Advertisement

Journal of Genetics

, Volume 70, Issue 1, pp 1–31 | Cite as

On testing the role of genetic asymmetries created by haplodiploidy in the evolution of eusociality in the Hymenoptera

  • Raghavendra Gadagkar
Article

Abstract

The haplodiploid genetic system found in all Hymenopterans creates an asymmetry in genetic relatedness so that full-sisters are more closely related to each other than a mother is to her daughters. Thus Hymenopteran workers who rear siblings can obtain higher inclusive fitness compared to individuals who rear offspring. However, polyandry and polygyny reduce relatedness between workers and their sisters and thus tend to break down the genetic asymmetry created by haplodiploidy. Since the advent of electrophoretic analysis of variability at enzyme loci, several estimates of intra-colony genetic relatedness in the Hymenoptera have been published. To test the role of the genetic asymmetry created by haplodiploidy in the evolution of eusociality, I assume that workers are capable of investing in their brothers and sisters in their ratio of relatedness to them. I then compute ahaplodiploidy threshold, which is the threshold relatedness to sisters required for workers to obtain a weighted mean relatedness of 0.5 to siblings and thus break even with solitary foundresses. When workers rear mixtures of sisters and brothers in an outbred population, the value of this threshold is 0.604. An examination of the distribution of 185 estimates of mean genetic relatedness between sisters in Hymenopteran colonies shows that the values are well below the expected 0.75 for full sisters, both in higly eusocial as well as in primitively eusocial species although relatedness values in the latter are higher than in the former. Of the 177 estimates with standard error, 49 are significantly lower than the haplodiploidy threshold and 22 are significantly higher. Of the 35 species studied only 6 have one or more estimates that are significantly higher than the haplodiploidy threshold. For more than half the estimates, the probability of the relatedness value being above the haplodiploidy threshold is less than 0.5. Reanalysis of these data using 0.5 as the threshold does not drastically alter these conclusions. I conclude that the genetic asymmetry created by haplodiploidy is, in most cases, insufficient by itself either topromote the origin of eusociality or tomaintain the highly eusocial state.

