Killer whale genomes reveal a complex history of recurrent admixture and vicariance

Abstract

Reconstruction of the demographic and evolutionary history of populations assuming a consensus tree‐like relationship can mask more complex scenarios, which are prevalent in nature. An emerging genomic toolset, which has been most comprehensively harnessed in the reconstruction of human evolutionary history, enables molecular ecologists to elucidate complex population histories. Killer whales have limited extrinsic barriers to dispersal and have radiated globally, and are therefore a good candidate model for the application of such tools. Here, we analyse a global data set of killer whale genomes in a rare attempt to elucidate global population structure in a nonhuman species. We identify a pattern of genetic homogenisation at lower latitudes and the greatest differentiation at high latitudes, even between currently sympatric lineages. The processes underlying the major axis of structure include high drift at the edge of species' range, likely associated with founder effects and allelic surfing during postglacial range expansion. Divergence between Antarctic and non‐Antarctic lineages is further driven by ancestry segments with up to four‐fold older coalescence time than the genome‐wide average; relicts of a previous vicariance during an earlier glacial cycle. Our study further underpins that episodic gene flow is ubiquitous in natural populations, and can occur across great distances and after substantial periods of isolation between populations. Thus, understanding the evolutionary history of a species requires comprehensive geographic sampling and genome‐wide data to sample the variation in ancestry within individuals.

False‐negative detections from environmental DNA collected in the presence of large numbers of killer whales (Orcinus orca)

“…Furthermore, comparing all reads in the enriched eDNA libraries that mapped to the killer whale genome to a global dataset(Foote et al 2019) found no shared SNPs. The successful amplification of the serial dilution of the positive control of killer whale DNA indicates that the ambiguous or negative detections of killer whale DNA from the seawater samples were not due to qPCR failure.…”

Excavating ghost footprints and tangled trees from modern genomes

“…A particularly intriguing result from Foote et al’s () paper is the detection of genomic tracts introgressed from a now extinct (or otherwise unsampled) deeply divergent “ghost” population into Antarctic killer whale morphs. These archaic ancestry segments have up to four‐fold older coalescence time with low‐latitude populations than the genome‐wide average and thus probably originated from a lineage that split off to colonize southern habitat that became available during an earlier interglacial period (>200,000 years ago), while the rest of the genome suggests the current Antarctic group split off during the most recent glacial cycle (~60,000 years ago).…”

“…Foote et al () infer that up to ~20% of the genome in Antarctic killer whales potentially originated from archaic admixture. The length of these archaic tracts and the density of private alleles within them provide important insights into the time since the introgression took place and the degree of divergence between the introgressing and receiving lineages (Figure ; Racimo et al, ).…”

“…As recombination will break down linkage among private alleles over time, longer archaic tracts indicate more recent introgression (as there has been less time for recombination to break them down), while shorter tracts suggest more ancient admixture. Foote et al () find that the introgressed archaic tracts in Antarctic killer whales are about an order of magnitude shorter than those seen non‐African humans and suggest that they are more likely to result from ancestral population structure and ancient admixture than recent introgression (Figure ).…”

“…Foote et al’s () novel insights into the evolutionary history of killer whales were underpinned by two key aspects of their data set: (a) having fully resequenced genomes that revealed multimodal patterns of ancestry within individuals and (b) having global coverage in sampling that together provide a comprehensive overview of the current diversity within the species and illustrate that gene flow has occurred across great distances and after long periods of isolation between populations. So far, only a few similar global whole genome data sets exist for nonmodel species, examples including the brown rat (Puckett & Munshi‐South, ) and yellowfin tuna (Barth, Damerau, Matschiner, Jentoft, & Hanel, ).…”