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International audience; The microbial community composition is crucial for diverse life-history traits in many organisms. However, we still lack a sufficient understanding of how the host microbiome is acquired and maintained, a pressing issue in times of global environmental change. Here we investigated to what extent host genotype, environmental conditions, and the endosymbiont Wolbachia influence the bacterial communities in the parasitic wasp Asobara japonica. We sampled multiple wasp populations across ten locations in their natural distribution range in Japan and sequenced the host genome (whole genome sequencing) and microbiome (16S rRNA gene). We compared the host population structure and bacterial community composition of wasps that reproduce sexually and are uninfected with Wolbachia with wasps that reproduce asexually and carry Wolbachia. The bacterial communities in asexual wasps were highly similar due to a strong effect of Wolbachia rather than host genomic structure. In contrast, in sexual wasps, bacterial communities appear primarily shaped by a combination of population structure and environmental conditions. Our research highlights that multiple factors shape the bacterial communities of an organism and that the presence of a single endosymbiont can strongly alter their compositions. This information is crucial to understanding how organisms and their associated microbiome will react in the face of environmental change.

Impact of climate changes on species is expected to be especially visible at the extremities of the species distribution, where they meet sub-optimal conditions. In Mauritania and Iberia, two genetically isolated populations of harbor porpoises form a distinct ecotype and are presumably locally adapted to the upwelling waters. By analyzing the evolution of mitochondrial genetic variation in the Iberian population between two temporal cohorts (1990-2002 vs. 2012-2015), we report a dramatic decrease in genetic diversity. Phylogenetic analyses including neighboring populations identified two porpoises in southern Iberia carrying a divergent haplotype close to the Mauritanian population, yet forming a distinctive lineage. This suggests that Iberian porpoises may not be as isolated as previously thought with immigration from Mauritania or an unknown population in between, but none from the northern ecotype. The rapid decline in the Iberian mitochondrial diversity may be driven by either genetic drift, or by a dramatic decline in census population size possibly resulting from environmental stochasticity, prey depletion, or acute fishery bycatches. These results illustrate the value of genetics time series to inform demographic trends and emphasize the urgent need for conservation measures to ensure the viability of this small harbor porpoise population in Iberia.

Although quite common in terrestrial environments, population differentiation across contiguous geographical areas due to vicariance processes or geographical barriers are far less frequent in the marine environment. Movements in pelagic species such as cetaceans are potentially unrestricted over vast distances. This raises the question of how populations become genetically differentiated, what factors drive individual dispersal, and how speciation occurs in marine pelagic species. The present thesis aimed to investigate how these processes occur at two different evolutionary scales: within (micro-evolution) and between (macro-evolution) species. Combining phylogenetic, phylogeographic, and population genetic approaches complemented with ecological modelling, this thesis investigates the evolution of a group of small cetaceans: the porpoise family (Phocoenidae). The study of the phylogenetic relationships between porpoises as well as their biogeography showed that the seven extant porpoise species radiated during the last 5 million years in response to past environmental changes. At the more recent evolutionary scale within the harbor and finless porpoise species, I investigated the processes partitioning the genetic variation among populations, ecotypes, or subspecies. Analysis of empirical and simulated genetic data shed light on past changes in population size and connectivity, while suitable habitat modelling provided insights into the environmental context in which these demographic events happened. Results revealed that all within species subdivisions arose during the last million years and were strongly influenced by the environmental changes occurring during the Last Glacial Maximum (~26-19 kilo years). The results of this thesis provide a framework for the management and conservation of porpoises.

