Coastal Elites: Recurrent Trans‐Arctic Migration and Vicariance in a Cosmopolitan Sea Slug Driven by Pleistocene Glacial Cycles

Abstract

Many coastal marine species experienced Pleistocene gene flow between the North Pacific and Atlantic. Understanding historical connectivity between ocean basins should aid in predicting how regional faunas will respond to recent warming that has intensified trans‐Arctic dispersal. Wetland fauna of the Northwestern Atlantic may have survived in estuarine refugia throughout glacial cycles, or recolonised from the southern coast, North Pacific or Northeastern Atlantic. Here, we used multilocus genetic markers and historical climate data to investigate lineage distribution and connectivity among populations of the nominally cosmopolitan sea slug Alderia modesta , sampled from mudflats on both coasts of the North Pacific and North Atlantic. Mitochondrial DNA clades from European and North American populations were deeply divergent and reciprocally monophyletic; differences at seven polymorphic nuclear loci indicated prolonged absence of trans‐Atlantic gene flow. A Pacific ancestor likely first colonised the Atlantic during the marine biotic interchange of the middle Pliocene ~3.5 Ma. Both mtDNA phylogenetics and nuclear genotype assignments support repeated trans‐Arctic colonisation of the Northwestern Atlantic from the Pacific during inter‐glacial cycles; no gene flow was evident since the last glacial maximum, however. Time‐calibrated coalescent phylogenies, Bayesian skyline plots and haplotype networks all indicated recent population expansions in the Pacific and Europe, but not Northwestern Atlantic. In both the Pacific and Northwestern Atlantic, older lineages persisted in patchy refugia north of glacial margins, while a derived clade of Pacific haplotypes indicates northward post‐LGM expansion. The biogeographical history of Alderia contrasts with rocky‐shore taxa that were largely extirpated by glacial advance and recolonised from refugia following the last glacial maximum. Based on molecular differences and distinctions in radular and penial stylet morphology, we resurrect the name Alderia harvardiensis Gould 1870 for Alderia from the Northwestern Atlantic and North Pacific; A. modesta refers exclusively to European slugs.

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