A Single Interacting Species Leads to Widespread Parallel Evolution of the Stickleback Genome

Abstract

Biotic interactions are potent, widespread causes of natural selection and divergent phenotypic evolution and can lead to genetic differentiation with gene flow among wild populations ("isolation by ecology") [1-4]. Biotic selection has been predicted to act onmore genes than abiotic selection thereby drivinggreater adaptation [5]. However, difficulties in isolating the genome-wide effect of single biotic agents of selection have limited our ability to identify and quantify the number and type of genetic regions responding to biotic selection [6-9]. We identified geographically interspersed lakes in which threespine stickleback fish (Gasterosteus aculeatus) have repeatedly adapted to the presence or absence of a single member of the ecological community, prickly sculpin (Cottus asper), a fish that is both a competitor and a predator of the stickleback [10]. Whole-genome sequencing revealed that sculpin presence or absence accounted for the majority of genetic divergence among stickleback populations, more so than geography. The major axis of genomic variation within and between the two lake types was correlated with multiple traits, indicating parallel natural selection across a gradient of biotic environments. A large proportion of the genome-about 1.8%, encompassing more than 600 genes-differentiated stickleback from the two biotic environments. Divergence occurred in 141 discrete genomic clumps located mainly in regions of low recombination, suggesting that genes brought to lakes by the colonizing ancestral population often evolved together in linked blocks. Strong selection and a wealth of standing genetic variation explain how a single member of the biotic community can have such a rapid and profound evolutionary impact.