Understanding a species response to past environmental changes can help forecast how they will cope with ongoing climate changes. Harbor porpoises are widely distributed in the North Atlantic and were deeply impacted by the Pleistocene changes with the split of three sub-species. Despite major impacts of fisheries on natural populations, little is known about population connectivity and dispersal, how they reacted to the Pleistocene changes and how they will evolve in the future. Here, we used phylogenetics, population genetics, and predictive habitat modelling to investigate population structure and phylogeographic history of the North Atlantic porpoises. A total of 925 porpoises were characterized at 10 microsatellite loci and one-quarter of the mitogenome (mtDNA). A highly divergent mtDNA lineage was uncovered in one porpoise off Western Greenland, suggesting that a cryptic group may occur and could belong to a recently discovered mesopelagic ecotype off Greenland. Aside from it and the southern sub-species, spatial genetic variation showed that porpoises from both sides of the North Atlantic form a continuous system belonging to the same subspecies (Phocoena phocoena phoceona). Yet, we identified important departures from random mating and restricted intergenerational dispersal forming a highly significant isolation-by-distance (IBD) at both mtDNA and nuclear markers. A ten times stronger IBD at mtDNA compared to nuclear loci supported previous evidence of female philopatry. Together with the lack of spatial trends in genetic diversity, this IBD suggests that migration-drift equilibrium has been reached, erasing any genetic signal of a leading-edge effect that accompanied the predicted recolonization of the northern habitats freed from Pleistocene ice. These results illuminate the processes shaping porpoise population structure and provide a framework for designing conservation strategies and forecasting future population evolution.

Climatic oscillations in Antarctica caused a succession of expansion and reduction of the ice sheets covering the continental shelf of the Southern Ocean. For marine invertebrates, these successions are suspected to have driven allopatric speciation, endemism and the prevalence of cryptic species, leading to the so-called Antarctic ‘biodiversity pump’ hypothesis. Here we took advantage of the recent sampling effort influenced by the International Polar Year (2007-8) to test for the validity of this hypothesis for 1,797 samples of two recognized crinoid species:Promachocrinus kerguelensisandFlorometra mawsoni. Species delimitation analysis identified seven phylogroups. As previously suggested,Promachocrinus kerguelensisforms a complex of six cryptic species. Conversely, despite the morphological differences, our results show thatFlorometra mawsoniis a lineage nested withinPromachocrinus kerguelensis. It suggests thatFlorometra mawsoniandPromachocrinus kerguelensisbelong to the same complex of species. Furthermore, this study indicates that over time and space the different sectors of the Southern Ocean show a remarkable rapid turn-over in term of phylogroups composition and also of genetic variants within phylogroups. We argue that strong “apparent” genetic drift causes this rapid genetic turn-over. Finally, we dated the last common ancestor of all phylogroups at less than 1,000 years, raising doubts on the relevance of the Antarctic “biodiversity pump” for this complex of species. This work is a first step towards a better understanding of how life is diversifying in the Southern Ocean.

Historical variation in food resources is expected to be a major driver of cetacean evolution, especially for the smallest species like porpoises. Despite major conservation issues among porpoise species (e.g., vaquita and finless), their evolutionary history remains understudied. Here, we reconstructed their evolutionary history across the speciation continuum. Phylogenetic analyses of 63 mitochondrial genomes suggest that porpoises radiated during the deep environmental changes of the Pliocene. However, all intra-specific subdivisions were shaped during the Quaternary glaciations. We observed analogous evolutionary patterns in both hemispheres associated with convergent evolution to coastal versus oceanic environments. This suggests that similar mechanisms are driving species diversification in northern (harbor and Dall’s) and southern species (spectacled and Burmeister’s). In contrast to previous studies, spectacled and Burmeister’s porpoises shared a more recent common ancestor than with the vaquita that diverged from southern species during the Pliocene. The low genetic diversity observed in the vaquita carried signatures of a very low population size since the last 5,000 years. Cryptic lineages within Dall’s, spectacled and Pacific harbor porpoises suggest a richer evolutionary history than previously suspected. These results provide a new perspective on the mechanisms driving diversification in porpoises and an evolutionary framework for their conservation.