Keywords

Evolution of eusociality haplodiploidy genetic relatedness haplodiploidy threshold Hymenoptera 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alexander R.D. 1974 The evolution of social behavior.Annu. Rev. Ecol. Syst. 5: 325–383CrossRefGoogle Scholar
  2. Alexander R. D. and Sherman P. W. 1977 Local mate competition and parental investment in social insects.Science 196: 494–500PubMedCrossRefGoogle Scholar
  3. Anderson R. H. 1963 The laying worker in the Cape honey bee,Apis mellifera capensis.J. Apic. Res. 2: 85–92Google Scholar
  4. Andersson M. 1984 The evolution of eusociality.Annu. Rev. Ecol. Syst. 15: 165–189Google Scholar
  5. Aoki S. 1982 Soldiers and altruistic dispersal in Aphids. InThe biology of social insects (eds) M. D. Breed, C. D. Michener and H. E. Evans (Boulder, Colorado: Westview Press) pp. 154–158Google Scholar
  6. Boomsma J. J. 1989 Sex-investment ratios in ants: Has female bias been systematically overestimated?Am. Nat. 133: 517–532CrossRefGoogle Scholar
  7. Bourke A. F. G. 1988 Worker reproduction in the higher eusocial hymenoptera.Q. Rev. Biol. 63: 291–311CrossRefGoogle Scholar
  8. Carlin N. F. and Frumhoff P. C. 1990 Nepotism in honey bees.Nature (London) 346: 706–707CrossRefGoogle Scholar
  9. Charnov E. L. 1978 Sex-ratio selection in eusocial hymenoptera.Am. Nat. 112: 317–326CrossRefGoogle Scholar
  10. Charnov E. L. 1982The theory of sex allocation (Princeton, New Jersey: Princeton University Press)Google Scholar
  11. Craig R. 1979 Parental manipulation, kin selection and the evolution of altruism.Evolution 33: 319–334CrossRefGoogle Scholar
  12. Craig R. 1980 Sex investment ratios in social Hymenoptera.Am. Nat. 116: 311–323CrossRefGoogle Scholar
  13. Craig R. and Crozier R. H. 1979 Relatedness in the polygynous antMyrmecia pilosula.Evolution 33: 335–341CrossRefGoogle Scholar
  14. Crozier R. H. 1973 Apparent differential selection at an isozyme locus between queens and workers of the antAphaenogaster rudis.Genetics 73: 313–318PubMedGoogle Scholar
  15. Crozier R. H. 1982 On insects and insects: twists and turns in our understanding of the evolution of eusociality. InThe biology of social insects (eds) M. D. Breed, C. D. Michener, H. E. Evans (Boulder, Colorado: Westview Press) pp. 4–9Google Scholar
  16. Crozier R. H. and Pamilo P. 1986 Relatedness within and between colonies of a queenless ant species of the genusRhytidoponera (Hymenoptera: Formicidae).Entomol. Gener. 11: 113–117Google Scholar
  17. Crozier R. H., Pamilo P. and Crozier Y. C. 1984 Relatedness and microgeographic genetic variation inRhytidoponera mayri, an Australian arid-zone ant.Behav. Ecol. Sociobiol. 15: 143–150CrossRefGoogle Scholar
  18. Crozier R. H., Smith B. H. and Crozier Y. C. 1987 Relatedness and population structure of the primitively eusocial beeLasioglossum zephyrum (Hymenoptera: Halictidae) in Kansas.Evolution 41: 902–910CrossRefGoogle Scholar
  19. Darwin C. 1859The origin of species (New York:Collier, 1962)Google Scholar
  20. Fisher R. A. 1930The genetical theory of natural selection (Oxford: Clarendon Press, 1958) pp. xiv & 291Google Scholar
  21. Fletcher D. J. C. and Ross K. G. 1985 Regulation of reproduction in eusocial Hymenoptera.Annu. Rev. Entomol. 30: 319–343CrossRefGoogle Scholar
  22. Frank S. A. and Crespi B. J. 1989 Synergism between sib-rearing and sex ratio in Hymenoptera.Behav. Ecol. Sociobiol. 24: 155–162CrossRefGoogle Scholar
  23. Gadagkar R. 1985a Evolution of insect sociality - A review of some attempts to test modern theories.Proc. Indian Acad. Sci. (Anim. Sci.) 94: 309–324CrossRefGoogle Scholar
  24. Gadagkar R. 1985b Kin recognition in social insects and other animals - A review of recent findings and a consideration of their relevance for the theory of kin selection.Proc. Indian Acad. Sci. (Anim. Sci.) 94: 587–621Google Scholar
