American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

“Experimental hybridization studies suggest that pleiotropic alleles commonly underlie adaptive divergence between natural population”

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Ken A. Thompson (Aug 2020)

A synthesis of experimental hybridization studies suggests highly pleiotropic alleles are often used for adaptation

Read the Article (Just Accepted)

A snippet of the R script underlying the analysis, overlaid above an image of səl̓ilw̓ət (Burrard Inlet) and Lighthouse Park, near Vancouver, BC.
A snippet of the R script underlying the analysis, overlaid above an image of səl̓ilw̓ət (Burrard Inlet) and Lighthouse Park, near Vancouver, BC.

A longstanding and fundamental mystery in evolutionary biology surrounds the question of whether the mutation of a single gene tends to affect few or many traits at a time. For example, do mutations that affect how large an organism grows also tend to affect other traits like behavior or pigmentation? A new article by Ken Thompson, a Ph.D. candidate at the University of British Columbia, appearing in The American Naturalist, sheds new light on this unresolved question.

Understanding the extent of pleiotropy—when a single gene affects many traits—is important because it tells us about the conditions under which evolution proceeds. In addition, knowledge of pleiotropy’s extent is critically important for applied studies of genome editing or genetic engineering.

Normally, testing for pleiotropy is extremely labor-intensive. For decades, scientists have been inducing single mutations into hundreds or thousands of plants or animals to study the number of traits that are changed.

In his article in The American Naturalist, Thompson leverages a prediction from evolutionary theory—based in simple geometric principles of genetics developed by Ronald Fisher in the 1930s—to conduct an indirect test of whether pleiotropy is widespread. Using data generated from experimental hybridization studies of naturally occurring plants and animals—where different species or subspecies are crossed in the lab—Thompson tests a specific prediction that only holds when genes are pleiotropic.

The results of his analysis provide evidence that the mutations that cause evolution in nature typically have a high degree of pleiotropy. This work could have implications for gene-editing studies by making it clear that simple genetic changes might often affect many more traits than just the one where changes are desired.


Abstract

The alleles used for adaptation can pleiotropically affect traits under stabilizing selection. The fixation of alleles with deleterious pleiotropic side-effects causes compensatory alleles to be favoured by selection. Such compensatory alleles might segregate in interpopulation hybrids, resulting in segregation variance for traits where parents have indistinguishable phenotypes. If adaptation typically involves pleiotropy and compensation, then the segregation variance for traits under stabilizing selection is expected to increase with the magnitude of adaptive phenotypic divergence between parents. This prediction has not been tested empirically, and I gathered data from experimental hybridization studies to evaluate it. I found that pairs of parents which are more phenotypically divergent beget hybrids with more segregation variance in traits for which the parents are statistically indistinguishable. This result suggests that adaptive divergence between pairs of natural populations proceeds via pleiotropy and compensation, and that deleterious transgressive segregation variance accumulates systematically as populations diverge.