A molecular view on adaptation on local and continental scales in the Sub-Antarctic and Antarctic bivalve Aequiyoldia

Marine species and populations have three potential responses to climate change: shift their distribution, adapt to the new environmental conditions or go extinct. The persistence of species unable to shift their ranges in response to changing conditions will be determined by their standing phenotypic plasticity or their ability to develop evolutionary adaptive responses. Physiological comparisons of closely related species/populations on latitudinal gradients have proven to be very informative in determining their respective phenotypic plasticity and genetic adaptability. These macro-scale perspectives, however, overlook the role of small-scale environmental variation in the inter-individual physiological and genetic differences. In this thesis, I used the Southern Ocean protobranch bivalve Aequiyoldia cf. eightsii (Jay, 1839) from West Antarctic Peninsula (WAP) and southern South America (SSA) as a “model species” to study the genetic and phenotypic traits that support adaptation to current and future environmental change at small (i.e., local or population scale) and large -scale (i.e., continental or species scale). As recent evidence suggests the possibility of cryptic speciation between Aequiyoldia bivalves from WAP and SSA, Chapter 2 aims at analysing the genetic diversity between and within populations on both sides of the Drake Passage. In this Chapter I report several highly differentiated mitochondrial genomes (h1, h2, h3, h4) within A. cf. eightsii coexisting in Antarctic populations but also inside a subset of the individuals sampled (mitochondrial heteroplasmy). The mitochondrial differentiation pattern is mirrored in nuclear Single Nucleotide Polymorphisms (SNPs) only across the Drake Passage, whilst the equally strongly differentiated mitochondrial lineages in the Southern Ocean are part of the same distribution of SNPs. These results suggest that populations on both sides of the Drake are two reproductively isolated species, and refuted the previous suggestions of cryptic speciation in WAP A. cf. eightsii. Using SNPs from the entire nuclear and mitochondrial genomes for reference, I demonstrated that mitochondrial heteroplasmy unpredictably misleads classical molecular barcoding procedures using universal cytochrome c oxidase subunit I (COI) primers, producing wrong taxonomic inferences with high confidence. The small-scale approach (Chapter 3) involved the study of in situ gene expression patterns within an Aequiyoldia population in front of a melting glacier in the region of the WAP. This population exhibited strikingly different gene expression pattern under subtly different natural conditions. This pattern was influenced by at least three independent underlying causes: small scale habitat heterogeneity (down to a kilometre scale), and the composition of the mitochondrial and nuclear genomes. Interestingly, the expression of nuclear genes correlated strongly with the mitochondrial genotype, with the highest gene expression differences between homoplasmic and heteroplasmic organisms. This novel mechanism might serve to add another layer of flexibility to respond to the environment and turn out instrumental in the face of the ongoing rapid environmental change in Antarctic fjords. The large-scale approach (Chapter 4) involved an experimental inter-continental comparison of gene expression patterns in response to changes in thermal and oxygen regimes expected under a global warming scenario. In both populations (from WAP and SSA), the experimental temperature implied exposure scenarios simulating a crossing of the Drake Passage, and to an expected near future warming scenario at the WAP. The WAP bivalves showed a moderated physiological response to warming and a remarkable ability to cope with short-term exposure to hypoxia by switching to a metabolic rate depression strategy and activating the alternative oxidation pathway. In SSA, the high prevalence of apoptosis (cell-death)-related differentially expressed genes especially under combined higher temperatures and hypoxia indicated that the SSA Aequiyoldia are operating near their physiological limits already. While the effect of temperature per se may not represent the single most effective barrier to Antarctic colonization by South American bivalves, the current distribution patterns as well as their resilience to future conditions may be better understood by looking at the synergistic effects of temperature in conjunction with short term exposure to hypoxia. Overall, this thesis provides a molecular perspective on the adaptive capacity and cross- continental invasibility of two Aequiyoldia sibling species inhabiting WAP and SSA under a global change scenario