Population genomics, phylogeographic history, and evolutionary patterns in Antartic shallow-water benthic invertebrates

Abstract

Benthic organisms inhabiting the shallow waters of the Southern Ocean are considered excellent models to study evolutionary processes, population connectivity patterns, and adaptation. They have evolved in an extreme environment, with expanding and retreating periods following glacial cycles, in an alternation pattern. Repeated rounds of population fragmentation in glacial refugia during glacial cycles followed by expansions and secondary contacts during interglacials were the main evolutionary force that brought Antarctic shallow-water ecosystems to their current state. In my PhD dissertation I have investigated in detail these singular evolutionary histories left in the genomes of our target species. Besides the past geological events, currently, threats from global warming arrive to the isolated southernmost continent. Indeed, coastal waters off West Antarctica are some of the most affected oceanic regions of the planet by global warming, with rather pessimistic projections for the near future. Considering this and the increasing local threats to which shallow-water ecosystems are exposed, it is fundamental to develop a well-connected network of Marine Protected Areas (MPAs) throughout the Southern Ocean. Despite genetic connectivity is not usually considered in MPA planning, population genetic studies can provide extremely valuable information to design connected MPA networks. In my dissertation I have also disentangled gene-flow patterns of Antarctic shallow-water benthic invertebrates, aiming to help to improve the current status of Southern Ocean MPAs.

In order to achieve my goals, I combined information coming from ‘traditional’ genetic markers, single nucleotide polymorphisms (SNPs) derived from restriction-site associated DNA sequencing (ddRADseq), transcriptomes, and draft-level genomes. A wide range of species presenting different reproductive modes was selected in order to test whether this factor plays a role on connectivity and evolutionary patterns in the explained scenario of glacial alternations: the brooding congeneric nemerteans Antarctonemertes valida, A. riesgoae, and A. unilineata; the demosponges Dendrilla antarctica and Mycale acerata, which present lecithotrophic larvae; and the annelids Pterocirrus giribeti (new species described in the Chapter 1 of my PhD dissertation) and Neanthes kerguelensis, that presumably presents planktotrophic larvae.

Our results regarding the evolutionary history of our target species revealed different glacial-refugium strategies independent of their reproductive mode, and generalised signals of bottleneck events. Moreover, blurred species boundaries were detected for the Antarctonemertes lineages, with a central role of glacial cycles in their introgressive evolutionary history. Additionally, we identified adaptive genes for particular glacial-refugium strategies and for the rise of prezygotic barriers during speciation and reinforcement events. Our connectivity results confirmed that genetic connectivity in the Southern Ocean is not determined by a priori dispersal abilities resulting from different reproductive strategies. We revealed an overall high gene flow along the Western Antarctic Peninsula (WAP), which is particularly exceptional for sponges and brooding species. Interestingly, loci under divergent selection were identified for D. antarctica despite admixture, broadly differentiating between the populations of Northern and Southern WAP. We suggest that ongoing natural selection is governed by differences in sea-ice extent and duration, exhibiting the vulnerability of the WAP benthic ecosystems due to the decline in the sea ice predicted for the near future. Finally, we demonstrated that long-distance connectivity did not surpass the regional WAP scale, supporting the implementation of an MPA covering the WAP and the coastal waters off the South Orkneys.

Overall, the studies presented in my PhD dissertation represent a step forward in understanding global forces and processes affecting the evolutionary history of Antarctic marine organisms. We illustrated the adaptability of shallow-water benthic invertebrates to the natural changes of the Southern Ocean, while manifesting their vulnerability to future global warming. Remarkably, we highlight the importance of using population genetic data of various benthic invertebrate species to implement MPA networks in one of the most threatened areas of the planet by global warming. The results of my thesis will be fundamental to address the suitability and effectiveness of an MPA network comprising the already implemented MPA at South Georgia and South Sandwich Islands and the proposed MPA covering the WAP and the South Orkney Islands, essential for the survival of Antarctic marine ecosystems.