Genome-culture coevolution promotes rapid divergence of killer whale ecotypes.
Foote ADDepartment of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, Uppsala SE-752 36, Sweden.
Vijay NDepartment of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, Uppsala SE-752 36, Sweden.
Ávila-Arcos MCCentre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Volgade 5-7, Copenhagen K 1350, Denmark.
Baird RWCascadia Research, 4th Avenue, Olympia, Washington 98501, USA.
Durban JWMarine Mammal and Turtle Division, Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanographic and Atmospheric Administration, 8901 La Jolla Shores Drive, La Jolla, California 92037, USA.
Fumagalli MDepartment of Genetics, Evolution, and Environment, UCL Genetics Institute, University College London, London WC1E 6BT, UK.
Gibbs RADepartment of Molecular and Human Genetics, Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.
Hanson MBNorthwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 2725 Montlake Boulevard East, Seattle, Washington 98112, USA.
Korneliussen TSCentre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Volgade 5-7, Copenhagen K 1350, Denmark.
Martin MDCentre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Volgade 5-7, Copenhagen K 1350, Denmark.
Robertson KMMarine Mammal and Turtle Division, Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanographic and Atmospheric Administration, 8901 La Jolla Shores Drive, La Jolla, California 92037, USA.
Sousa VCComputational and Molecular Population Genetics Laboratory, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, Bern 3012, Switzerland.
Vieira FGCentre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Volgade 5-7, Copenhagen K 1350, Denmark.
Vinař TFaculty of Mathematics, Physics and Informatics, Comenius University, Mlynska Dolina, Bratislava 84248, Slovakia.
Wade PNational Marine Mammal Laboratory, Alaska Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 7600 Sand Point Way NE, Seattle, Washington 98115, USA.
Worley KCDepartment of Molecular and Human Genetics, Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.
Excoffier LComputational and Molecular Population Genetics Laboratory, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, Bern 3012, Switzerland.
Morin PAMarine Mammal and Turtle Division, Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanographic and Atmospheric Administration, 8901 La Jolla Shores Drive, La Jolla, California 92037, USA.
Gilbert MTPCentre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Volgade 5-7, Copenhagen K 1350, Denmark.
Wolf JBWDepartment of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, Uppsala SE-752 36, Sweden.
English
Analysing population genomic data from killer whale ecotypes, which we estimate have globally radiated within less than 250,000 years, we show that genetic structuring including the segregation of potentially functional alleles is associated with socially inherited ecological niche. Reconstruction of ancestral demographic history revealed bottlenecks during founder events, likely promoting ecological divergence and genetic drift resulting in a wide range of genome-wide differentiation between pairs of allopatric and sympatric ecotypes. Functional enrichment analyses provided evidence for regional genomic divergence associated with habitat, dietary preferences and post-zygotic reproductive isolation. Our findings are consistent with expansion of small founder groups into novel niches by an initial plastic behavioural response, perpetuated by social learning imposing an altered natural selection regime. The study constitutes an important step towards an understanding of the complex interaction between demographic history, culture, ecological adaptation and evolution at the genomic level.