Trans‐Arctic dispersals and the evolution of a circumpolar marine fish species complex, the capelin (Mallotus villosus)

Abstract

Trans-Arctic dispersals and population and range expansions during the Pleistocene enhanced opportunities for evolutionary diversification and contributed to the process of speciation within the capelin, a northern marine-fish complex exhibiting a circumpolar distribution. Capelin is composed of four highly divergent and geographically discrete mitochondrial DNA (mtDNA) clades (609 bp; cytochrome b). Two clades occur in the North Atlantic, one associated with Canadian Atlantic waters, including Hudson Bay, and the second distributed from West Greenland to the Barents Sea. Two additional clades occur in the Arctic and northeast Pacific Oceans, representing the most recent divergence within the capelin phylogenetic tree. Judged from mtDNA diversity, capelin populations comprising all clades experienced at least one demographic and spatial reduction-expansion episode during recent Pleistocene glaciations that imprinted their molecular architecture. The large contemporary populations in the northeast Pacific and Arctic Oceans exhibited significant genetic structure whereas no such structure was detected in the equally extensive North Atlantic clades. All clades are characterized by one or two prevalent mtDNA haplotypes distributed over the entire range of the clade. Assuming a Pacific ancestor for capelin, we infer that capelin dispersed on two separate occasions to the North Atlantic. A more recent event resulted in the isolation of eastern Pacific and Arctic clades, with the Arctic clade positioned for a potential third Atlantic invasion, as revealed by the presence of this clade in the Labrador Sea. The Labrador Sea is a potential contact zone for three of the four capelin clades.

Biodiversity and phylogeography of Arctic marine fauna: insights from molecular tools

“…These authors note evidence of multiple trans-Arctic invasions which gave rise to increased genetic diversity in the North Atlantic. A similar scenario was proposed for the capelin (Mallotus villosus), an anadromous fish species with circum-Arctic distribution (Dodson et al 2007). This study identified a strong phylogeographic signal with four distinct clades that appear to have diverged 1-2 million years ago (Ma).…”

“…3 Map depicting proposed secondary contact zones and locations of Arctic glacial and periglacial marine refugia for various taxa: a clam Macoma balthica (Luttikhuizen et al 2003;Väinölä 2003;Nikula et al 2007); b jellyfish Obelia geniculata (Govindarajan et al 2005); c scale worm Harmothoe imbricata (this study); d red macroalga Phycodrys rubens (van Oppen et al 1995); e ice cream cone worm Pectinaria koreni (Jolly et al 2006); f barnacle Pollicipes pollicipes (Campo et al 2010); g clam Arctica islandica (Dahlgren et al 2000;Maggs et al 2008; but see Ingólfsson 2009); h brown macroalga Fucus serratus (Hoarau et al 2007); i capelin Mallotus villosus (Dodson et al 2007); j rainbow smelt Osmerus mordax (Bernatchez 1997); k sea stars Asterias spp. ; l hermit crab Pagurus longicarpus (Young et al 2002); m Arctic charr Salvelinus alpines (Brunner et al 2001); n whitefish Coregonus sp.…”

“…In both cases, when ice recedes and the isolated populations can again intermingle, increased allelic richness occurs in these secondary contact zones. Some divergent refugial lineages remain distinct despite secondary contact (e.g., Dodson et al 2007), but others interbreed, creating hybrid zones containing novel genetic diversity (e.g., Addison and Hart 2005;Riginos and Cunningham 2005;Strelkov et al 2007). …”

“…The fact that most cold-water species in the Bering Sea do not have ranges extending south to British Columbia also suggests that temperature could be an important factor generating these patterns. For example, Arctic lineages of the capelin fish (Mallotus villosus) occur in the Bering Sea but are genetically distinct from populations south of the Alaskan Peninsula (Dodson et al 2007). This cold-tolerant species also exhibits evidence of population subdivision between the North Pacific and the North Atlantic, and is thought to have experienced a population decline and southerly range contraction during the Pleistocene glaciation, followed by subsequent re-invasion of the Arctic from the Atlantic and Pacific.…”

Phylogeographic Estimates of Colonization of The Deep Atlantic by The Protobranch Bivalve Nucula Atacellana

“…The Trans−Arctic Exchange was a period of high Atlantic−Pacific con− nectivity after the opening of the Bering Strait in the Pliocene; this connectivity was impeded by subsequent Pleistocene glaciation, and has likely been reinvigo− rated in the warming following the Last Glacial Maximum (Vermeij 1991). There is genetic evidence for Atlantic−Pacific exchange via the Arctic Ocean in several taxa (vertebrates: Dodson et al 2007;Laakkonen et al 2013;invertebrates: Addi− son and Hart 2005;Govindarajan et al 2005;Carmack and Wassmann 2006;Nikula et al 2007;Rawson and Harper 2009).…”