Skip to main content
SpringerLink
Log in

The evolution of caste polymorphism in social insects:0 Genetic release followed by diversifying evolution

  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

Caste polymorphism, defined as the presence within a colony of two or more morphologically differentiated individuals of the same sex, is an important character of highly eusocial insects both in the Hymenoptera (ants, bees and wasps) and in the Isoptera (termites), the only two groups in the animal kingdom where highly eusocial species occur. Frequently, caste polymorphism extends beyond mere variations in size (although the extent of variations in size can be in the extreme) and is accompanied by allometric variations in certain body parts. How such polymorphism has evolved and why, in its extreme form, it is essentially restricted to the social insects are questions of obvious interest but without satisfactory answers at the present time. I present a hypothesis entitled ‘genetic release followed by diversifying evolution’, that provides potential answers to these questions. I argue that genetic release followed by diversifying evolution is made possible under a number of circumstances. One of them I propose is when some individuals in a species begin to rely on the indirect component of inclusive fitness while others continue to rely largely on the direct component, as workers and queens in social insects are expected to do. Thus when queens begin to rely on workers for most of the foraging, nest building and brood care, and workers begin to rely increasingly on queens to lay eggs—when queen traits and worker traits do not have to be expressed in the same individual—I postulate the relaxation of stabilizing selection and new spurts of directional selection on both queen-trait genes and worker-trait genes (in contrasting directions) leading to caste polymorphism.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Atsatt P. R. 1981a Ant-dependent food plant selection by the mistletoe butterflyOgyris amaryllis (Lycaenidae).Oecologia 48: 60–63

    Article  Google Scholar 

  • Atsatt P. R. 1981b Lycaenid butterflies and ants: Selection for enemy-free spaceAm. Nat. 18: 638–654

    Article  Google Scholar 

  • Bell T. R. 1915 – 1920 The common butterflies of the plains of India.J. Bombay Nat. Hist. Soc. vols. 23 – 27

  • Berenbaum M. R. 1990 Coevolution between herbivorous insects and plants: Tempo and orchestration. InInsect life cycles—genetics, evolution and coordination (ed.) F. Gilbert (London: Springer) pp. 87–99

    Google Scholar 

  • Bourke A. F. G. and Franks N. R. 1995Social evolution in ants (Princeton: Princeton University Press)

    Google Scholar 

  • Burtis K. C. 1993 The regulation of sex determination and sexually dimorphic differentiation inDrosophila. Curr. Opin. Cell Biol. 5: 1006–1014

    Article  CAS  Google Scholar 

  • Caspari E. 1952 Pleiotropic gene action.Evolution 6: 1–18

    Article  Google Scholar 

  • Clarke G. M. and Mckenzie J. A. 1987 Developmental stability of insecticide resistant phenotypes in glow fly: A result of canalizing natural selection.Nature 325: 345–346

    Article  CAS  Google Scholar 

  • Cohan F. M. and Hoffmann A. A. 1986 Genetic divergence under uniform selection. II. Different responses to selection for knockdown resistance to ethanol amongDrosophila melanogaster populations and their replicate lines.Genetics 114: 145–163

    PubMed  CAS  Google Scholar 

  • Craig R. 1983 Subfertility and the evolution of eusociality by kin selection.J. Theor. Biol. 100: 379–397

    Article  Google Scholar 

  • Craig R. and Crozier R. H. 1978 Caste-specific locus expression in ants.Isozyme Bull. 11: 64–65

    Google Scholar 

  • Crozier R. H. and Pamilo P. 1996Evolution of social insect colonies. Sex allocation and kin-selection (eds.) R. M. May and P. Harvey (Oxford: Oxford University Press)

    Google Scholar 

  • Dykhuizen D. and Davies M. 1980 An experimental model: Bacterial specialists and generalists competing in chemostats.Ecology 61: 1213–1227

    Article  Google Scholar 

  • Ehrlich P. R. and Raven P. H. 1964 Butterflies and plants: a study in coevolution.Evolution 18: 568–608

