Genetics, Gene Flow, and Glaciation: The Case of the South American Limpet Nacella mytilina

Abstract

Glacial episodes of the Quaternary, and particularly the Last Glacial Maximum (LGM) drastically altered the distribution of the Southern-Hemisphere biota, principally at higher latitudes. The irregular coastline of Patagonia expanding for more than 84.000 km constitutes a remarkable area to evaluate the effect of Quaternary landscape and seascape shifts over the demography of near-shore marine benthic organisms. Few studies describing the bio-geographic responses of marine species to the LGM have been conducted in Patagonia, but existing data from coastal marine species have demonstrated marked genetic signatures of post-LGM recolonization and expansion. The kelp-dweller limpet Nacella mytilina is broadly distributed along the southern tip of South America and at the Falkland/Malvinas Islands. Considering its distribution, abundance, and narrow bathymetry, N. mytilina represents an appropriate model to infer how historical and contemporary processes affected the distribution of intraspecific genetic diversity and structure along the southern tip of South America. At the same time, it will be possible to determine how life history traits and the ecology of the species are responsible for the current pattern of gene flow and connectivity across the study area. We conducted phylogeographic and demographic inference analyses in N. mytilina from 12 localities along Pacific Patagonia (PP) and one population from the Falkland/Malvinas Islands (FI). Analyses of the mitochondrial gene COI in 300 individuals of N. mytilina revealed low levels of genetic polymorphism and the absence of genetic differentiation along PP. In contrast, FI showed a strong and significant differentiation from Pacific Patagonian populations. Higher levels of genetic diversity were also recorded in the FI population, together with a more expanded genealogy supporting the hypothesis of glacial persistence of the species in these islands. Haplotype genealogy, and mismatch analyses in the FI population recognized an older and more complex demographic history than in PP. Demographic reconstructions along PP suggest a post-LGM expansion process (7.5 ka), also supported by neutrality tests, mismatch distribution and maximum parsimony haplotype genealogies. Migration rate estimations showed evidence of asymmetrical gene flow from PP to FI. The absence of genetic differentiation, the presence of a single dominant haplotype, high estimated migration rates, and marked signal of recent demographic growth, support the hypothesis of rapid post-glacial expansion in N. mytilina along PP. This expansion could have been sustained by larval and rafting-mediated dispersal of adults from northernmost populations following the Cape Horn Current System. Marked genetic differentiation between PP and FI could be explained through differences in their respective glacial histories. During the LGM, Pacific Patagonia (PP) was almost fully covered by the Patagonian Ice Sheet, while sheet coverage in the FI ice was restricted to small cirques and valleys. As previously recorded in the sister-species N. magellanica, the FI rather than represent a classical glacial refugium for N. mytilina, seems to represent a sink area and/or a secondary contact zone. Accordingly, historical and contemporary processes, contrasting glacial histories between the analyzed sectors, as well as life history traits constitute the main factors explaining the current biogeographical patterns of most shallow Patagonian marine benthic organisms