Origin and Diversification Dynamics of Self-Incompatibility Haplotypes

Abstract

Self-incompatibility (SI) is a genetic system found in some hermaphrodite plants. Recognition of pollen by pistils expressing cognate specificities at two linked genes leads to rejection of self pollen and pollen from close relatives, i.e., to avoidance of selffertilization and inbred matings, and thus increased outcrossing. These genes generally have many alleles, yet the conditions allowing the evolution of new alleles remain mysterious. Evolutionary changes are clearly necessary in both genes, since any mutation affecting only one of them would result in a nonfunctional self-compatible haplotype. Here, we study diversification at the S-locus (i.e., a stable increase in the total number of SI haplotypes in the population, through the incorporation of new SI haplotypes), both deterministically (by investigating analytically the fate of mutations in an infinite population) and by simulations of finite populations. We show that the conditions allowing diversification are far less stringent in finite populations with recurrent mutations of the pollen and pistil genes, suggesting that diversification is possible in a panmictic population. We find that new SI haplotypes emerge fastest in populations with few SI haplotypes, and we discuss some implications for empirical data on S-alleles. However, allele numbers in our simulations never reach values as high as observed in plants whose SI systems have been studied, and we suggest extensions of our models that may reconcile the theory and data.G ENES involved in recognition systems, such as the major histocompatibility complex in vertebrates (Solberg et al. 2008), mating types either in fungi (Billiard et al. 2011) or protists (Phadke andZufall 2009), and self-incompatibility (SI) in plants (Lawrence 2000), typically show extraordinarily high levels of genetic diversity. SI is widespread in angiosperms [found in .100 families ] and is highly multiallelic [up to 200 SI haplotypes (Lawrence 2000)]. This system enables hermaphrodite plants to avoid selfing and mating with close relatives and is based on recognition and rejection of pollen by pistils if they express cognate SI specificities. In many species, SI specificity is controlled by a single genetic locus (the S-locus) composed of two linked genes, one expressed in pollen and the other in styles (Takayama and Isogai 2005). The maintenance of high diversity in gametophytic self-incompatibility (GSI) is easily explained by negative frequency-dependent selection, whereby individuals with a rare SI haplotype can fertilize more partners than individuals with a common SI haplotype. As a consequence, rare SI haplotypes are unlikely to be lost by drift, especially new SI haplotypes arising by mutation (Wright 1939). A major unsolved puzzle, though, is how new SI haplotypes appear, while it is a long-standing question (Lewis 1949;Fisher 1961). Some information exists about sequence changes affecting the specificity of the pollen or pistil protein, e.g., in the Solanum chacoense pistil gene (Matton et al. 1999) and ...

Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia

“…6b). Occasionally, self-compatible alleles are found in natural SC/SI-mixed populations of Petunia 29 , and could be fixed by selective forces such as mate limitation or automatic transmission advantage and by escaping rejection from all S-haplotypes in outcrossing 24,26,[30][31][32][33] . Although it has long hypothesized that recombination and/or gene conversion between different S-alleles could induce self-compatibility, no clear example has been found.…”

“…We note that the recognition rate from these models may be considered as minimum estimates, because different SLF types may tend to recognize different S-RNases since overlapping targets may not be favored by selection. The upper limit of the number of SLF types should be constrained by factors such as the strength of inbreeding depression and the proportion of self-pollen deposited on a stigma in natural population, birth-and-death rate of SLF types and effective population size [24][25][26] . These simple models suggest that we have identified the majority of the genetic components of this non-self recognition system.…”

Genetic architecture and balancing selection: the life and death of differentiated variants

“…However, the promotion of polymorphism by NFDS can be limited, because the advantage to rare alleles and the probability for a new allele to establish decrease as the number of alleles increases in the population (Gervais et al . ).…”

Breakdown of gametophytic self‐incompatibility in subdivided populations

“…As shown by Gervais et al. (), the diversification rate of SI alleles decreased as the number of SI alleles itself increased, so we expect that population subdivision, by keeping the local number of SI alleles at a low level, will actually increase the rate at which new SI alleles arise. Moreover, Gervais et al.…”

“…Moreover, Gervais et al. () also predicted that in most circumstances, the transient SC allele was expected to replace its ancestral copy, resulting in allelic turnover rather than diversification per se. It is possible that in a metapopulation, the replacement phenomenon may take place independently in different demes if they are sufficiently isolated, generating new alleles in different parts of the range.…”