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Evolution of Multiple Mating Behaviour, in Honey Bees... A Speculation

The multiple mating of a queen honeybees has long been controversial, because of ideas on human morality propagated by religionists. This page seeks to indicate the current range of ideas on how the trait has become part of honey bee behaviour.

What follows is published with the permission of the authors, it is not a complete reproduction of the original text, but has been mainly extracted, in order to give a broad view, from a paper by Kellie Palmer and Ben Oldroyd Entitled...

Evolution of multiple mating in the genus Apis

Apart from the omission of much of the fine detail, the only alterations are due to page structure and re-numbering of references. For full details... Please consult the original paper.

The main arguments
The following arguments are as listed in Crozier and Page [1], with certain modifications:
  1. Multiple mating increases effective population size and therefore is selected for, because it increases population longevity [2].

  2. Multiple mating is favored because it increases the genetic variation within broods.
    This may be beneficial because:
    1. it increases genetic variation between founding queens and between workers;
    2. it forms a basis for caste differentiation;
    3. a mixture of genotypes is 'useful' in a variable environment.

  3. Females mate a number of times because:
    1. of selection favoring sperm competition within their spermathecae;
    2. competition between worker sub-groups favors a more rapid colony division rate, favoring multiple mating which intensifies such competition [3].

  4. Multiple mating is favored by queens because it increases their genetic output relative to that of their worker progeny [4].

  5. Multiple mating by queens is favored because it selects for worker adjustment of the sex ratio to be closer to that selected for at the queen level [4], [5], [6], [7], [8].

  6. Multiple mating is easier for queens than resisting the mating attempts of males [9], [10].

  7. Multiple mating by queens is favored because it enables queens to store sufficient sperm to build up large and long-lived colonies [1], [11], [12], [13].

  8. Multiple mating by queens is selected under certain conditions of colony growth because, when accompanied by a sex determination system based on heterozygosity, it leads to higher colony reproductive success than single mating [14], [15], [16].

  9. The following arguments have been put forward since Crozier and Page [1]: mitigates against the effects of parasitism [17], [18], [19], [20], [21].

  10. Multiple mating is selected for because it increases the probability that an important specialist trait in a population is rare [22].

  11. Polyandry increases the chance that the proportions of the paternity array will produce workers having increased fitness through heterosis [23].
ACKNOWLEDGMENTS

The authors wish to thank the Bee Laboratory at Sydney University and Robin Moritz for constructive comments.
The authors were financially supported by the Australian Research Council.

Kellie A. PALMER, Benjamin P. OLDROYD
School of Biological Sciences A12, University of Sydney, New South Wales 2006, Australia

Abstract
Multiple mating by social insect queens is a widespread phenomenon. Because of the apparent inclusive fitness benefits of monandry, and the potential costs of polyandry, explanations for the evolution of multiple mating have been frequently sought.

Current leading explanations are collectively known as 'genetic variance' hypotheses which posit that both queen and colony fitness are increased by an increase in the intracolonial genetic diversity that accrues from multiple mating.

However, the precise way in which genetic diversity acts to increase colony fitness is not clear. Furthermore, some of these hypotheses are probably insufficient to explain extreme levels of polyandry observed in the genus Apis.

[1] Crozier R.H., Page R.E., On being the right size: male contributions and multiple mating in the social hymenoptera, Behav. Ecol. Sociobiol. 18 (1985) 105-115.

[2] Cole B.J., Multiple mating and the evolution of social behavior in the Hymenoptera, Behav. Ecol. Sociobiol. 12 (1983) 191-201.

[3] Getz W.M., Brückner D., Parisian T.R., Kin structure and the swarming behavior of the honey bee Apis mellifera, Behav. Ecol. Sociobiol. 10 (1982) 265-270.

[4] Moritz R.F.A., The effects of multiple mating on the worker-queen conflict in Apis mellifera, Behav. Ecol. Sociobiol. 16 (1985) 375-377.

[5] Pamilo P., Evolution of colony characteristics in social insects. I. Sex allocation, Am. Nat. 137 (1991) 83-107.

[6] Ratnieks F.L.W., The evolution of polyandry by queens in social hymenoptera: the significance of the timing of removal of diploid males, Behav. Ecol. Sociobiol. 28 (1990) 343-348.

[7] Robinson G., Regulation of division of labor in insect colonies, Annu. Rev. Entomol. 37 (1992) 637-665.

[8] Starr C.K., Sperm competition, kinship, and sociality in the aculate Hymenoptera, in: Smith R.L. (Ed.), Sperm Competition and the Evolution of Animal Mating Systems, Academic Press, Orlando, FL, 1984, pp. 427-464

[9] Alcock J., Eickwort G.V., Eickwort K.R., The reproductive behavior of Anthicium maculoum (Hymenoptera: Megachilidae) and the evolutionary significance of multiple copulations by females, Behav. Ecol. Sociobiol. 2 (1977) 385-396.

[10] Alcock J., Barrows E.M., Gordh G., Hubbard L.J., Kierkendall L., Pyle D.W., Ponder T.L., Zalon F.G., The ecology and evolution of male reproductive behavior in the bees and wasps, Zool. J. Linn. Soc. 64 (1978) 293-336.

[11] Fjerdingstad E.J., Boomsma J.J., Multiple mating increases the sperm stores of Atta colombica leafcutter ant queens, Behav. Ecol. Sociobiol. 42 (1998) 257-261.

[12] Trivers R.L., Hare H., Haplodiploidy and the evolution of the social insects, Science 191 (1976) 249-263.

[13] West-Eberhard M.J., The evolution of social behavior by kin selection, Quart. Rev. Biol. 50 (1975) 1-33.

[14] Page R.E., The evolution of multiple mating behavior by honey bee queens (Apis mellifera L.), Genetics 96 (1980) 263-273.

[15] Page R.E., Metcalf R.A., Multiple mating, sperm utilization, and social evolution, Am. Nat. 119 (1982) 263-281.

[16] Ratnieks F.L.W., The evolution of polyandry by queens in social hymenoptera: the significance of the timing of removal of diploid males, Behav. Ecol. Sociobiol. 28 (1990) 343-348.

[17] Hamilton W.D., Kinship, recognition, disease, and intelligence: constraints of social evolution, in: Ito Y., Brown J.L., Kikkawa J. (Eds.), Animal Societies: Theories and Facts, Japan Sci. Soc. Press, Tokyo, 1987, pp. 81-102.

[18] Schmid-Hempel P., Infection and colony viability in social insects, Phil. Trans. R. Soc. Lond. B 346 (1994) 313-320.

[19] Sherman P.W., Seeley T.D., Reeve H.K., Parasites, pathogens and polyandry in social hymenoptera, Am. Nat. 131 (1988) 602-610.

[20] Shykoff J.A., Schmid-Hempel P., Genetic relatedness and eusociality: parasite-mediated selection on the genetic composition of groups, Behav. Ecol. Sociobiol. 28 (1991) 371-376.

[21] Shykoff J.A., Schmid-Hempel P., Parasites and the advantage of genetic variability within social insect colonies, Proc. R. Soc. Lond. Ser. B 243 (1991) 55-58.

[22] Fuchs S., Schade V., Lower performance in honeybee colonies of uniform paternity, Apidologie 25 (1994) 155-169.

[23] Rinderer T.E., Stelzer J.A., Oldroyd B.P., Tingek S., Levels of polyandry and intracolonial genetic relationships in Apis koschevnikovi, J. Apic. Res. 37 (1998) 281-287.


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Written... 27 November 2003,

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