  25. Gadakgar R. 1990a Social biology ofRopalidia: Investigations into the origins of eusociality. InSocial insects and the environment, Proceedings of the 11th International Congress of IUSSI (eds) G. K. Veeresh, B. Mallik and C. A. Viraktamath (New Delhi: Oxford and IBH) pp. 9–11Google Scholar
  26. Gadagkar R. 1990b The haplodiploidy threshold and social evolution.Curr. Sci. 59: 374–376Google Scholar
  27. Gadagkar R. 1990c Evolution of eusociality: The advantage of assured fitness returns.Philos. Trans. R. Soc. London B329: 17–25Google Scholar
  28. Gadagkar R. 1990d Origin and evolution of eusociality: A perspective from studying primitively eusocial wasps.J. Genet. 69: 113–125Google Scholar
  29. Gadagkar R. 1991Belonogaster, Mischocyttarus, Parapolybia and independent foundingRopalidia. InSocial biology of wasps (eds) K. G. Ross and R. W. Matthews (Ithaca, NY: Cornell University Press) pp. 149–190 (in press)Google Scholar
  30. Gadagkar R., Chandrashekara K., Chandran, S. and Bhagavan, S. 1990 Serial polygyny inRopalidia marginata: Implications for the evolution of eusociality. InSocial insects and the environment, Proceedings of the 11th International Congress of IUSSI (eds) G. K. Veeresh, B. Mallik and C. A. Viraktamath (New Delhi: Oxford and IBH) pp. 227–228Google Scholar
  31. Gamboa G. J., Reeve H. K. and Pfenning D. W. 1986 The evolution and ontogeny of nestmate recognition in social wasps.Annu. Rev. Entomol. 31: 431–454CrossRefGoogle Scholar
  32. Godfrey H. C. J. and Grafen A. 1988 Unmatedness and the evolution of eusociality.Am. Nat. 131: 303–305CrossRefGoogle Scholar
  33. Grafen A. 1986 Split sex ratios and the evolutionary origins of eusociality.J. Theor. Biol. 122: 95–121CrossRefGoogle Scholar
  34. Hamilton W. D. 1964a The genetical evolution of social behaviour I.J. Theor. Biol. 7: 1–16PubMedCrossRefGoogle Scholar
  35. Hamilton W. D. 1964b The genetical evolution of social behaviour II.J. Theor. Biol. 7: 17–52PubMedCrossRefGoogle Scholar
  36. Hamilton W. D. 1972 Altruism and related phenomena, mainly in social insects.Annu. Rev. Ecol. Syst. 3: 193–232CrossRefGoogle Scholar
  37. Harris H. 1966 Enzyme polymorphisms in man.Proc. R. Soc. London B164: 298–310Google Scholar
  38. Hubby J. L. and Lewontin R. C. 1966 A. molecular approach to the study of genic heterozygosity in natural populations. I. The number of alleles at different loci inDrosophila pseudoobscura.Genetics 54: 577–94PubMedGoogle Scholar
  39. Ito Y. 1989 The evolutionary biology of sterile soldier in Aphids.Tree 4: 69–73Google Scholar
  40. Jarvis J. U. M. 1981 Eusociality in a mammal: Cooperative breeding in naked mole-rat colonies.Science 212: 571–573PubMedCrossRefGoogle Scholar
  41. Joshi N. V. and Gadagkar R. 1985 Evolution of sex ratios in social Hymenoptera: Kin selection, local mate competition, polyandry and kin recognition.J. Genet. 64: 41–58CrossRefGoogle Scholar
  42. Kukuk P. F. 1989 Evolutionary genetics of a primitively eusocial halictine bee,Dialictus zephyrus. InThe genetics of social evolution (eds) M. D. Breed and R. E. Page Jr (Boulder, Colorado: Westview Press) pp. 183–202Google Scholar
  43. Lester L. J. and Selander R. K. 1981 Genetic relatedness and the social organization ofPolistes colonies.Am. Nat. 117: 147–166CrossRefGoogle Scholar
  44. Lewontin R. C. and Hubby J. L. 1966 A molecular approach to the study of genic heterozygosity in natural populations. II. Amount of variation and degree of heterozygosity in natural populations ofDrosophila pseudoobscura.Genetics 54: 595–609PubMedGoogle Scholar
  45. Lin N. and Michener C. D. 1972 Evolution of sociality in insects.Q. Rev. Biol. 47: 131–159CrossRefGoogle Scholar
  46. Macnair M. R. 1978 An ESS for the sex ratio in animals, with particular reference to the social Hymenoptera.J. Theor. Biol. 70: 449–459PubMedCrossRefGoogle Scholar
  47. Metcalf R. A. and Whitt G. S. 1977a Intra-nest relatedness in the social waspPolistes metricus: A genetic analysis.Behav. Ecol. Sociobiol. 2: 339–351CrossRefGoogle Scholar
