Do queens select sperm?

Abstract

In their recent Research Update in TREE discussing the genetic caste determination in certain hybrid populations of the harvester ant Pogonomyrmex barbatus [1xGenetic determination of caste in harvester ants. Ashe, A. and Oldroyd, B. Trends Ecol. Evol. 2002; 17: 448–449Abstract | Full Text | Full Text PDF | Scopus (13)See all References[1], Ashe and Oldroyd highlight an interesting problem for queen ants. Because queens are homozygous and workers are heterozygous at a particular locus, successful queens are not only obligatorily polyandrous, but must also mate with males of two different haplotypes to form a successful colony containing both workers and alate queens [2xGenetic basis for queen-worker dimorphism in a social insect. Volny, V. and Gordon, D.M. Proc. Natl. Acad. Sci. U.S.A. 2002; 99: 6108–6111Crossref | PubMed | Scopus (115)See all References, 3xGenetic determination of the queen caste in an ant hybrid zone. Julian, G.E. et al. Proc. Natl. Acad. Sci. U.S.A. 2002; 99: 8157–8160Crossref | PubMed | Scopus (102)See all References]. Authors of one of the original papers reviewed [2xGenetic basis for queen-worker dimorphism in a social insect. Volny, V. and Gordon, D.M. Proc. Natl. Acad. Sci. U.S.A. 2002; 99: 6108–6111Crossref | PubMed | Scopus (115)See all References[2] report an average effective mate number of 3.34 and calculate that, with random mating, ∼26% of triple-mated queens would be unable to produce both workers and reproductive offspring. Ashe and Oldroyd [1xGenetic determination of caste in harvester ants. Ashe, A. and Oldroyd, B. Trends Ecol. Evol. 2002; 17: 448–449Abstract | Full Text | Full Text PDF | Scopus (13)See all References[1] postulate that mating frequency is low because females have evolved sophisticated precopulatory mate choice that involves the ability to distinguish between males of different genotypes.We would like to point out an additional problem facing these queens that might make these ants a superb model for examining the relationship between sexual selection and social evolution. As indicated by Volny and Gordon [2xGenetic basis for queen-worker dimorphism in a social insect. Volny, V. and Gordon, D.M. Proc. Natl. Acad. Sci. U.S.A. 2002; 99: 6108–6111Crossref | PubMed | Scopus (115)See all References[2], ‘a genetic system of caste determination will constrain the ability of a colony to adjust its ratio of workers to reproductives according to its changing needs in different seasons and stages of life’. The problem therefore is that without some sophisticated means of organizing or otherwise discriminating between the two sperm haplotypes and selectively utilizing the competing sperm within her reproductive tract, queens will be unlikely to produce selectively advantageous proportions of female reproductives and workers. In particular, there is likely to be a massive overproduction of reproductive females, because reproductive output of ants is often <10% than that of worker production over a queen's lifetime [4xBourke, A.F.G. and Franks, N.R. See all References[4]. Even if females could somehow manage to mate strategically so as to obtain the right proportion of the two sperm haplotypes, some form of ‘sperm choice’ [5xCryptic female choice: criteria for establishing female sperm choice. Birkhead, T.R. Evolution. 1998; 52: 1212–1218CrossrefSee all References[5] would still be required to modulate temporal variation in the production of female reproductives. Colonies of P. barbatus typically do not produce reproductives during the first five years of their existence – the time required to build a sufficient worker force [6xThe development of an ant colony's foraging range. Gordon, D.M. Anim. Behav. 1995; 49: 649–659Crossref | Scopus (79)See all References[6]. Even after colonies begin production of reproductives, worker production remains continuous, whereas reproductives are only produced seasonally in preparation for the mating flight [2xGenetic basis for queen-worker dimorphism in a social insect. Volny, V. and Gordon, D.M. Proc. Natl. Acad. Sci. U.S.A. 2002; 99: 6108–6111Crossref | PubMed | Scopus (115)See all References[2].Sperm choice by females is challenging to demonstrate and so has been a contentious issue among evolutionary ecologists [5xCryptic female choice: criteria for establishing female sperm choice. Birkhead, T.R. Evolution. 1998; 52: 1212–1218CrossrefSee all References, 7xEberhard, W.G. See all References, 8xCriteria for demonstrating female sperm choice. Pitnick, S. and Brown, W.D. Evolution. 2000; 54: 1052–1056PubMedSee all References, 9xSperm–female co-evolution in Drosophila. Miller, G.T. and Pitnick, S. Science. 2002; 298: 1230–1234Crossref | PubMed | Scopus (256)See all References]. Natural selection for the physiological capacity to selectively use different sperm should have been extremely strong in these harvester ants. They could provide a unique and relatively easy opportunity for unequivocal demonstration of female sperm choice.