Abstract

The evolution of diversity in the marine ecosystem is poorly understood, given the relatively high potential for connectivity, especially for highly mobile species such as whales and dolphins. The killer whale (Orcinus orca) has a worldwide distribution, and individual social groups travel over a wide geographic range. Even so, regional populations have been shown to be genetically differentiated, including among different foraging specialists (ecotypes) in sympatry. Given the strong matrifocal social structure of this species together with strong resource specializations, understanding the process of differentiation will require an understanding of the relative importance of both genetic drift and local adaptation. Here we provide a high-resolution analysis based on nuclear single-nucleotide polymorphic markers and inference about differentiation at both neutral loci and those potentially under selection. We find that all population comparisons, within or among foraging ecotypes, show significant differentiation, including populations in parapatry and sympatry. Loci putatively under selection show a different pattern of structure compared to neutral loci and are associated with gene ontology terms reflecting physiologically relevant functions (e.g. related to digestion). The pattern of differentiation for one ecotype in the North Pacific suggests local adaptation and shows some fixed differences among sympatric ecotypes. We suggest that differential habitat use and resource specializations have promoted sufficient isolation to allow differential evolution at neutral and functional loci, but that the process is recent and dependent on both selection and drift.

Highlights

  • The scarcity of strong geographical barriers and the large dispersal abilities of many marine species have led to suggestions that selection is a dominant mechanism driving population differentiation (Naciri et al 1999; Bierne et al 2003)

  • When we compared against the restriction-site-associated DNA (RAD) list, we found that there is lower power as expected, and some gene ontology (GO) terms associated with the same subset of genes are identified as potentially overrepresented, the resolution is too low for strong inference

  • Earlier studies have proposed everything from relatively recent (Holocene) population differentiation (e.g. Hoelzel et al 2007) to species-level differences established in the middle Pleistocene (Morin et al 2010), and we do not propose to fully resolve the question of alpha taxonomy here

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Summary

Introduction

The scarcity of strong geographical barriers and the large dispersal abilities of many marine species have led to suggestions that selection is a dominant mechanism driving population differentiation (Naciri et al 1999; Bierne et al 2003). This view has been supported by studies showing genetic structure associated with environmental and physiological differences (Ruzzante et al 1996; Beheregaray & Sunnucks 2001; Jorgensen et al 2005; Palumbi & Lessios 2005; Atarhouch et al 2007; White et al 2010; Bowen et al 2013). This may emphasize the importance of species-specific resource requirements and specializations towards the evolution of habitat dependence, philopatry and population differentiation (Yurk et al 2002; Natoli et al 2006; Hoelzel et al 2007; Moura et al 2013a)

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