Origins of the Greenland shark (Somniosus microcephalus): Impacts of ice-olation and introgression

Abstract

Herein, we use genetic data from 277 sleeper sharks to perform coalescent-based modeling to test the hypothesis of early Quaternary emergence of the Greenland shark (Somniosus microcephalus) from ancestral sleeper sharks in the Canadian Arctic-Subarctic region. Our results show that morphologically cryptic somniosids S. microcephalus and Somniosus pacificus can be genetically distinguished using combined mitochondrial and nuclear DNA markers. Our data confirm the presence of genetically admixed individuals in the Canadian Arctic and sub-Arctic, and temperate Eastern Atlantic regions, suggesting introgressive hybridization upon secondary contact following the initial species divergence. Conservative substitution rates fitted to an Isolation with Migration (IM) model indicate a likely species divergence time of 2.34 Ma, using the mitochondrial sequence DNA, which in conjunction with the geographic distribution of admixtures and Pacific signatures likely indicates speciation associated with processes other than the closing of the Isthmus of Panama. This time span coincides with further planetary cooling in the early Quaternary period followed by the onset of oscillating glacial-interglacial cycles. We propose that the initial S. microcephalus-S. pacificus split, and subsequent hybridization events, were likely associated with the onset of Pleistocene glacial oscillations, whereby fluctuating sea levels constrained connectivity among Arctic oceanic basins, Arctic marginal seas, and the North Atlantic Ocean. Our data demonstrates support for the evolutionary consequences of oscillatory vicariance via transient oceanic isolation with subsequent secondary contact associated with fluctuating sea levels throughout the Quaternary period-which may serve as a model for the origins of Arctic marine fauna on a broad taxonomic scale.

Keywords: Greenland shark; Somniosus microcephalus; elasmobranch; interspecific gene flow; introgressive hybridization; isolation with migration.

Figure 1

Sampling locations of somniosid sharks in the Arctic, North Atlantic Ocean, and North Pacific: Somniosus microcephalus (green); Somniosus pacificus (blue) and; cytonuclear discordant individuals (yellow). Numbers inside circles are sample sizes

Figure 2

Haplotype variation at cyt b, ITS2, and RAG1 loci among sampled somniosids as depicted through a 95% statistically parsimony network. For cyt b, the size of the circles is proportional to the frequency of each haplotype in the 277 individual dataset, ITS2 and RAG1 haplotypes are not scaled for frequency. Haplotype numbers correspond to Table S1, white numbers are previously reported haplotypes, black numbers are novel haplotypes to this study. Individuals identified in the field as Somniosus microcephalus possess haplotypes in green, while those identified as Somniosus pacificus possess blue haplotypes

Figure 3

Genetic indicators of population expansion using the mtDNA cyt b data for Somniosus microcephalus individuals (including hybrids). (a) Mismatch distribution of pairwise nucleotide differences (dark gray columns) with expected curve fit to a model of population expansion (gray line); (b) Bayesian skyline plot for S. microcephalus using the HKY+I nucleotide substitution model

Figure 4

Marginal posterior probability density distributions of species‐split time (t ₀; panel a), migration rates (m; panel b) and long‐term effective population size (N _e; panel c) as estimated in IMa2 using mtDNA (cyt b). Migration directions are presented forward in time. PPD, posterior probability density