Genetic polarization: unifying theories for the adaptive significance of recombination

Abstract

The paper by West, Lively and Read (1999) advocates a pluralistic approach to the adaptive signi®cance of recombination, i.e. that a combination of models may better explain the advantage of recombination compared with any single model. This certainly makes intuitive sense since there is no a priori reason to expect a single bene®t to recombination. The paper focuses primarily on three processes: (a) deterministic accumulation of bene®cial mutations in response to chronic antagonistic coevolution (Red Queen); (b) deterministic accumulation of deleterious mutations due to mutation-selection balance (mutational load) and, to a lesser extent, (c) stochastic accumulation of deleterious mutations (Muller's ratchet). Here I provide a simple genetic argument that reinforces the authors call for a pluralistic approach, i.e. I show that the advantages to recombination based on the Red Queen, mutational load and Muller's ratchet are all a direct consequence of the same underlying genetic property that is common to all nonrecombining populations ± so if one process operates they should all operate, at least under the appropriate permissive conditions. The common property of all nonrecombining populations is the movement of new deleterious mutations among individuals within the ®tness distribution of a population. Substantial heritable variance in ®tness among individuals is expected in all natural populations due to recurrent deleterious mutation (in addition to other factors). When recombination is present, the combination of syngamy, segregation and intrachromosomal recombination causes new deleterious mutations to move bidirectionally to better and to worse genetic backgrounds each generation. But when recombination is absent, each new deleterious mutation is trapped in its recipient genome, moving it unidirectionally toward lower ®tness. This generates a continuous `current' of new deleterious mutations owing within the ®tness distribution from greater to lower ®tness classes. Recurrent mutation causes lineages from the highest-®tness class to ux unidirectionally through the population like water down a slow-motion stream. Eventually all genomes in the population are multiply mutated descendants from the highest-®tness class. To accumulate in a nonrecombining population, a new mutation must make its way to the headwaters (highest-®tness class) of this stream of decaying genomes. The only way to reach the headwaters is to be introduced (fortuitously) via mutation into the highest-®tness class, or a neighbouring high-®tness class. All other new mutations (bene®cial or detrimental) are trapped in inferior genetic backgrounds and thereby deterministically eliminated. Rare reverse and compensatory mutations occasionally reverse the unidirectional ow of deleterious mutations, but this effect is miniscule, analogous to turbulence occasionally moving a pebble a short distance upstream. The term `genetic polarization' denotes the virtual unidirectional ow of new deleterious mutations (see for review, Rice, 1996). Many hundreds of mutations of very small effect are expected to accumulate in a population from a number of sources, for example: (a) nonpreferred codon mutations (selective disadvantage £10, Akashi et al., 1998), (b) transposable element inserts (average selective disadvantage »10, Charlesworth et al., 1992) and (c) mutations of nonessential genes (many selection coef®cients »10, Thatcher et al., 1998). The large number of accumulated mutations causes the expected number of individuals in the highest-®tness class to be quite small (one to a few individuals). This is expected even when the genome-wide mutation rate is small (e.g. 0.1) and the populations size is very large (i.e. of the order of 10 or higher). Genetic polarization has two major consequences: (1) it greatly reduces the effective size of a nonrecombining population, i.e. the effective size is the number of individuals in the highest-®tness class and the neighbouring high-®tness classes (Manning & Thompson, 1984; Charlesworth, 1994; Barton, 1995), and (2) it constrains the highest-®tness class to rely solely on its own reproduction to persist, rather than being produced globally by syngamy, recombination and segregation from the population as a whole, as is the case for a recombining population (Rice, 1998). The greatly reduced effective size of a nonrecombining population, compared with its sexual counterpart, causes Correspondence: William R. Rice, Department of Biology & University of California, Santa Cruz, California 95064, USA. Tel: +1 805 893 5793; fax: +1 805 893 4724; e-mail: rice@lifesci.ucsb.edu