Evolution and diversification of Amphipoda in the polar regions: the case study of Eusirus genus

Abstract

The past major climate changes have disrupted life in the polar regions and triggered different responses in marine organisms. Confronted now with fast-paced environmental changes such as global warming, understanding the adaptations and patterns of diversification in these regions with extreme environmental conditions can help to predict their possible response to future climate change. To do so, the genus Eusirus was chosen as a model organism because: 1) of its worldwide distribution with representatives in both polar regions; 2) local abundance and a large number of species showing high level of endemicity; 3) occupying both deep and shallow marine waters; 4) exhibiting a wide range of morphological variation; and 5) belonging to the Eusiridae family, which is a major family of polar amphipods. By combining molecular, morphological, and ecological data, this thesis aims to understand the genetic adaptations and the evolutionary processes that shaped the current diversity of the Eusirus amphipods in the Arctic and Southern Oceans. First, three novel complete Antarctic mitogenomes were assembled and annotated. Their analysis showed distinct features such as a lower AT-richness in the whole mitogenomes, negative GC-skews on both strands of protein coding genes, and unique gene rearrangements. These mitogenomes also shared characteristics with other amphipod mitogenomes including aberrant tRNA and short rRNA genes, which could be linked to minimalization of mitogenomes. Nucleotide diversity analysis revealed nad6 and atp8 to be the most variable mitochondrial regions of amphipods. In contrast, cox1 showed low nucleotide diversity among closely and more distantly related amphipod species. Second, molecular signatures of cold adaptations were highlighted by comparing different mitogenomic features of amphipods from cold, temperate, and warm regions. Among other results, amphipods living in cold environment possessed mitogenomes with low proportions of charged amino acids and high, average ratios of non-synonymous to synonymous substitutions (ω). On the other hand, mitogenomic gene translocations and phylogenetic relationships had no distinct patterns being related to cold adaptations. Third, new phylogenetic reconstructions of Eusirus and a novel dated tree were produced. These data strongly supported the monophyly of the Antarctic clade whereas Arctic Eusirus had a polyphyletic origin. The mean age of Arctic Eusirus is older than Antarctic Eusirus despite the older existence and longer geographic isolation of Antarctica. Finally, the integration of phylogenetic information, phenotypic and ecological data identified two different evolutionary patterns of Eusirus in the polar oceans. A high rate of lineage diversification coupled with low rate of morphological evolution supported a non-adaptive radiation scenario in the Antarctic clade. Even if ecology certainly played a role during the diversification of the Antarctic clade, it is hypothesized that allopatric speciation such as vicariant events following the opening of the Drake passage and the formation of the Antarctic Circumpolar Current formation mainly produced new lineages. The contrasting slower diversification rates observed in the Arctic Eusirus lineages could be explained by higher gene flow and higher extinction rates. Morphological and ecological diversity in the Arctic clade probably accumulated more constantly along speciation events. Despite the constant rate of lineage diversification in the Arctic Eusirus, the morphological and the ecological diversity were both observed to be high. This high morphological and ecological diversity in Arctic Eusirus could be associated to their polyphyletic origin and their older evolutionary age. Certainly, the high levels of morphological and ecological diversity in the Arctic Eusirus support the hypothesis that niche partitioning played a crucial role during the diversification of Eusirus in the Arctic. In conclusion, the multi-disciplinary approach integrating molecular, morphological, and ecological data successfully unraveled the different evolutionary patterns of the genus Eusirus in the two polar regions.