Balancing Selection in the Wild: Testing Population Genetics Theory of Self-Incompatibility in the Rare SpeciesBrassica insularis

Abstract

Self-incompatibility (SI) systems are widespread mechanisms that prevent self-fertilization in angiosperms. They are generally encoded by one genome region containing several multiallelic genes, usually called the S-locus. They involve a recognition step between the pollen and the pistil component and pollen is rejected when it shares alleles with the pistil. The direct consequence is that rare alleles are favored, such that the S-alleles are subject to negative frequency-dependent selection. Several theoretical articles have predicted the specific patterns of polymorphism, compared to neutral loci, expected for such genes under balancing selection. For instance, many more alleles should be maintained and populations should be less differentiated than for neutral loci. However, empirical tests of these predictions in natural populations have remained scarce. Here, we compare the genetic structure at the S-locus and microsatellite markers for five natural populations of the rare species Brassica insularis. As in other Brassica species, B. insularis has a sporophytic SI system for which molecular markers are available. Our results match well the theoretical predictions and constitute the first general comparison of S-allele and neutral polymorphism.H OMOMORPHIC self-incompatibility (SI) systems are widespread physiological mechanisms preventing self-fertilization in Angiosperms by controlling pollen germination or pollen tube growth (De Nettancourt 2001). Pollen and pistil are incompatible when they both express identical alleles. The recognition involves specificity molecules usually encoded by one genome region containing several multiallelic genes (De Nettancourt 2001). In gametophytic (GSI) systems, the pollen phenotype is encoded by its own haploid genome, whereas in sporophytic (SSI) systems, the pollen phenotype is determined by the sporophyte (diploid pollen parent) and can involve dominance interactions among alleles. For instance, two classes of alleles are known in Brassica oleracea (Nasrallah 1991). Class I alleles are dominant over the class II alleles in the pollen, while alleles within class I and class II are mutually codominant. In the pistil, all alleles are codominant. This scheme is also found in B. campestris, with the exception that alleles occur in three dominance levels in the pollen and a few alleles are recessive in the stigma (Hatakeyama et al. 1998). At the molecular level, the SSI system of the Brassicaceae is among the best known (for a recent review see Hiscock and McInnis 2003). Both pistil and pollen genes have been identified (Schopfer et al. 1999;Takayama et al. 2000). In this system, recognition proceeds through receptor-ligand interaction between S-locus cysteinerich protein (SCR), a small hypervariable ligand peptide, and S-locus receptor kinase (SRK), a transmembrane receptor with an intracellular kinase domain (Kachroo et al. 2001).SI evolutionary properties have also long aroused the population geneticist's interest because selection pressures are known a priori. C...

Sporophytic self-incompatibility in Senecio squalidus (Asteraceae): S allele dominance interactions and modifiers of cross-compatibility and selfing rates

“…This observation of increasing numbers of S alleles with increasing dominance level is in accordance with both theoretical expectations (Schierup et al, 1997;Schierup, 1998;Uyenoyama, 2000;Billiard et al, 2007) and empirical observations (Kowyama et al, 1994;Glemin et al, 2005;Prigoda et al, 2005;Schierup et al, 2006) for SSI systems with multiple S allele dominance classes. This difference in S allele diversity, dependant on the relative dominance level of individual S alleles, is due to stronger negative frequency-dependent selection acting upon more dominant S alleles because their S phenotypes are more frequently expressed and exposed to selection in different S genotype combinations than more recessive S alleles.…”

“…No such constraints apply to SSI in which complex S allele dominance interactions are possible in both pollen and pistil, thereby introducing an additional level of mating system complexity relative to GSI (Schierup et al, 1997). Within SSI systems, different kind of dominance interactions are possible, including complete dominance and tissue-specific dominance, and S alleles can often be ranked into a dominance hierarchy consisting of dominance classes of S alleles with codominant interactions between alleles within the group and dominance interactions between alleles from different groups (for example, Ockendon, 1974;Kowyama et al, 1994;Mehlenbacher, 1997;Glemin et al, 2005). S alleles that are frequently recessive in S allele interactions (hereafter referred to as recessive S alleles) are subject to less intense negative frequencydependent selection than dominant or codominant S alleles leading to a 'recessive effect' whereby recessive S alleles are more frequent within populations than more dominant S alleles (Sampson, 1974;Schierup, 1998;Billiard et al, 2007).…”

“…For example, in the well-studied Brassica (Brassicaceae) SSI system, S allele dominance in the pistil appears to be limited to two or three dominance levels, whereas in pollen, there are multiple dominance levels (Ockendon, 1974;Glemin et al, 2005). In contrast many largely coincident dominance levels have been observed for both pollen and pistil S alleles in other SSI systems within the Brassicaceae and other plant families such as the Convolvulaceae and Betulaceae (Kowyama et al, 1994;Mehlenbacher, 1997;Prigoda et al, 2005;Schierup et al, 2006).…”

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

“…In Brassica insularis, Glémin et al (2005) compared the population structure at the S-locus with that indicated by selectively neutral loci, nuclear simple sequence repeats (SSRs or microsatellites); their data supported most of the theoretical predictions. 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).…”

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

“…A low population genetic structure at the S-locus is thus expected, even under very restricted migration (Schierup et al, 2000;Muirhead, 2001). These predictions have been tested in natural populations, and the results showed that the S-locus has indeed a lower genetic differentiation among populations than neutral loci (Glémin et al, 2005;Schierup et al, 2008;Stoeckel et al, 2008).…”