Natural selection shapes nucleotide polymorphism across the genome of the nematode Caenorhabditis briggsae.
The combined actions of natural selection, mutation, and recombination forge the landscape of genetic variation across genomes. One frequently observed manifestation of these processes is a positive association between neutral genetic variation and local recombination rates. Two selective mechanisms and/or recombination-associated mutation (RAM) could generate this pattern, and the relative importance of these alternative possibilities remains unresolved generally. Here we quantify nucleotide differences within populations, between populations, and between species to test for genome-wide effects of selection and RAM in the partially selfing nematode Caenorhabditis briggsae. We find that nearly half of genome-wide variation in nucleotide polymorphism is explained by differences in local recombination rates. By quantifying divergence between several reproductively isolated lineages, we demonstrate that ancestral polymorphism generates a spurious signal of RAM for closely related lineages, with implications for analyses of humans and primates; RAM is, at most, a minor factor in C. briggsae. We conclude that the positive relation between nucleotide polymorphism and the rate of crossover represents the footprint of natural selection across the C. briggsae genome and demonstrate that background selection against deleterious mutations is sufficient to explain this pattern. Hill-Robertson interference also leaves a signature of more effective purifying selection in high-recombination regions of the genome. Finally, we identify an emerging contrast between widespread adaptive hitchhiking effects in species with large outcrossing populations (e.g., Drosophila) versus pervasive background selection effects on the genomes of organisms with self-fertilizing lifestyles and/or small population sizes (e.g., Caenorhabditis elegans, C. briggsae, Arabidopsis thaliana, Lycopersicon, human). These results illustrate how recombination, mutation, selection, and population history interact in important ways to shape molecular heterogeneity within and between genomes.
Department of Ecology & Evolutionary Biology and Centre for the Analysis of Genome Evolution and Function, University of Toronto, Toronto, Ontario M5S 3B2, Canada. asher.cutter@utoronto.ca
Asher D
AD
Cutter
Jae Young
JY
Choi
D000818:Animals; D001483:Base Sequence; D002107:Caenorhabditis / Q000235:genetics*; D014644:Genetic Variation; D049751:Genome, Helminth; D008969:Molecular Sequence Data; D009154:Mutation; D011110:Polymorphism, Genetic; D011995:Recombination, Genetic; D012641:Selection, Genetic