Wednesday, September 9, 2009

Can the Red Queen keep running? A case against recombination


In 2004, Otto and Nuismer published a theoretical paper on the evolution of sex where they examined a range of stereotyped models (e.g. gene-for-gene) of species interactions (both antagonistic and beneficial) that are often used by theoreticians. Their results indicated that sex and recombination were generally selected against regardless of the model of interaction given the assumptions of the quasi linkage equilibrium (QLE, in this case, weak selection and strong recombination). In their numerical simulations that explored parameter space potentially outside the assumptions of the QLE, they found that some cases of the matching-genotypes model (or a strict matching alleles model) of interactions would favor sex and recombination.

Kouyos et al (2007) looked at a wide range of matching alleles models (MAM) and found that when selection was strong, some models would favor sex and recombination. Salathé et al (2008b) also provide evidence of strong selection favoring recombination under the MAM. However, both did find that the closer these models were to a multiplicative form of the MAM, sex and recombination were selected against. These multiplicative matching alleles models (MMAM) were described by Otto and Nuismer (2004) as the negative control in their numerical simulations because they never favored recombination. Their QLE results also indicated that this model of interaction should not generate linkage disequilibrium and therefore neither favor nor select against recombination. Contrary to this, in a surprising result by Kouyos et al (2007), their simulations found that there was strong selection against recombination (rather than no selection at all) in the parameter space near a MMAM.

It was this surprising result that was explained in the paper that we read this past week for Coevolvers (Kouyos et al 2009). Here the authors investigated why this parameter space shows strong selection again recombination. In a MMAM, there are no epistatic interactions between the loci involved in the fitness of the interaction between host and parasite. Despite this, previous observations (Kouyos et al 2007) and the current simulations have shown that strong linkage disequilibrium is built up and maintained. It turns out that here that an interaction governed by the MMAM can equilibrate to a region of high complementarity. The importance of this is that this equilibrium is such that any recombination among the loci will generate genotypes that have a lower fitness and recombination should be selected against.

I think that this recent paper (Kouyos et al 2009) sheds more light on specific potential microevolutionary mechanisms that drive the maintenance of recombination. We still need empirical test of some more of these new predictions. The challenge for empiricists is to find the right kind of systems and a challenge for the theoreticians is to help design the right kinds of experiments.

While I have just touched on a couple of recent results testing aspects of the Red Queen Hypothesis, Salathé et al (2008a) produced a wonderful review of many of many recent theoretical results on the evolution of sex and recombination driven by host-parasite interactions. In addition, this group has another paper on this topic out recently in the American Naturalist (Salathé et al 2009) that I'm looking forward to reading.

References

Kouyos, R., M. Salathe, and S. Bonhoeffer. 2007. The Red Queen and the persistence of linkage-disequilibrium oscillations in finite and infinite populations. BMC Evolutionary Biology 7:211.

Kouyos, R. D., M. Salathé, S. P. Otto, and S. Bonhoeffer. 2009. The role of epistasis on the evolution of recombination in host-parasite coevolution. Theoretical Population Biology 75:1-13.

Otto, S. P., and S. L. Nuismer. 2004. Species interactions and the evolution of sex. Science 304:1018-1020.

Salathé, M., R. D. Kouyos, and S. Bonhoeffer. 2008a. The state of affairs in the kingdom of the Red Queen. Trends in Ecology & Evolution 23:439-445.

Salathé, M., R. D. Kouyos, and S. Bonhoeffer. 2009. On the Causes of Selection for Recombination Underlying the Red Queen Hypothesis. The American Naturalist 174:S31-S42.

Salathé, M., R. D. Kouyos, R. R. Regoes, and S. Bonhoeffer. 2008b. Rapid parasite adaptation drives selection for high recombination rates. Evolution 62:295-300.


KOUYOS, R., SALATHE, M., OTTO, S., & BONHOEFFER, S. (2009). The role of epistasis on the evolution of recombination in host–parasite coevolution Theoretical Population Biology, 75 (1), 1-13 DOI: 10.1016/j.tpb.2008.09.007

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