Abstract

The Antarctic coastal fauna is characterized by high endemism related to the progressive cooling of Antarctic waters and their isolation by the Antarctic Circumpolar Current. The origin of the Antarctic coastal fauna could involve either colonization from adjoining deep-sea areas or migration through the Drake Passage from sub-Antarctic areas. Here, we tested these hypotheses by comparing the morphology and genetics of benthic foraminifera collected from Antarctica, sub-Antarctic coastal settings in South Georgia, the Falkland Islands and Patagonian fjords. We analyzed four genera (Cassidulina, Globocassidulina, Cassidulinoides, Ehrenbergina) of the family Cassidulinidae that are represented by at least nine species in our samples. Focusing on the genera Globocassidulina and Cassidulinoides, our results showed that the first split between sub-Antarctic and Antarctic lineages took place during the mid-Miocene climate reorganization, probably about 20 to 17 million years ago (Ma). It was followed by a divergence between Antarctic species ~ 10 Ma, probably related to the cooling of deep water and vertical structuring of the water-column, as well as broadening and deepening of the continental shelf. The gene flow across the Drake Passage, as well as between South America and South Georgia, seems to have occurred from the Late Miocene to the Early Pliocene. It appears that climate warming during 7–5 Ma and the migration of the Polar Front breached biogeographic barriers and facilitated inter-species hybridization. The latest radiation coincided with glacial intensification (~ 2 Ma), which accelerated geographic fragmentation of populations, demographic changes, and genetic diversification in Antarctic species. Our results show that the evolution of Antarctic and sub-Antarctic coastal benthic foraminifera was linked to the tectonic and climatic history of the area, but their evolutionary response was not uniform and reflected species-specific ecological adaptations that influenced the dispersal patterns and biogeography of each species in different ways.

Highlights

  • The Antarctic coastal fauna is characterized by high endemism related to the progressive cooling of Antarctic waters and their isolation by the Antarctic Circumpolar Current

  • Progressive widening and deepening of this seaway enabled the formation of the Antarctic Circumpolar Current (ACC), which in combination with global carbon dioxide decline around the Eocene/Oligocene boundary ~ 34 ­Ma6, facilitated a gradual process of Antarctic ­cooling[7], strengthening of thermal gradients between Patagonia and the Antarctic Peninsula, and a marked separation of ecosystems on the two sides of the Drake P­ assage[8]

  • Our results suggest that some Cassidulinidae species could have crossed the Polar Front (PF) and ACC barriers as their molecular and morphologic diversity does not fit a simple pattern of evolution of Antarctic and sub-Antarctic species in isolation since the full opening of the Drake Passage in the Middle Miocene

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Summary

Introduction

Progressive widening and deepening of this seaway enabled the formation of the Antarctic Circumpolar Current (ACC), which in combination with global carbon dioxide decline around the Eocene/Oligocene boundary ~ 34 ­Ma6, facilitated a gradual process of Antarctic ­cooling[7], strengthening of thermal gradients between Patagonia and the Antarctic Peninsula, and a marked separation of ecosystems on the two sides of the Drake P­ assage[8] This process reversed during the mid-Miocene climatic warming between 17 and 14.5 Ma, and even increased with the Middle Miocene cooling at ~ 14 ­Ma9 and the final opening of the Drake Passage for deep oceanic circulation ~ 12 ­Ma10. As one of the key elements of the Antarctic fauna, the Cassidulinidae have been used extensively in paleoenvironmental r­ esearch[35,36,37,38,39] and are well represented in the Cenozoic fossil record from the Ross ­Sea[40,41,42,43], the Antarctic Peninsula ­sector[44,45,46,47], and East ­Antarctica[48,49,50]

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