Effect of balancing selection on spatial genetic structure within populations: theoretical investigations on the self-incompatibility locus and empirical studies in Arabidopsis halleri

Abstract

The effect of selection on patterns of genetic structure within and between populations may be studied by contrasting observed patterns at the genes targeted by selection with those of unlinked neutral marker loci. Local directional selection on target genes will produce stronger population genetic structure than at neutral loci, whereas the reverse is expected for balancing selection. However, theoretical predictions on the intensity of this signal under precise models of balancing selection are still lacking. Using negative frequency-dependent selection acting on self-incompatibility systems in plants as a model of balancing selection, we investigated the effect of such selection on patterns of spatial genetic structure within a continuous population. Using numerical simulations, we tested the effect of the type of self-incompatibility system, the number of alleles at the selfincompatibility locus and the dominance interactions among them, the extent of gene dispersal, and the immigration rate on spatial genetic structure at the selected locus and at unlinked neutral loci. We confirm that frequency-dependent selection is expected to reduce the extent of spatial genetic structure as compared to neutral loci, particularly in situations with low number of alleles at the self-incompatibility locus, high frequency of codominant interactions among alleles, restricted gene dispersal and restricted immigration from outside populations. Hence the signature of selection on spatial genetic structure is expected to vary across species and populations, and we show that empirical data from the literature as well as data reported here on three natural populations of the herb Arabidopsis halleri confirm these theoretical results.

Impact of negative frequency-dependent selection on mating pattern and genetic structure: a comparative analysis of the S-locus and nuclear SSR loci in Prunus lannesiana var. speciosa

“…Although the relatively narrow areas of the plots were investigated in our study, the gene dispersal within plots and the pollen immigration from outside the plots were restricted in comparison with those recorded from the other related species (P. avium in Schueler et al, 2006and Cottrell et al, 2009, P. mahaleb in Garcíia et al, 2005. Thus, less-clear spatial genetic structure at the S-locus observed in P. lannesiana populations was consistent with the expectations in Leducq et al (2011).…”

“…Population structure at the S-locus Theoretical predictions for balancing selection are lower genetic differentiation between populations and less-clear spatial genetic structure at the S-locus in comparison with that at selectively neutral9 loci (Schierup, 1998;Schierup et al, 2000;Muirhead, 2001;Leducq et al, 2011). Glémin et al, 2005 compared genetic structure between the S-locus and SSR loci in five populations of Brassica insularis with a sporophytic SI system, and their results were consistent with these predictions.…”

“…Glémin et al, 2005 compared genetic structure between the S-locus and SSR loci in five populations of Brassica insularis with a sporophytic SI system, and their results were consistent with these predictions. Although Brennan et al, 2003 found no significant spatial genetic structure at either the S-locus or allozyme loci in Senecio aqualidus, Leducq et al (2011) recorded reduced spatial genetic structure at the S-locus than at SSR loci in Arabidopsis halleri. In rosaceous species with a gametophytic SI system, Stoeckel et al (2008) and Holderegger et al (2008) found less genetic differentiation between populations at the S-locus than at SSR loci, although Schueler et al (2006) did not find any differences in the extent of spatial genetic structure between the two locus types.…”

“…In Senecio squalidus, spatial genetic structure within populations was found to be weak at both the S-locus and at allozyme loci for which variation seemed to be selectively neutral (Brennan et al, 2003), whereas genetic differentiation among populations was smaller at the S-locus than at the allozyme loci (Brennan et al, 2006). In Arabidopsis halleri, the spatial genetic structure within populations was weaker when determined on the basis of the S-locus than when SSR loci were considered (Leducq et al, 2011). In P. avium, genetic differentiation among populations was smaller according to S-locus data than SSR loci (Stoeckel et al, 2008); higher diversity and evenness in allele frequencies, as well as larger deviations from neutrality at the S-locus than at the SSR loci were observed in a local population, but the spatial genetic structure within the population did not differ between these loci (Schueler et al, 2006).…”

“…Our results showed less genetic differentiation between populations and reduced spatial genetic structure, as indicated by the G ST values and kinship coefficients, at the S-locus than at the SSR loci at different spatial scales (Tables 3 and 4). Unlike the genetic differentiations among populations, the signature of NFDS effects on spatial genetic structure is expected to depend strongly on population and species characteristics, such as the extent of pollen and seed dispersal, the degree of population isolation, the type of SI system and the allelic diversity at the S-locus (Leducq et al, 2011). It is predicted that, for a certain allelic diversity at the S-locus, limited gene dispersal in isolated populations tends to increase difference in the NFDS effects on spatial genetic structure between the S-locus and SSR loci.…”