A Metapopulation Perspective on Genetic Diversity and Differentiation in Partially Self-Fertilizing Plants

Abstract

Abstract. Partial self-fertilization is common in higher plants. Mating system variation is known to have important consequences for how genetic variation is distributed within and among populations. Selfing is known to reduce effective population size, and inbreeding species are therefore expected to have lower levels of genetic variation than comparable outcrossing taxa. However, several recent empirical studies have shown that reductions in genetic diversity within populations of inbreeding species are far greater than the expected reductions based on the reduced effective population size. Two different processes have been argued to cause these patterns, selective sweeps (or hitchhiking) and background selection. Both are expected to be most effective in reducing genetic variation in regions of low recombination rates. Selfing is known to reduce the effective recombination rate, and inbreeding taxa are thus thought to be particularly vulnerable to the effects of hitchhiking or background selection. Here I propose a third explanation for the lower-than-expected levels of genetic diversity within populations of selfing species; recurrent extinctions and recolonizations of local populations, also known as metapopulation dynamics. I show that selfing in a metapopulation setting can result in large reductions in genetic diversity within populations, far greater than expected based the lower effective population size inbreeding species is expected to have. The reason for this depends on an interaction between selfing and pollen migration. Self-fertilization is a common mode of reproduction in plants and has important consequences for how genetic variation is distributed within and among populations. Selfing is known to have several effects on both genetic diversity and differentiation, but two general observations have been made. First, data on allozyme variation in both plants (Hamrick andGodt 1990, 1996) and animals (Jarne 1995) have shown that inbreeding species have lower neutral genetic diversity within populations than more outcrossing taxa. Recent studies, using molecular data have verified this observation and also shown that neutral genetic diversity at the species level is often lower in inbreeding species, compared to closely related, more outcrossing species, although this effect is far less pronounced than within-population diversity

Molecular Evolution of the GapC Gene Family in Amsinckia spectabilis Populations That Differ in Outcrossing Rate

“…Thus reductions in diversity in selfing versus outcrossing populations were beyond that expected from the effect of the selfing rate alone at GapC3. These findings are consistent with predictions of the background selection hypothesis, but selective sweeps (Maynard Smith and Haigh 1974), consequences of metapopulation dynamics (Ingvarsson 2002), and past population bottlenecks cannot be completely ruled out.…”

“…Levels of genetic diversity may result from the action of several factors, including population history, mating system, and direct selection, as well as selection at linked sites. Population history can exert strong effects on levels of DNA polymorphism-for instance, recent extinction and colonizing events (Ingvarsson 2002) and unequal contribution of migrants between demes in subdivided populations (Nagylaki 1982(Nagylaki , 2000Whitlock and Barton 1997) may also reduce effective population size and thereby lead to loss of population genetic variation at neutral loci. The mating system may also contribute to levels of population genetic diversity.…”

Multilocus Analysis of Variation and Speciation in the Closely Related Species Arabidopsis halleri and A. lyrata

“…In the level of variation should be lower in the inbreeding than in the outbreeding species (Pollack 1987; Nordborg absence of population extinction (appendix, Equation A3), the expected ratio is approximated by the expresand Donnelly 1997). Indeed, Ingvarsson (2002) has shown that the ratio of within-population genetic diversion ( 1 ⁄ 2 M ϩ 1)/(M ϩ 1), where M is the population migration parameter 4Nm. A twofold reduction would sity in selfing vs. outbreeding species is much lower in structured populations.…”

“…by the structure of the populations. Indeed, total levels of variation could be quite similar in selfing and in High levels of inbreeding are thus expected to increase the effects of genetic hitchhiking accompanying selecoutcrossing species if migration and effective population size are much lower in inbreeding species than in tive sweeps (Maynard Smith and Haigh 1974;Kaplan et al 1989) and background selection (Charlesworth outcrossing species (Ingvarsson 2002). …”

“…Clauss, M. J., and T. Mitchell-Olds, 2003Population genetics et al 1993 and may greatly influence genetic variability of tandem trypsin inhibitor genes in Arabidopsis species with in inbreeding species (Nordborg et al 1996) eters (Ingvarsson 2002; appendix), the expected effecHilton, H., R. M. Kliman and J. Hey, 1994 Using hitchhiking genes to study adaptation and divergence during speciation within the…”