Selection at Work in Self-Incompatible Arabidopsis lyrata: Mating Patterns in a Natural Population

Abstract

Identification and characterization of the self-incompatibility genes in Brassicaceae species now allow typing of self-incompatibility haplotypes in natural populations. In this study we sampled and mapped all 88 individuals in a small population of Arabidopsis lyrata from Iceland. The self-incompatibility haplotypes at the SRK gene were typed for all the plants and some of their progeny and used to investigate the realized mating patterns in the population. The observed frequencies of haplotypes were found to change considerably from the parent generation to the offspring generation around their deterministic equilibria as determined from the known dominance relations among haplotypes. We provide direct evidence that the incompatibility system discriminates against matings among adjacent individuals. Multiple paternity is very common, causing mate availability among progeny of a single mother to be much larger than expected for single paternity.H OMOMORPHIC self-incompatibility (SI) systems constitute invisible barriers to self-fertilization and mating among related individuals. Thus, the presence of a self-incompatibility system has a large influence on realized mating patterns in natural populations. Homomorphic SI systems are divided into gametophytic and sporophytic systems that are usually controlled by a single locus with multiple specificities (haplotypes) consisting of two (or more) genes responsible for stigma and pollen reactions. In gametophytic SI (GSI), compatibility results if the haplotype of the pollen is different from both haplotypes of the diploid stigma. When individuals share one haplotype, the reaction is compatible but only one type of pollen fertilizes; that is, an individual of genotype S i S j can be fertilized by pollen carrying S k from an S i S k individual but not by pollen carrying S i . In sporophytic SI (SSI), the diploid pollen parent determines the phenotype of all pollen, and growth of the pollen is averted if this phenotype matches with the phenotype determined by the genotype of the diploid stigma.

Population structure and historical biogeography of European Arabidopsis lyrata

“…Thus our study helps to define the range and extent of diploid A. l. petraea. Within diploid A. l. petraea most diversity (c. 70%) was maintained within populations, which is consistent with early predictions made for this obligate outcrossing (selfincompatible SI) species (Clauss and Mitchell-Olds, 2006;Schierup et al, 2006;Mable and Adam, 2007). The mean estimates for diversity measures were higher compared with average estimates for other short-lived outcrossing perennials (Hamrick and Godt, 1996), potentially reflecting the prolonged flowering period and insect pollination that promote local gene flow.…”

“…The European A. l. petraea retains sporophytic self-incompatibility (Schierup, 1998;Charlesworth et al, 2003), the genetic control ensuring that populations must be established by at least two unrelated individuals. Schierup et al, (2006) detected 11 SRK (pistile locus) haplotypes in an Icelandic population, implying a minimum of six diploid foundering individuals. Consequently the SI system may have helped to retain diversity, counterbalancing the effects of rapid population expansion (Ibrahim et al, 1996) and explain the absence of a clear 'southern richness versus northern purity' pattern associated with many organism's recent post-glacial history (Petit et al, 2003;Hewitt, 2004).…”

“…Arabidopsis lyrata is an outcrossing perennial that shows extensive phenotypic variation and grows in natural habitats that span a large ecological range (Jonsell et al, 1995;Kivimäki et al, 2007;Leinonen et al, 2009;Sandring and Å gren, 2009). Already several local adaptation/ selection studies have been published (Kivimäki et al, 2007;Kuittinen et al, 2007;Leinonen et al, 2009), with special emphasis on studying self-incompatibility evolution Schierup et al, 2006;Mable and Adam, 2007). More of such studies are likely to emerge with the recent availability of the genomic sequence, which makes a comprehensive study of A. lyrata's phylogeographic structure timely.…”

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.…”

“…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). These differences may be a consequence of different molecular mechanisms of SSI in these groups of plants (Hiscock and McInnis, 2003).…”