Evolution of sex and recombination: theory


Sex vs. asex.--Steve Howard and I have used computer simulations to study the roles of mutation accumulation and host-parasite coevolution on the evolutionary maintenance of sexual reproduction. The results may be summarized as follows. (Link to Steve Howard's research)

1. Consistent with the results of May & Anderson (1983), we find that host-parasite coevolution is NOT sufficient by itself to prevent the replacement of a sexual population by a clonal lineage, unless the parasites kill or castrate infected hosts (Howard & Lively 1994). In fact, parasites can select for the accumulation of clonal diversity; leading to the elimination of a sexual population by a diverse set of clonal genotypes (Lively & Howard 1994).

2. We also find that mutation accumulation is not sufficient, assuming that clones do not begin in mutation-selection balance (as assumed in some models), but rather are sampled from the distribution of mutations in the sexual population, which is at mutation-selection balance (Howard & Lively 1998). This result is surprisingly insensitive to the function that maps mutation number onto fitness.

3. However, we find that the combination of mutation accumulation and host-parasite coevolution is a powerful mechanism for the elimination of clones in the short term, and the evolutionary persistence of sexual reproduction (Howard & Lively 1994, 1998). The reason is that, in these simulations, parasites drive clones through repeated bottlenecks (but do not eliminate them). These bottlenecks increase the rate of mutation accumulation by genetic drift (Muller's ratchet). The clones are then eventually eliminated by a mutational meltdown (show me the results). The basic ideas form a pluralist hypothesis for sex, which we have argued provides the most productive course for future studies (West et al. 1999).

4. The combination of antagonistic coevolution and Muller's ratchet can also maintain sex in parasites (Howard and Lively 2002). Thus, happily, parasites are not required to maintain sex in parasites, thereby avoiding an infinite regress.

Recombination.--Andy Peters and I have similarly used computer simulations to determine the effect of host-parasite coevolution on the fate of alleles that increase the rate of physical recombination between loci. We have found that host-parasite coevolution generates fluctuating epistasis for both host and parasite fitness, and that fluctuating epistasis can select for recombination (Peters & Lively 1999). Fluctuating epistasis differs as a mechanism from directional selection for recombination in that the product of linkage disequilibrium and epistasis oscillates between positive and negative (see Barton, 1995).  Andy Peters' webpage

Self-fertilization.--Finally, Aneil Agrawal and I have used simulation models to determine whether an allele for self-fertilization would go to fixation in a population interacting with parasites (Agrawal & Lively 2001). The results depend heavily on the genetic basis for infection, but we did find that for much of the parameter space we examined, interactions with parasites led to the evolution of mixed mating systems. Mixed mating is the condition where hermaphroditic parents produce a mixture of selfed and outcrossed progeny.  Aneil Agrawal's webpage.

Papers cited

Agrawal, A. and C. M. Lively. 2001. Parasites and the evolution of self fertilization. Evolution 55:869-879.

May. R.M. and R.M. Anderson. 1983. Epidemiology and genetics in the coevolution of parasites and hosts. Proceedings of the Royal Society of London B, Biological Sciences 219: 281-313.

Barton, N.H. 1995. A general model for the evolution of recombination. Genetical Research, Cambridge 65:123-144.

Howard, R.S. and C.M. Lively. 1994. Parasitism, mutation accumulation and the maintenance of sex. Nature 367:554-557. (MS copy)

Howard, R.S. and C.M. Lively. 1998. The maintenance of sex by parasitism and mutation accumulation under epistatic fitness functions. Evolution 52:604-610. (MS copy)

Howard, R. S. and C.M. Lively. 2002. The ratchet and the Red Queen: the maintenance of sex in parasites. Journal of Evolutionary Biology 15:648-656.

Lively, C.M.,and R.S. Howard. 1994. Selection by parasites for clonal diversity and mixed mating. Philosophical Transactions of the Royal Society 346:271-281. (MS copy)

Peters, A.D. and C.M. Lively. 1999. The Red Queen and fluctuating epistasis: a population genetic analysis of antagonistic coevolution. American Naturalist 154:393-405.

West, S. A., C. M. Lively, and A. F. Read. 1999. A pluralist approach to sex and recombination. Journal of Evolutionary Biology 12:1003-1012.

C. M. Lively, Dept. of Biology, Indiana University
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