A pluralist approach to sex and recombination

One of the greatest challenges for evolutionary biology is explaining the widespread occurrence of sexual reproduction, and the associated process of genetic recombination (Williams, 1975; Maynard Smith, 1978; Bell, 1982; Stearns, 1987; Michod & Levin, 1988; Hurst & Peck, 1996). Asexual females can potentially produce twice as many daughters as sexual females, so that the ratio of asexual to sexual females should initially double each generation, resulting in a `two-fold cost of sex'. In addition, recombination breaks up favourable gene combinations that have increased in frequency under the action of natural selection. Given these costs, we would expect natural selection to favour asexual reproduction in wild populations. However, it generally does not: sexual reproduction is widespread throughout the animal and plant kingdoms. In order to solve this apparent paradox, a considerable number (>20) of theoretical models have been developed which purport to show conditions under which there is a suf®ciently large short-term advantage for sex to offset a two-fold cost (Kondrashov, 1993). In this paper we are concerned primarily with models that provide a deterministic advantage to sex and recombination through the production of genetically variable offspring (Weismann, 1889). This can increase the ef®ciency of selection, and hence accelerate the increase in mean ®tness (Kondrashov, 1993; Barton, 1995; Feldman et al., 1997). These models can be broadly classi®ed into two groups: (1) environmental (or ecological) models and (2) mutation-based models (Kondrashov, 1988; Maynard Smith, 1988b). Environmental models suggest that sex accelerates adaptation to a changing environment by creating new gene combinations (Bell, 1982). The biological basis of such varying selection pressures may involve a variety of biotic or abiotic mechanisms (Haldane, 1932; Bell, 1982). Currently the most popular environmental hypothesis, the Red Queen, states that sex provides an advantage in biotic interactions (Bell, 1982; Bell & Maynard Smith, 1987). Usually, parasites are assumed to provide the antagonistic driving force in this coevolutionary dance (Jaenike, 1978; Bremermann, 1980; Hamilton, 1980, 1993; Seger & Hamilton, 1988; Hamilton et al., 1990), though host immune responses may also do so (Gemmill et al., 1997). The `dance' results from time-lagged selection by coevolving parasites against common host genotypes, leading to sustained oscillations in host and parasite gene frequencies (Hutson & Law, 1981; Bell, 1982).