This guest post is by Matthew Hartfield (@mathyhartfield) on his preprint (with Sylvain Glemin) “Limits to adaptation in partially selfing species”, available from bioRxiv here

Our paper “Limits to adaptation in partially selfing species” is now available from bioRxiv. This preprint is the result from a collaboration that has been sent back-and-forth across the Atlantic for well over a year, so we are pleased to see it online.

Haldane’s Sieve, after which this blog is named, is a theory pertaining to the role of dominance in adaptation, which was initially developed for outcrossing species and then shown to be absent in selfing species. When beneficial alleles initially appear in diploid individuals, they do so in heterozygote form (so only one of two alleles at the locus carry the advantageous type). Mathematically, these mutations have selective advantage 1 + hs where h is the degree of dominance, and s the selective advantage. Haldane’s Sieve states that recessive mutations (h 1/2), because selection is not efficient on heterozygotes if mutations are recessive. However, self-fertilising individuals are able to rapidly create homozygote forms of the mutant, increasing the efficacy of selection acting on them. Yet selfing also increases genetic drift, and hence the risk that these adaptations will go extinct by chance. Consequently, an extension of Haldane’s Sieve states that if the mutation is recessive (h 1/2).

This result holds for a single mutant in isolation. Yet mutants seldom act independently; they usually arise alongside other alleles in the genome, each of which has their own evolutionary outcomes. A known additional advantage of outcrossing is that, through recombining genomes from each parent, selected alleles can be moved from disadvantageous genomes to fitter backgrounds. For example, say an adaptive allele was present in a population, and a second adaptation arose at a nearby locus. If the second allele was not as strongly selected as the first, then it has to arise on the same genome as the initial adaptation. Otherwise it is likely to be lost as the less-fit genotype is replaced over time, a process known as selective interference. However, outcrossing can unite the two mutations into the same genome, so both can spread.

Despite these potential advantages of outcrossing, the effect of selective interference has not yet been investigated in the context of how facultative selfing influences the fixation of multiple beneficial alleles. Our model therefore aimed to determine how likely it is that secondary beneficial alleles can fix in the population, given an existing adaptation was already present, and reproduction involved a certain degree of self-fertilisation.

After working through the calculations, two subtle yet important twists on Haldane’s Sieve revealed themselves. First, due to the effects of selection interference, Haldane’s Sieve is likely to be reinforced in areas of low recombination. That is, recessive mutants are more likely to be lost in outcrossers (when compared to single-locus results), with similar losses for dominant mutations in self-fertilising organisms. Secondly, we also investigated a case where the second beneficial mutant could be reintroduced by recurrent mutation. In this case, selection interference can be very severe in selfers due to the lack of recombination. Hence some degree of outcrossing would be optimal to prevent these beneficial alleles from being repeatedly lost, even if they are recessive. In the most extreme case, complete outcrossing is best if secondary mutations only confer minor advantages.

In recent years, the role that selection interference plays in affecting mating system evolution is starting to become recognised. Our theoretical study is just one of many that elucidates how important outcrossing can be in augmenting the efficacy of selection. Our hope is that these studies will spur on further empirical work quantifying the rate of adaptation in species with different mating systems, to further unravel why species reproduce in vastly different ways.