    Article  Google Scholar 

  • Falconer D. S. 1981Introduction to quantitative genetics 2nd edn (London and New York: Longman)

    Google Scholar 

  • Fisher R. A. 1958The genetical theory of natural selection (New York: Dover)

    Google Scholar 

  • Fukuda H., Kubo K, Takeshi K., Takahashi A., Takahashi M., Tanaka B., Wakabayashi M. and Shirozu T. 1978Insects’life in Japan. III. Butterflies (Tokyo: Hoikushu)

    Google Scholar 

  • Gadagkar R. 1991 Demographic predisposition to the evolution of eusociality—A hierarchy of models.Proc. Natl. Acad. Sci. USA 88: 10993–10997

    Article  PubMed  CAS  Google Scholar 

  • Gadagkar R. 1996a What’s the essence of royalty—one keto group.Curr. Sci. 71: 975–980

    CAS  Google Scholar 

  • Gadagkar R. 1996b The evolution of eusociality, including a review of the social status ofRopalidia marginata. InNatural history and evolution of paper wasps (eds.) S. Turillazzi and M. J. West-Eberhard (Oxford: Oxford University Press) pp. 248–271

    Google Scholar 

  • Gilbert F. 1990 Size, phylogeny, and life-history in the evolution of feeding specialization in insect predators. InInsect life cycles—genetics, evolution and co-ordination (ed.) F. Gilbert (London: Springer) pp. 101–124

    Google Scholar 

  • Gorman M., Kuroda M. I. and Baker B. S. 1993 Regulation of the sex-specific binding of themaleless dosage compensation protein to the male X chromosome inDrosophila.Cell 72: 39–49

    Article  PubMed  CAS  Google Scholar 

  • Gorman M., Franke A. and Baker B.S. 1995 Molecular characterization of themale-specific lethal-3 gene and investigations of the regulation of dosage compensation inDrosophila.Development 121: 463–475

    PubMed  CAS  Google Scholar 

  • Haldane J. B. S. 1932The causes of evolution (London: Longmans Green)

    Google Scholar 

  • Hall B. G. 1983 Evolution of new metabolic functions in laboratory organisms. InEvolution of genes and proteins (eds.) M. Nei and R. K. Koehn (Sunderland, Mass., USA: Sinauer) pp. 234–257

    Google Scholar 

  • Hamilton W. D. 1964a The genetical evolution of social behaviour I.J. Theor. Biol. 7: 1–16

    Article  PubMed  CAS  Google Scholar 

  • Hamilton W. D. 1964b The genetical evolution of social behaviour II. J.Theor. Biol. 7: 17–52

    Article  CAS  Google Scholar 

  • Hardison R. C. 1991 Evolution of globin gene families. InEvolution at the molecular level (eds.) R. K. Selander, A. G. Clark and T. S. Whittam (Sunderland, Mass., USA: Sinauer) pp. 272–289

    Google Scholar 

  • Henikoff S. and Meneely P. M. 1993 Unwinding dosage compensation.Cell. 72: 1–2

    Article  PubMed  CAS  Google Scholar 

  • Henning S. F. 1983 Biological groups within the Lycaenidae (Lepidoptera).J. Entomol. Soc. S. Afr. 46:65–85

    Google Scholar 

  • Holldobler B. and Wilson E. O. 1990The ants (Cambridge, USA: Harvard University Press: Cambridge)

    Google Scholar 

  • Hung A. C. F. and Vinson S. B. 1977 Interspecific hybridization and caste specificity of proteins in fire ant.Science 196: 1458–1460

    Article  PubMed  CAS  Google Scholar 

  • Hung A. C. F., Dowler M. and Vinson S. B. 1977 Alpha-glycerophosphate dehydrogenase isozyme of the fire antSolenopsis invicta.Isozyme Bull. 10: 29

    Google Scholar 

  • Kelley R. L., Solovyeva I., Lyman L. M., Richman R., Solovyev V. and Kuroda M. I. 1995 Expression of Ms 1-2 causes assembly of dosage compensation regulators on the X chromosomes and female lethality inDrosophila.Cell. 81: 867–877

