidae. Oecologia (Berlin) 80:236-240.
48. Monnin, T., and C. Peeters. 1999. Dominance hierarchy and reproductive conflicts among subordinates in a monogynous queenless ant. Behavioral Ecology 10:323-332.
49. O'Donnell, S., and R. L. Jeanne. 1995. The roles of body-size and dominance in division of labor among workers of the eusocial wasp Polybia occidentalis (Olivier) (Hymenoptera, Vespidae). Journal of the Kansas Entomological Society 68:43-50.
50. Oster, G. F., and E. O. Wilson. 1978. Caste and ecology in the social insects. Princeton University Press, Princeton, NJ.
51. Pamilo, P. 1991. Evolution of colony characteristics in social insects. II. Number of reproductive individuals. American Naturalist 138:412-433.
52. Passera, L., E. Roncin, B. Kaufmann, and L. Keller. 1996. Increased soldier production in ant colonies exposed to intraspecific competition. Nature 379:630-631.
53. Peeters, C. 1997. Morphologically "primitive" ants: comparative review of social characters, and the importance of queen-worker dimorphism. Pages 372-391 in J. C. Choe and B. J. Crespi, eds. The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge.
54. Purvis, A., and A. Rambaut. 1995. Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Computer Applications in the Biosciences 11:247-251.
55. Ratnieks, F. L. W. 1988. Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. American Naturalist 132:217-236.
56. Ratnieks, F. L. W., K. R. Foster, and T. Wenseleers. 2006. Conflict resolution in insect societies. Annual Review of Entomology 51:581-608.
57. Schmid-Hempel, P. 1992. Worker castes and adaptive demography. Journal of Evolutionary Biology 5:1-12.
58. Schmid-Hempel, P., and R. H. Crozier. 1999. Polyandry versus polygyny versus parasites. Philosophical Transactions of the Royal Society of London B 354:507-515.
59. Stapley, L. 1999. Physical worker castes in colonies of an acacia-ant (Crematogaster nigriceps) correlated with an intra-colonial division of defensive behaviour. Insectes Sociaux 46:146-149.
60. Traniello, J. F. A., and S. N. Beshers. 1991. Polymorphism and size-pairing in the harvester ant Pogonomyrmex badius: a test of the ecological release hypothesis. Insectes Sociaux 32:121-128.
61. Tschinkel, W. R. 1987. Relationship between ovariole number and spermathecal sperm count in ant queens: a new allometry. Annals of the Entomological Society of America 80:208-211.
62. _. 1988. Colony growth and the ontogeny of worker polymorphism in the fire ant, Solenopsis invicta. Behavioral Ecology and Sociobiology 22:103-115.
63. _. 1993. Sociometry and sociogenesis of colonies of the fire ant Solenopsis invicta during one annual cycle. Ecological Monographs 63:425-457.
64. Tschinkel, W. R., A. S. Mikheyev, and S. R. Storz. 2003. Allometry of workers of the fire ant, Solenopsis invicta. Journal of Insect Sciences 3:1-11
65. Tsuji, K. 1995. Reproductive conflicts and levels of selection in the ant Pristomyrmex pungens: contextual analysis and partitioning of covariance. American Naturalist 146:586-607.
66. Walker, J., and J. Stamps. 1986. A test of optimal caste theory using the ant Camponotus (Colobopsis) impressus. Evolution 67:1052-1062.
67. Ward, P. S. 1986. Functional queens in the Australian greenhead ant, Rhytidoponera metallica (Hymenoptera: Formicidae). Psyche 93:1-12.
68. Ward, P. S., and S. G. Brady. 2003. Phylogeny and biogeography of the ant subfamily Myrmeciinae (Hymenoptera: Formicidae). Invertebrate Systematics 17:361-386.
69. Wenseleers, T., A. G. Hart, and F. L. W. Ratnieks. 2004a. When resistance is useless: policing and the evolution of reproductive acquiescence in insect societies. American Naturalist 164:E154-E167.
70. Wenseleers, T., H. Helantera, A. G. Hart, and F. L. W. Ratnieks. 2004b. Worker reproduction and policing in insect societies: an ESS analysis. Journal of Evolutionary Biology 17:1035-1047.
71. West-Eberhard, M. J. 1975. The evolution of social behavior by kin selection. Quarterly Review of Biology 50:1-33.
72. Wetterer, J. K. 1994. Ontogenic changes in forager polymorphism and foraging ecology in the leaf-cutting ant Atta cephalotes. Oecologia (Berlin) 98:235-238.
73. _. 1999. The ecology and evolution of worker-size distribution in leaf-cutting ants (Hymenoptera: Formicidae). Sociobiology 34:119-144.
74. Wheeler, D. E. 1986. Developmental and physiological determinants of caste in social Hymenoptera: evolutionary implications. American Naturalist 128:13-34.
75. _. 1991. The developmental basis of worker caste polymorphism in ants. American Naturalist 138:1218-1238
76. Whitehouse, M. E. A., and K. Jaffe. 1996. Ant wars: combat strategies, territory and nest defence in the leaf-cutting ant Atta laevigata. Animal Behaviour 51:1204-1217.
77. Wilson, E. O. 1953. The origin and evolution of polymorphism in ants. Quarterly Review of Biology 28:136-156.
78. _. 1971. The insect societies. Belknap/Harvard University Press, Cambridge, MA.
79. _. 1984. The relation between caste ratios and division of labor in the ant genus Pheidole Hymenoptera Formicidae. Behavioral Ecology and Sociobiology 16:89-98.
80. _. 1985. Between-caste aversion as a basis for division of labor in the ant Pheidole pubiventris, Hymenoptera: Formicidae. Behavioral Ecology and Sociobiology 17:35-38.
81. Wilson, E. O., and B. Hölldobler. 1985. Caste-specific techniques of defense in the polymorphic ant Pheidole embolopyx Hymenoptera: Formicidae. Insectes Sociaux 32:3-22.
82. Winter, U., and A. Buschinger. 1986. Genetically mediated queen polymorphism and caste determination in the slave-making ant Harpagoxenus sublaevis (Hymenoptera: Formicidae). Entomologia Generalis 11:125-137.
83. Yang, A. S., C. H. Martin, and H. F. Nijhout. 2004. Geographic variation of caste structure among ant populations. Current Biology 14:514-519.