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Widespread genetic incompatibility in C. elegans maintained by balancing selection.

ABSTRACT: Natural selection is expected to eliminate genetic incompatibilities from interbreeding populations. We have discovered a globally distributed incompatibility in the primarily selfing species Caenorhabditis elegans that has been maintained despite its negative consequences for fitness. Embryos homozygous for a naturally occurring deletion of the zygotically acting gene zeel-1 arrest if their sperm parent carries an incompatible allele of a second, paternal-effect locus, peel-1. The two interacting loci are tightly linked, with incompatible alleles occurring in linkage disequilibrium in two common haplotypes. These haplotypes exhibit elevated sequence divergence, and population genetic analyses of this region indicate that natural selection is preserving both haplotypes in the population. Our data suggest that long-term maintenance of a balanced polymorphism has permitted the incompatibility to persist despite gene flow across the rest of the genome.

SUBMITTER: Seidel HS

PROVIDER: S-EPMC2421010 | biostudies-literature | 2008 Feb

REPOSITORIES: biostudies-literature

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Widespread genetic incompatibility in C. elegans maintained by balancing selection.

Seidel Hannah S HS Rockman Matthew V MV Kruglyak Leonid L

Science (New York, N.Y.) 20080110 5863

Natural selection is expected to eliminate genetic incompatibilities from interbreeding populations. We have discovered a globally distributed incompatibility in the primarily selfing species Caenorhabditis elegans that has been maintained despite its negative consequences for fitness. Embryos homozygous for a naturally occurring deletion of the zygotically acting gene zeel-1 arrest if their sperm parent carries an incompatible allele of a second, paternal-effect locus, peel-1. The two interacti ...[more]

PMID: 18187622

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Project description:Arbutus unedo L. is an evergreen shrub with a circum-Mediterranean distribution that also reaches the Eurosiberian region in northern Iberia, Atlantic France, and a disjunct population in southern Ireland. Due to the variety of climatic conditions across its distribution range, the populations of A. unedo were expected to display local adaptation. Conversely, common garden experiments revealed that diverse genotypes from a range of provenances produce similar phenotypes through adaptive plasticity, suggesting the action of stabilizing selection across its climatically heterogeneous range. Nonetheless, since a uniform response might also result from extensive gene flow, we have inferred the population structure of A. unedo and assessed whether its extended and largely one-dimensional range influences gene flow with the help of AFLP genotypes for 491 individuals from 19 populations covering the whole range of the species. As we had anticipated, gene flow is restricted in A. unedo, providing further support to the hypothesis that stabilizing selection is the most likely explanation for the homogeneous phenotypes along the range. The Euro-Siberian populations were not particularly isolated from the Mediterranean. Instead, there was a distinct genetic divide between the populations around the Mediterranean Sea and those sampled along Atlantic coasts from northern Africa up to Ireland. This genetic structure suggests the action of historic rather than biogeographic factors as it seems consistent with a scenario of independent glacial refugia in the Atlantic and Mediterranean portions of the range of A. unedo. Genetic exchange was likewise restricted within each set of populations. Nevertheless, isolation-by-distance (IBD) was stronger, and F ST increased faster with distance, along the Atlantic, suggesting that gene flow might be larger among Mediterranean populations. Genetic diversity was significantly lower in NW Iberia and Ireland than in other populations whereas Ireland was more closely related to populations in NW Iberia than to a population in Atlantic France, suggesting a postglacial stepping-stone colonization of the Atlantic coast. Altogether, our results show that stabilizing selection is able to homogenize the phenotypic response even when population structure is strong, gene flow is constrained, and the phylogeographic past is complex.

Dataset Information

Widespread genetic incompatibility in C. elegans maintained by balancing selection.

Publications

Widespread genetic incompatibility in C. elegans maintained by balancing selection.

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