Evolution of Population Structure in a Highly Social Top Predator, the Killer Whale

Abstract

Intraspecific resource partitioning and social affiliations both have the potential to structure populations, though it is rarely possible to directly assess the impact of these mechanisms on genetic diversity and population divergence. Here, we address this for killer whales (Orcinus orca), which specialize on prey species and hunting strategy and have long-term social affiliations involving both males and females. We used genetic markers to assess the structure and demographic history of regional populations and test the hypothesis that known foraging specializations and matrifocal sociality contributed significantly to the evolution of population structure. We find genetic structure in sympatry between populations of foraging specialists (ecotypes) and evidence for isolation by distance within an ecotype. Fitting of an isolation with migration model suggested ongoing, low-level migration between regional populations (within and between ecotypes) and small effective sizes for extant local populations. The founding of local populations by matrifocal social groups was indicated by the pattern of fixed mtDNA haplotypes in regional populations. Simulations indicate that this occurred within the last 20,000 years (after the last glacial maximum). Our data indicate a key role for social and foraging behavior in the evolution of genetic structure among conspecific populations of the killer whale.

Patterns of population structure at microsatellite and mitochondrial DNA markers in the franciscana dolphin (Pontoporia blainvillei)

“…Regarding sex‐biased dispersal, although mammals often exhibit a pattern of male‐biased dispersal and female philopatry (Greenwood, 1980) and sex‐biased dispersal is common in other cetacean species (e.g., Escorza Treviño & Dizon, 2000; Hoelzel et al., 2007; Krützen, Sherwin, Berggren, & Gales, 2004; Möller & Beheregaray, 2004), our results did not detect a bias in dispersal between the sexes (Figure 3). Although this result should be regarded with caution since the ability of the tests performed to detect the bias in dispersal is limited mainly due to the lack of extreme bias in dispersal, the low to moderate dispersal estimates, and the number of loci and samples analyzed (Goudet et al., 2002), previous franciscana dolphin studies also found a lack of sex‐biased dispersal (Costa Urrutia et al., 2012; Méndez et al., 2008), supporting our findings.…”

“…In accordance with a previous mtDNA control region analysis (Gariboldi et al., 2015), high rates of gene flow (Table 3 and mtDNA results) and a lack of genetic differentiation between CL and NC were observed based on the microsatellite loci and mtDNA analyses (Table 2), suggesting that individuals from both localities form a panmictic population. This may be due to close geographic proximity between localities which may entail similar resource use, as it was previously suggested for this species (Costa Urrutia et al., 2012; Gariboldi et al., 2015; Méndez et al., 2008; Méndez, Rosenbaum, Subramaniam, et al., 2010) and other cetaceans (Fullard et al., 2000; Hoelzel et al., 2007; Natoli et al., 2005). In fact, individuals from NC and CL were found to fed primary on Loligo sanpaulensis (Paso Viola, 2014; Paso Viola et al., 2014).…”

“…Additionally, although the genetic population structure of many species may be characterized by a pattern of IBD (e.g., Ansmann, Parra, Lanyon, & Seddon, 2012; Hoelzel et al., 2007; Natoli et al., 2005), we did not observe a significant correlation between genetic differentiation and geographic distance among populations (Figure 4). If equilibrium between the loss of alleles due to genetic drift and their replacement by gene flow between populations exists, the genetic distance between populations will increase with geographic distance due to the changing influence of gene flow and genetic drift as populations become more or less geographically separated (Hutchison & Templeton, 1999).…”

Post-glacial habitat release and incipient speciation in the genus Delphinus

“…In marine fishes, both niche partitioning and mate choice were affected by divergent selection on characters that resulted in sympatric speciation within the genus Hexagrammos (Crow et al, 2010). Among cetacean species, both killer whales (Orcinus orca) and bottlenose dolphins (Tursiops truncatus) show genetic differentiation among populations correlated to foraging specializations or habitat dependence (O. orca, Hoelzel et al, 2007;Moura et al, 2014;T. truncatus, Hoelzel et al, 1998;Natoli et al, 2005;Segura et al, 2006;CharltonRobb et al, 2011;Moura et al, 2013).…”

Resource specialisation and the divergence of killer whale populations

“…Foote and Morin (2015) suggest that the co-occurrence of populations in the same ocean doesn't necessarily imply that they differentiated in sympatry, which is clearly true. However, as Moura et al (2015) and others (for example, Hoelzel et al, 1998Hoelzel et al, , 2007 have discussed, it is the life history and behaviour of killer whales that suggest the potential for differentiation in sympatry. Although the proximity of resources brings killer whale pods into sympatry, the differential pattern of spatial and temporal habitat use, as well as fidelity to pods that forage by similar learned methods, could serve to isolate resource specialist communities reproductively.…”