Genome-culture coevolution promotes rapid divergence of killer whale ecotypes

Andrew D Foote,M Thomas P Gilbert,Matteo Fumagalli,Kim C Worley,Tomáš Vinař,Laurent Excoffier,Nagarjun Vijay,Robin W Baird,John W Durban,Kelly M Robertson,Michael D Martin,Phillip A Morin,M Bradley Hanson,Richard A Gibbs,Filipe Garrett Vieira ,Vítor C Sousa ,Thorfinn Sand Korneliussen ,Paul R Wade ,María C Ávila‐Arcos ,Jochen B W Wolf

doi:10.1038/ncomms11693

Abstract

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.

Highlights

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
The dataset incorporated individuals each of the transient and resident ecotypes that occur in sympatry in the North Pacific; and from Antarctic waters, 7 ndividuals of a large mammal-eating form, individuals of a partially sympatric, smaller form which feeds on penguins, and 10 individuals of the smallest form of killer whale, which feeds on fish (Fig. 1)
A total of 2,577 million reads uniquely mapped to the 2.4-Gbp killer whale reference genome[16] (Supplementary Fig. 1) for which a chromosomal assembly was generated for this study, so that approximately 50% of the autosomal regions of each individual were sequenced at Z2 Â coverage (Supplementary Table 1)

Summary

Introduction

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. By perpetuating exposure to a novel environment, stable cultural transmission of behaviour can provide an opportunity for natural selection to act on adaptive genomic variation. Several studies have argued that behavioural differences among killer whale ecotypes are examples of culture in this broader sense of the term[13,14] This behavioural variation among ecotypes likely results from ecological, genetic and cultural variation and the interaction between them, rather than a single process explaining all behavioural variance[15]. Offer a prime example of how behavioural innovation perpetuated by cultural transmission may have enabled access to novel ecological conditions with altered selection regimes, and provide an excellent study system for understanding the interaction between ecological and behavioural variation, and genome-level evolution

Methods

Results

Conclusion