  48. Metcalf R. A. and Whitt G. S. 1977b Relative inclusive fitness in the social waspPolistes metricus.Behav. Ecol. Sociobiol. 2: 353–360CrossRefGoogle Scholar
  49. Moritz R. F. A. 1986 Two parthenogenetical strategies of laying workers in populations of the honeybee,Apis mellifera (Hymenoptera: Apidae).Entomol. Gener. 11: 159–164Google Scholar
  50. Moritz R. F. A. 1989 Colony level and within colony level selection in honeybees.Behav. Ecol. Sociobiol. 25: 437–444CrossRefGoogle Scholar
  51. Muralidharan K., Shaila M. S. and Gadagkar R. 1986 Evidence for multiple mating in the primitively eusocial waspRopalidia marginata (Lep.) (Hymenoptera: Vespidae).J. Genet. 65: 153–158Google Scholar
  52. Nonacs P. 1986 Ant reproductive strategies and sex allocation theory.Q. Rev. Biol. 61: 1–21CrossRefGoogle Scholar
  53. Oldroyd B. P. and Rinderer T. E. 1990 Nepotism in honey bees.Nature (London) 346: 707–708CrossRefGoogle Scholar
  54. Oster G., Eshel I. and Cohen D. 1977 Worker-queen conflict and the evolution of social insects.Theor. Popul. Biol. 12: 49–85PubMedCrossRefGoogle Scholar
  55. Page R. E. Jr 1986 Sperm utilization in social insects.Annu. Rev. Entomol. 31: 297–320CrossRefGoogle Scholar
  56. Page R. E. Jr, Breed M. D. and Getz W. M. 1990 Nepotism in honey bees.Nature (London) 346: 707Google Scholar
  57. Page R. E. and Metcalf R. A. 1982 Multiple mating, sperm utilization and social evolution.Am. Nat. 119: 263–281CrossRefGoogle Scholar
  58. Page R. E. Jr, and Robinson G. E. 1990 Nepotism in honey bees.Nature (London) 346: 708CrossRefGoogle Scholar
  59. Page R. E. Jr, Robinson G. E. and Fondrk M. K. 1989 Genetic specialists, kin recognition and nepotism in honey-bee colonies.Nature (London) 338: 576–579CrossRefGoogle Scholar
  60. Pamilo P. 1981 Genetic organization ofFormica sanguined populations.Behav. Ecol. Sociobiol. 9: 45–50CrossRefGoogle Scholar
  61. Pamilo P. 1982 Genetic population structure in polygynous formica ants.Heredity 48: 95–106PubMedCrossRefGoogle Scholar
  62. Pamilo P. 1984 Genotypic correlation and regression in social groups: Multiple alleles, multiple loci and subdivided populations.Genetics 107: 307–320PubMedGoogle Scholar
  63. Pamilo P. 1987 Sex ratios and the evolution of eusociality in the Hymenoptera.J. Genet. 66: 111–122Google Scholar
  64. Pamilo P. 1989 Estimating relatedness in social groups.Tree 4: 353–355Google Scholar
  65. Pamilo P. and Crozier R. H. 1982 Measuring genetic relatedness in natural populations: Methodology.Theor. Popul. Biol. 21: 171–193CrossRefGoogle Scholar
  66. Pamilo P. and Rosengren R. 1984 Evolution of nesting strategies of ants: genetic evidence from different population types ofFormica ants.Biol. J. Linn. Soc. 21: 331–348CrossRefGoogle Scholar
  67. Pamilo P. and Varvio-Aho S. 1979 Genetic structure of nests in the antFormica sanguined.Behav. Ecol. Sociobiol. 6: 91–98CrossRefGoogle Scholar
  68. Pearson B. 1983 Intra-colonial relatedness amongst workers in a population of nests of polygynous ant,Myrmica rubra Latreille.Behav. Ecol. Sociobiol. 12: 1–4CrossRefGoogle Scholar
  69. Queller D. C. and Goodnight K. F. 1989 Estimating relatedness using genetic markers.Evolution 43: 258–275CrossRefGoogle Scholar
  70. Queller D. C. and Strassmann J. E. 1989 Measuring inclusive fitness in social wasps. InThe Genetics of social evolution (eds) M. D. Breed and R. E. Page Jr (Boulder, Colorado: Westview Press) pp. 103–122Google Scholar
  71. Queller D. C, Strassmann J. E. and Hughes C. R. 1988 Genetic relatedness in colonies of tropical wasps with multiple queens.Science 242: 1155–1157PubMedCrossRefGoogle Scholar
  72. Ratnieks F. L. W. 1988 Reproductive harmony via mutual policing by workers in eusocial hymenoptera.Am. Nat. 132: 217–236CrossRefGoogle Scholar
