Towards a model of postglacial biogeography in shallow marine species along the Patagonian Province: lessons from the limpet Nacella magellanica (Gmelin, 1791)

Abstract

BackgroundPatagonia extends for more than 84,000 km of irregular coasts is an area especially apt to evaluate how historic and contemporary processes influence the distribution and connectivity of shallow marine benthic organisms. The true limpet Nacella magellanica has a wide distribution in this province and represents a suitable model to infer the Quaternary glacial legacy on marine benthic organisms. This species inhabits ice-free rocky ecosystems, has a narrow bathymetric range and consequently should have been severely affected by recurrent glacial cycles during the Quaternary. We performed phylogeographic and demographic analyses of N. magellanica from 14 localities along its distribution in Pacific Patagonia, Atlantic Patagonia, and the Falkland/Malvinas Islands.ResultsMitochondrial (COI) DNA analyses of 357 individuals of N. magellanica revealed an absence of genetic differentiation in the species with a single genetic unit along Pacific Patagonia. However, we detected significant genetic differences among three main groups named Pacific Patagonia, Atlantic Patagonia and Falkland/Malvinas Islands. Migration rate estimations indicated asymmetrical gene flow, primarily from Pacific Patagonia to Atlantic Patagonia (Nem=2.21) and the Falkland/Malvinas Islands (Nem=16.6). Demographic reconstruction in Pacific Patagonia suggests a recent recolonization process (< 10 ka) supported by neutrality tests, mismatch distribution and the median-joining haplotype genealogy.ConclusionsAbsence of genetic structure, a single dominant haplotype, lack of correlation between geographic and genetic distance, high estimated migration rates and the signal of recent demographic growth represent a large body of evidence supporting the hypothesis of rapid postglacial expansion in this species in Pacific Patagonia. This expansion could have been sustained by larval dispersal following the main current system in this area. Lower levels of genetic diversity in inland sea areas suggest that fjords and channels represent the areas most recently colonized by the species. Hence recolonization seems to follow a west to east direction to areas that were progressively deglaciated. Significant genetic differences among Pacific, Atlantic and Falkland/Malvinas Islands populations may be also explained through disparities in their respective glaciological and geological histories. The Falkland/Malvinas Islands, more than representing a glacial refugium for the species, seems to constitute a sink area considering the strong asymmetric gene flow detected from Pacific to Atlantic sectors. These results suggest that historical and contemporary processes represent the main factors shaping the modern biogeography of most shallow marine benthic invertebrates inhabiting the Patagonian Province.

Deep genetic divergence between austral populations of the red alga Gigartina skottsbergii reveals a cryptic species endemic to the Antarctic continent

“…Similarly, the overall low genetic diversity and the 382 presence of the same common haplotype C1 in every population from the Chilean coast to the 383 Falkland Islands seems to support the hypothesis of persistence in a single glacial refugium 384 followed by a massive demographic expansion over 2500 km. Such a pattern of genetic 385 homogeneity over a broad geographical range has usually been related to high dispersal 386 potential (Bortolotto et al 2011;González-Wevar et al 2012b). The scenario of rapid 387 recolonization leading to the presence of only one haplotype over thousands of kilometers of 388 coast is, however, difficult to envision for G. skottsbergii.…”

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

“…mytilina are lower than those recorded in tropical and temperate patellogastropods [94,95] and in other Patagonian nacellid limpets [20,24,25]. In fact, levels of genetic polymorphism in N .…”

“…The first one flows eastward to the South Georgia [122,123] while the second one flows northwards on both sides of the Falkland/Malvinas Islands up north to Rio de la Plata Province (30°S) following the continental shelf margin [135,136]. As previously proposed for another Patagonian nacellid limpet [25], FI seems to represent a sink area, as well as a secondary contact zone where endemic haplotypes that survived the LGM are mixed together with recently arrived PP ones. Future studies in Patagonian near-shore marine benthic invertebrates will require to integrate mtDNA/nucDNA genes together with fast-evolving markers (microsatellites, RADseq, SNPs) to further understand the role of the Quaternary cycles over the current patterns of genetic diversity, structure and connectivity.…”

“…At the same time, several studies have demonstrated that kelp-specialized Subantarctic invertebrates show very low levels of genetic diversity and structure along their distribution and also across geographically distant areas [101,102]. Such an hypothesis is supported by the comparative higher levels of COI genetic diversity recorded in other rocky Patagonian species of Nacella [20,21,24,25]. General molecular diversity indices in N .…”

“…Most of these studies evidenced clear patterns of postglacial recolonization and recognized the presence of Quaternary glacial refugia on the East side of the Andes, along the Patagonian Steppe [26,29], with refugia on the West side of Andes both within [23,29,38] and outside of the glacier limits [26,34]. Absence of genetic structure and a strong signal of recent demographic growth recorded in shallow Patagonian marine benthic invertebrates support the hypothesis of rapid postglacial expansion [20–22,25]. Species with high dispersive potential (i.e., Durvillaea antarctica and Macrocystis pyrifera ) recolonized Patagonia since the LGM from geographically distant regions [46,48] evidence of the major role of long-distance dispersal in the biogeography of Subantarctic near-shore marine benthic organisms [49–51].…”