Sweeping away differences

Thinking about those wolves and their population structure a bit more, I was leafing through a back issue of New Phytologist, and found an article by Loren Rieseberg and colleagues. From a theoretical perspective, strong population differentiation is no problem, since there is always recourse to natural selection as a mechanism to make local populations different -- exactly the solution proposed for the wolves.

Rieseberg and colleagues have a section that considers the opposite problem: what is it that keeps species with low gene flow cohesive?

Students of speciation have primarily focused on the conservative role of gene flow, in which high levels of gene flow (Nem > 4, where Nem is the effective number of migrants per generation) serve to homogenize populations at neutral loci (Hartl & Clark, 1997). It was recognized more than three decades ago, however, that levels of gene flow in many species are not nearly this high (Ehrlich & Raven, 1969). Indeed, for many plant and animal species, estimates of Nem fall well below one (Fig. 1), the level of gene flow required to prevent divergence at neutral loci (Wright, 1931).

Humans today have Nem > 1, but a lot of large mammal species don't (as a yardstick, Nem > 1 predicts FST < 0.2). </p>

Consideration of the creative role of gene flow as a mechanism for the spread of advantageous alleles offers a potential solution to this problem (Rieseberg & Burke, 2001). Only very low levels of gene flow are required for the spread of advantageous alleles and fixation times are much less than for their neutral counterparts (Slatkin, 1976). Thus, it is conceivable that species' populations could remain connected through repeated selective sweeps of favored mutations and associated hitchhiking events or 'genetic draft' (Gillespie, 2001).
Is this scenario likely? In low gene flow species, population subdivision greatly reduces the rate of allelic spread, particularly for weakly selected or neutral alleles (Slatkin, 1976; Whitlock, 2003). Thus, one concern is whether a favored allele will spread to fixation before it goes extinct. A second concern is whether selective sweeps are frequent enough to produce cohesion. If they are rare or restricted to a handful of loci, the level of connectedness might not be sufficient to account for the apparent cohesiveness observed for many species in nature.

They discuss modeling results that quantify the possible dispersal rates of favorable mutations with low gene flow, concluding:

In sum, the effects of population subdivision are to greatly increase fixation times relative to panmictic populations with a slight positive effect on fixation probabilities. More importantly, however, population subdivision magnifies the differences in time to fixation for strongly and weakly selected alleles. Thus, weakly selected alleles that spread to fixation in panmictic populations are less likely to do so in subdivided populations, possibly biasing fixed interspecific differences toward major genes.

Next comes an empirical question: are beneficial mutations typically selected strongly enough to disperse through such metapopulations? They conclude that they often are, so much so that repeated sweeps may be the major reason that the genomes of widespread species remain connected instead of fragmenting into local, isolated variants.

The theme of the paper as a whole is to discuss the ways that natural selection may lead to speciation, focusing on peripatric and sympatric contexts. Thus, several "sterility loci", and other genes promoting and maintaining differentiation of populations, are described.

References:

Rieseberg LH, Church SA, Morjan CL. 2004. Integration of populations and differentiation of species. New Phytologist 161:59--70. DOI link