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 biogeographic 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 ...

Quaternary ice sheets and sea level regression drove divergence in a marine gastropod along Eastern and Western coasts of South America

“…Strong demographic and geographic expansion following post-glacial sea level rise may also be a suitable explanation for the low levels of genetic diversity and the high degree of genetic homogeneity in S. lessonii across these provinces. This pattern of genetic structure has been found in several Magellan marine benthic near-shore organisms with dispersive potential including invertebrates 20,55 , vertebrates 14,22 and macroalgae 19,27 . Finally, in contrast to recent phylogeographic analyses in sub-Antarctic invertebrates including Siphonaria species 21 , isopods 57 , and patellogastropods 20,55 , we found in S. lessonii a complete absence of genetic structure between continental Magellan and the Malvinas/Falkland Islands populations.…”

“…This pattern of genetic structure has been found in several Magellan marine benthic near-shore organisms with dispersive potential including invertebrates 20,55 , vertebrates 14,22 and macroalgae 19,27 . Finally, in contrast to recent phylogeographic analyses in sub-Antarctic invertebrates including Siphonaria species 21 , isopods 57 , and patellogastropods 20,55 , we found in S. lessonii a complete absence of genetic structure between continental Magellan and the Malvinas/Falkland Islands populations. The presence of a free-living dispersive stage in S. lessonii, absent in other sub-Antarctic Siphonaria species, seems to play a key role establishing genetic homogeneity across thousands of kilometers from Chiloé Island to Uruguay in the southwest Atlantic.…”

“…Another interesting result recorded in S. lessonii is the absence of genetic structure along the Chile-Peru province (R1), as well as along the Magellan-Argentina provinces (R2). Such results may be a consequence of gene flow mediated by larval dispersal through the main flows of the Humboldt Current System, heading north along the Chilean coast, as well as the Cape Horn Current, heading south across the Magellan province, as recorded in several cold and temperate near-shore marine organisms [19][20][21]55,56 . Strong demographic and geographic expansion following post-glacial sea level rise may also be a suitable explanation for the low levels of genetic diversity and the high degree of genetic homogeneity in S. lessonii across these provinces.…”

Unexpected absence of island endemics: Long‐distance dispersal in higher latitude sub‐Antarctic Siphonaria (Gastropoda: Euthyneura) species

“…Quaternary glacial processes in the Southern Ocean severely affected the demography of shallow benthic populations as has been demonstrated in several population‐based studies (e.g. Allcock & Strugnell, ; Fraser et al., ; González‐Wevar, Saucède, Morley, Chown, & Poulin, ; González‐Wevar et al., , ; Nikula et al., ; Thornhill et al., ). Repeated ice advances and retreats would have generated massive reductions in population sizes (or even local extinctions) and consequent severe declines in genetic diversity.…”

“…Unexpectedly, our results showed that haplotypes of S. lateralis from FI are clearly differentiated (≥8 steps away) from those of other localities, including adjacent areas such as Patagonia. Evidence of genetic differentiation between PP and FI populations has been recorded in crustaceans like Parawaldeckia kidderi (Nikula et al., ), and Serolis paradoxa (Leese et al., ) and limpets of the genus Nacella (González‐Wevar et al., , ). Due to their geographical position, the FI were less affected by Quaternary glaciations than other areas of the Southern Ocean (Hodgson et al., ).…”