Abstract
AbstractIn angiosperm self-incompatibility systems, pollen with an allele matching the pollen recipient at the self-incompatibility locus is rejected. Extreme allelic polymorphism is maintained by frequency-dependent selection favoring rare alleles. However, two challenges result in a chicken-or-egg problem for the spread of a new allele (a tightly linked haplotype in this case) under the widespread "collaborative non-self-recognition" mechanism. A novel pollen function mutation alone would merely grant compatibility with a nonexistent style function allele: a neutral change at best. A novel pistil function mutation alone could be fertilized only by pollen with a nonexistent pollen function allele: a deleterious change that would reduce seed set to zero. However, a pistil function mutation complementary to a previously neutral pollen mutation may spread if it restores self-incompatibility to a self-compatible intermediate. We show that novel haplotypes can also drive elimination of existing ones with fewer siring opportunities. We calculate relative probabilities of increase and collapse in haplotype number given the initial collection of incompatibility haplotypes and the population gene conversion rate. Expansion in haplotype number is possible when population gene conversion rate is large, but large contractions are likely otherwise. A Markov chain model derived from these expansion and collapse probabilities generates a stable haplotype number distribution in the realistic range of 10-40 under plausible parameters. However, smaller populations might lose many haplotypes beyond those lost by chance during bottlenecks.
Highlights
Self-incompatibility (SI), a common strategy by which plants ensure outcrossing, is a classic ex22 ample of extreme allelic polymorphism maintained by long-term balancing selection
While Bod’ová et al (2018) assumed the novel RNase was neutral, we model the case when this RNase suffers more intense pollen limitation than the rest of the population. How could such a stylar mutation, which increases pollen limitation, increase ovular fitness? We suggest that novel locks can be favored on self-compatible genetic backgrounds otherwise maintained by the balance of selection against self-compatibility and gene conversion of F-box alleles which restore self-compatibility
We developed a new model of ‘haplotypic rescue’ to estimate the relative probabilities of expansion and contraction in S-haplotype number, calculate the distribution of contraction magnitudes, and predict the long-term evolution of haplotype number
Summary
Self-incompatibility (SI), a common strategy by which plants ensure outcrossing, is a classic ex ample of extreme allelic polymorphism maintained by long-term balancing selection. Pollen with a rare specificity has an advantage because 30 it is less likely to encounter a pistil with a matching specificity and is less likely to be rejected This advantage of rarity results in balancing selection, which maintains polymorphism at 32 the S-locus by protecting S-locus alleles (S-alleles) from loss through drift (Wright 1939). We predict that, when many but not all S-alleles are fortuitously capable of fertilizing plants carrying the novel S-allele, the S-alleles lacking this capability are very likely to be lost This is because the alleles possessing this fortuitous compatibility eliminate their competitors when a novel specificity arises, thereby reducing the total number of surviving alleles. We predict that when allopatric populations exhibit large disparities in S-allele number, the population with the smaller number of S-alleles will harbor a stylar allele absent from and incompatible with pollen from the population with more S-alleles, while all S-alleles from the population with more S-alleles can be fertilized by pollen in the population with fewer S-alleles
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