    Article  PubMed  CAS  Google Scholar 

  • Lenski R. E. 1988a Experimental studies of pleiotropy and epistasis inEscherichia coll. I. Variation in competitive fitness among mutants resistant to virus T4.Evolution 42: 425–432

    Article  Google Scholar 

  • Lenski R. E. 1988b Experimental studies of pleiotropy and epistasis inEscherichia coli. II, Compensation for maladaptive effects associated with resistance to virus T4.Evolution 42: 433–440

    Article  Google Scholar 

  • Lenski R. E. and Levin B. R. 1985 Constraints on the coevolution of bacteria and virulent phage: A model, some experiments, and predictions for natural communities.Am. Nat. 125: 585–602

    Article  Google Scholar 

  • Li W.-H. and Graur D. 1991Fundamentals of molecular evolution (Sunderland, Mass., USA: Sinauer)

    Google Scholar 

  • McKenzie J. A., Whitten M. J. and Adena M. A. 1982 The effect of genetic background on the fitness of diazinon resistance genotypes of the Australian sheep blowfly.Lucilia cuprina. Heredity 49: 1–9

    Article  Google Scholar 

  • Maynard Smith J., Burian R., Kauffman S., Alberch P., Campbell J., Goodwin B., Lande R., Raup D. and Wolpert L. 1985 Developmental constraints and evolution.Q. Rev. Biol. 60: 265–287

    Article  Google Scholar 

  • Moffett M. 1987 Division of labor and diet in the extremely polymorphic antPheidologeton diversus.Nat. Geogr. Res. 3: 282–304

    Google Scholar 

  • Moritz R. F. A. and Southwick E. E. 1992Bees as superorganisms—An evolutionary reality (Berlin: Springer)

    Google Scholar 

  • Muller H. J. 1935 The origination of chromatin deficiencies as minute deletions subject to insertion elsewhere.Genetics 17: 237–252

    Article  Google Scholar 

  • Olino S. 1970Evolution by gene duplication (Berlin: Springer)

    Google Scholar 

  • Oster G. F. and Wilson E. O. 1978Caste and ecology in the social insects (Princeton: Princeton University Press)

    Google Scholar 

  • Pamilo P. and Crozier R. H. 1982 Measuring relatedness in natural populations: Methodology.Theor. Popul. Biol. 21: 171–193

    Article  Google Scholar 

  • Pierce N. E. and Elgar M. A. 1985 The influence of ants on host plant selection byJalmenus evagoras a myrmecophilous lycaenid butterfly.Behav. Ecol. Sociobiol. 16: 209–222

    Article  Google Scholar 

  • Plettner E., Slessor K. N., Winston M. L. and Oliver J. E. 1996 Caste-selective pheromone biosynthesis in honeybees.Science 271: 1851–1853

    Article  CAS  Google Scholar 

  • RoffD. A. 1990 Understanding the evolution of insect life-cycles: The role of genetic analysis. InInsect life cycles—genetics, evolution and co-ordination (ed.) F. Gilbert (London: Springer) pp. 5–27

    Google Scholar 

  • Rose M. R. 1982 Antagonistic pleiotropy, dominance, and genetic variation.Heredity 48: 63–78

    Article  Google Scholar 

  • Rose M. R., Graves J. L. and Edward W. 1990 The use of selection to probe patterns of pleiotropy in fitness characters. InInsect life cycles—genetics, evolution and co-ordination (ed.) F. Gilbert (London: Springer) pp. 29–42

    Google Scholar 

  • Ross K. G. and Matthews R. W. (eds.) 1991The social biology of wasps (Ithaca and London: Cornell University Press)

    Google Scholar 

  • Scott S. M. and Dingle H. 1990 Developmental programmes and adaptive syndromes in insect life-cycles. InInsect, life cycle—genetcs, evolution and co-ordination (ed.) F. Gilbert (London: Springer) pp. 69–85

    Google Scholar 

  • Service P. M. and Lenski R. E. 1982 Aphid genotypes, plant phenotypes, and genetic diversity: A demographic analysis of experimental data.Evolution 36: 1276–1282

