When finding a mate is difficult, self-fertilization offers a tempting solution by increasing the number of offspring an individual can produce. But although “selfing” provides a stopgap solution when mates are scarce, it is frequently an evolutionary dead end; when environmental conditions change, species with high selfing rates seem prone to extinction. In an article in the June issue of GENETICS, Matthew Hartfield and Sylvain Glémin provide a glimpse into the mechanisms behind selfing’s shortcomings by examining how this reproductive strategy might limit the capacity of a species to adapt.  

A species adapts when a helpful gene variant spreads through the population by natural selection until it becomes the only version of the gene: the beneficial allele is then “fixed” in the population. To better understand this process in highly-selfing species, the researchers calculated the likelihood that a beneficial allele will fix in a species already undergoing selection at another locus.

In their mathematical model, the researchers considered two possible scenarios: that one helpful mutation may be lost if a second, even more beneficial mutation is already present at a different locus, and that an existing beneficial allele may be replaced by a second mutation that confers greater fitness. They found that in a highly-selfing species, the loss of a new helpful allele had a more powerful effect than did the replacement of the first allele. To interpret the finding, they turned to results from their own and others’ prior research, pointing out that selfers should have not only an initial increase in fecundity but should also benefit from escaping an effect known as Haldane’s sieve.

Haldane’s sieve predicts that in diploid organisms, a recessive helpful allele is less likely to fix than a dominant one. In outcrossing populations, the relative dearth of homozygotes means a rare recessive allele is less exposed to selection than a dominant one. But self-fertilization dramatically increases the number of homozygous sites, exposing recessive alleles to selection and relieving this limitation. Selfers should thus be able to reap more benefits from recessive mutations that are helpful but rare.

Despite this hypothetical advantage, the longer stretches of homozygosity in highly-selfing species also mean that the effective recombination rate is lower. In effect, the genome is less thoroughly shuffled between each generation. The researchers calculated that since these homozygous tracts stretch over longer genetic regions in highly selfing species, they increase the chance the second mutation will be lost. This is because the second allele must recombine to a genetic background carrying the first allele, which is less likely with high homozygosity. The results showed that this loss outweighs the advantages of sidestepping Haldane’s sieve, especially if new mutations are not as favorable as the one that gave rise to the first beneficial allele.

Once a species becomes self-fertilizing, it’s difficult to evolve back into an outcrossing species. Selfing, it seems, is a short-term and often perilous evolutionary path to take. The mutations contributing to self-fertilization become more and more prevalent simply because organisms bearing them make more copies of the mutated genome. To the detriment of the species as a whole, these selfish genes are difficult to dislodge from the species’ DNA. With the insights provided by this research, we are one step closer to understanding how selfing can ultimately cripple populations, one of the many examples of natural selection gone awry.

CITATION:

Hartfield, M.; Glémin, S. Limits to Adaptation in Partially Selfing Species.
GENETICS, 203(2), 959-974.
DOI: 10.1534/genetics.116.188821
http://www.genetics.org/content/203/2/959

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Nicole Haloupek is a freelance science writer and a recent graduate of UC Berkeley's molecular and cell biology PhD program.

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