  73. Ratnieks F. L. W. and Visscher P. K. 1989 Worker policing in the honeybee.Nature (London) 342: 796–797CrossRefGoogle Scholar
  74. Ross K. G. 1986 Kin selection and the problem of sperm utilization in social insects.Nature (Londonu) 323: 798–800CrossRefGoogle Scholar
  75. Ross K. G. and Fletcher D. J. C. 1985 Comparative study of genetic and social structure in two forms of the fire antSolenopsis invicta (Hymenoptera: Formicidae).Behav. Ecol. Sociobiol. 17: 349–356CrossRefGoogle Scholar
  76. Ross K. G. and Matthews R. W. 1989a New evidence for eusociality in the sphecid waspMicrostigmus comes.Anim. Behav. 38: 613–619CrossRefGoogle Scholar
  77. Ross K. G. and Matthews R. W. 1989b Population genetic structure and social evolution in the sphecid waspMicrostigmus comes.Am. Nat. 134: 574–598CrossRefGoogle Scholar
  78. Ross K. G., Vargo E. L. and Fletcher D. J. C. 1988 Colony genetic structure and queen mating frequency in fire ants of the subgenusSolenopsis (Hymenoptera: Formicidae).Biol. J. Linn. Soc. 34: 105–117CrossRefGoogle Scholar
  79. Schwarz M. P. 1987 Intra-colony relatedness and sociality in the allodapine beeExoneura bicolor.Behav. Ecol. Sociobiol. 21: 387–392CrossRefGoogle Scholar
  80. Seger J. 1983 Partial bivoltinism may cause alternating sex-ratio biases that favour eusociality.Nature (London) 301: 59–62CrossRefGoogle Scholar
  81. Shermann P. W., Jarvis J. U. M. and Alexander R. D. 1991The biology of naked mole rat (Princeton, New Jersey: Princeton University Press)Google Scholar
  82. Starr C. K. 1984 Sperm competition, kinship and sociality in the Aculeate Hymenoptera. InSperm competition and the evolution of animal mating systems (ed.) R. L. Smith (New York: Academic Press) pp. 427–464Google Scholar
  83. Strassmann J. E., Hughes C. R., Queller D. C., Turillazzi S., Cervo R., Davis S. K. and Goodnight K. F. 1989 Genetic relatedness in primitively eusocial wasps.Nature (London) 342: 268–270CrossRefGoogle Scholar
  84. Stubblefield J. W. and Charnov E. L. 1986 Some conceptual issues in the origin of eusociality.Heredity 57: 181–187PubMedCrossRefGoogle Scholar
  85. Trivers R. L. and Hare H. 1976 Haplodiploidy and the evolution of the social insects.Science 191: 249–263PubMedCrossRefGoogle Scholar
  86. Uyenoyama M. K. and Bengtsson B. O. 1981 Towards a genetic theory for the evolution of sex ratio. II. Haplodiploid and diploid models with sibling and parental control of the brood sex ratio and brood size.Theor. Popul. Biol. 20: 57–79CrossRefGoogle Scholar
  87. Venkataraman A. B., Swarnalatha V. B., Nair P. and Gadagkar R. 1988 The mechanism of nestmate discrimination in the tropical social waspRopalidia marginata and its implications for the evolution of sociality.Behav. Ecol. Sociobiol. 23: 271–279CrossRefGoogle Scholar
  88. Visscher P. K. 1989 A quantitative study of worker reproduction in honey bee colonies.Behav. Ecol. Sociobiol. 25: 247–254CrossRefGoogle Scholar
  89. Ward P. S. 1983 Genetic relatedness and colony organization in a species complex of Ponerine ants.Behav. Ecol Sociobiol. 12: 285–299CrossRefGoogle Scholar
  90. Ward P. S. and Taylor R. W. 1981 Allozyme variation, colony structure and genetic relatedness in primitive antNothomyrmecia macrops Clark (Hymenoptera: Formicidae).J. Aust. Entomol, Soc. 20: 177–183CrossRefGoogle Scholar
  91. West-Eberhard M. J. 1975 The evolution of social behaviour by kin selection.Q. Rev. Biol. 50: 1–33CrossRefGoogle Scholar
  92. West-Eberhard M. J. 1978 Polygyny and the evolution of social behavior in social wasps.J. Kans. Entomol. Soc. 51: 832–856Google Scholar
  93. Wilson E. O. 1971The insect societies (Cambridge, Mass: Harvard University Press)Google Scholar

Copyright information

© Indian Academy of Sciences 1991

Authors and Affiliations

  • Raghavendra Gadagkar
    • 1
  1. 1.Centre for Ecological Sciences and Centre for Theoretical StudiesIndian Institute of ScienceBangaloreIndia

Personalised recommendations