    Article  Google Scholar 

  • Thompson J. N. 1989 Concepts of coevolution.Trends EcoL Evol. 4: 179–183

    Article  Google Scholar 

  • Thompson J. N. 1994The revolutionary process (Chicago and London: The Univeristy of Chicago Press)

    Google Scholar 

  • Uyenoyama M. K. 1986 Pleiotropy and the evolution of genetic systems conferring resistance to pesticides. InPesticide resistance: strategies and tactics for management (eds.) National Research Council Committee on Strategies for the Managament of Pesticide Resistant Pest Populations (Washington DC: National Academic Press) pp. 207–221

    Google Scholar 

  • Via S. 1984 The quantitative genetics of polyphagy in an insect herbivore. II. Genetic correlations in larval performance within and across host plants.Evolution 38: 896–905

    Article  Google Scholar 

  • West-Eberhard M. J. 1975 The evolution of social behavior by kin selection.Q. Rev. Biol. 50: 1–33

    Article  Google Scholar 

  • West-Eberhard M. J. 1978 Polygyny and the evolution of social behavior in wasps.J. Kansas Entomol. Soc. 51: 832–856

    Google Scholar 

  • West-Eberhard M. J. 1979 Sexual selection, social competition, and evolution.Proc. Am. Philos. Soc. 123: 222–234

    Google Scholar 

  • West-Eberhard M. J. 1987 Flexible strategy and social evolution. InAnimal societies: theories and facts (eds.) Y. Ito, J. L. Brown and J. Kikkawa (Tokyo: Japan Scientific Societies Press) pp. 35–51

    Google Scholar 

  • West-Eberhard M. J. 1989 Phenotypic plasticity and the origins of diversity.Annu. Rev. Ecol. Syst. 20: 249–278

    Article  Google Scholar 

  • West-Eberhard M. J. 1992 Behavior and evolution. InMolds, molecules, and metazoa, growing points in evolutionary viology (eds.) P. R. Grant and H. S. Horn (Princeton: Princeton University Press) pp. 57–75

    Google Scholar 

  • Wheeler D. E. 1986 Developmental and physiological determinants of caste in social Hymenoptera: evolutionary implications.Am. Nat. 128: 13–34

    Article  Google Scholar 

  • Wheeler W. M. 1991 The ant-colony as an organism.J. Morph. 22: 307–325

    Article  Google Scholar 

  • Wheeler W. M. 1913 The ants—their structure, development and behaviour (New York Columbia University Press)

  • Wilson E. O. 1953 The origin and evolution of polymorphism in ants.Q. Rev. Biol. 28: 136–156

    Article  PubMed  CAS  Google Scholar 

  • Wilson E. O. 1967 The superorganism concept and beyond. InL’effet de group chez les animaux (Paris: CNRS)pp. 1–13

    Google Scholar 

  • Wilson E. O. 1971The insect societies (Cambridge, USA: Harvard Univeristy Press)

    Google Scholar 

  • Wilson E. O. 1975Sociobiology: The new synthesis (Cambridge, USA: Harvard University Press)

    Google Scholar 

  • Wilson D. S. and Sober E. 1989 Reviving the superorganism.J. Theory, biol 136: 337–356

    Article  CAS  Google Scholar 

  • Wright S. 1968Evolution and genetics of populations. Vol 1 Genetics and biometric foundations (Chicago: University of Chicago Press)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Centre for Ecological Sciences, Indian Institute of Science, 560012, Bangalore, India

    Raghavendra Gadagkar

  2. Animal Behaviour Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Jakkur P. O., 560064, Bangalore, India

    Raghavendra Gadagkar

Authors
  1. Raghavendra Gadagkar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Raghavendra Gadagkar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gadagkar, R. The evolution of caste polymorphism in social insects:0 Genetic release followed by diversifying evolution. J. Genet. 76, 167–179 (1997). https://doi.org/10.1007/BF02932215

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02932215

Keywords

Search

Navigation