Historical changes affecting food resources are a major driver of cetacean evolution. Small cetaceans like porpoises (Phocoenidae) are among the most metabolically challenged marine mammals and are particularly sensitive to changes in their food resources. The seven species of this family inhabit mostly temperate waters and constitute a textbook example of antitropical distribution. Yet, their evolutionary history remains poorly known despite major conservation issues threatening the survival of some porpoises (e.g., vaquita and Yangzte finless porpoises). Here, we reconstructed their evolutionary history across the speciation continuum, from intraspecific subdivisions to species divergence. Phylogenetic analyses of 63 mitochondrial genomes suggest that, like other toothed whales, porpoises radiated during the Pliocene in response to deep environmental changes. However, all intra-specific phylogeographic patterns were shaped during the Quaternary Glaciations. We observed analogous evolutionary patterns in both hemispheres associated with convergent adaptations to coastalversusoceanic environments. This result suggests that the mechanism(s) driving species diversification in the relatively well-known species from the northern hemisphere may apply also to the poorly-known southern species. In contrast to previous studies, we showed that the spectacled and Burmeister’s porpoises share a more recent common ancestor than with the vaquita that diverged from southern species during the Pliocene. The low genetic diversity observed in the vaquita carried signatures of a very low population size throughout at least the last 5,000 years, leaving one single relict mitochondrial lineage. Finally, we observed unreported subspecies level divergence within Dall’s, spectacled and Pacific harbor porpoises, suggesting a richer evolutionary history than previously suspected. These results provide a new perspective on the mechanism driving the adaptation and speciation processes involved in the diversification of cetacean species. This knowledge can illuminate their demographic trends and provide an evolutionary framework for their conservation.

Absence of genetic differentiation is usually taken as an evidence of panmixia, but can also reflect other situations, including even nearly complete demographic independence among large-sized populations. Deciphering which situation applies has major practical implications (e.g., in conservation biology). The endangered harbor porpoises in the Black Sea illustrates this point well. While morphological heterogeneity suggested that population differentiation may exist between individuals from the Black and Azov seas, no genetic study provided conclusive evidence or covered the entire subspecies range. Here, we assessed the genetic structure at ten microsatellite loci and a 3904 base-pairs mitochondrial fragment in 144 porpoises across the subspecies range (i.e., Aegean, Marmara, Black, and Azov seas). Analyses of the genetic structure, including F ST, Bayesian clustering, and multivariate analyses revealed a nearly complete genetic homogeneity. Power analyses rejected the possibility of underpowered analyses (power to detect F ST ≥ 0.008 at microsatellite loci). Simulations under various demographic models, evaluating the evolution of F ST, showed that a time-lag effect between demographic and genetic subdivision is also unlikely. With a realistic effective population size of 1000 individuals, the expected “gray zone” would be at most 20 generations under moderate levels of gene flow (≤10 migrants per generation). After excluding alternative hypotheses, panmixia remains the most likely hypothesis explaining the genetic homogeneity in the Black Sea porpoises. Morphological heterogeneity may thus reflect other processes than population subdivision (e.g., plasticity, selection). This study illustrates how combining empirical and theoretical approaches can contribute to understanding patterns of weak population structure in highly mobile marine species.

Understanding demographic trends and patterns of gene flow in an endangered species is crucial for devising conservation strategies. Here, we examined the extent of population structure and recent evolution of the critically endangered Yangtze finless porpoise (Neophocaena asiaeorientalis asiaeorientalis). By analysing genetic variation at the mitochondrial and nuclear microsatellite loci for 148 individuals, we identified three populations along the Yangtze River, each one connected to a group of admixed ancestry. Each population displayed extremely low genetic diversity, consistent with extremely small effective size (≤92 individuals). Habitat degradation and distribution gaps correlated with highly asymmetric gene-flow that was inefficient in maintaining connectivity between populations. Genetic inferences of historical demography revealed that the populations in the Yangtze descended from a small number of founders colonizing the river from the sea during the last Ice Age. The colonization was followed by a rapid population split during the last millennium predating the Chinese Modern Economy Development. However, genetic diversity showed a clear footprint of population contraction over the last 50 years leaving only ~2% of the pre-collapsed size, consistent with the population collapses reported from field studies. This genetic perspective provides background information for devising mitigation strategies to prevent this species from extinction.

Decrease in male fertility observed in the past decades have involved sperm quantity and quality disorders. However, decrease in quality or quantity of seminal fluid may also trigger drastic reduction of female and also male fertility. The present paper documents on the composition of seminal fluid, the consequences on sperm cells and on the physiological and behavioral effects towards females. The work evidences the crucial role of seminal fluid in the postcopulatory interactions between the sexes and illustrates the selective effects in the male-female coevolution.

Decrease in male fertility observed in the past decades have involved sperm quantity and quality disorders. However, decrease in quality or quantity of seminal fluid may also trigger drastic reduction of female and also male fertility. The present paper documents on the composition of seminal fluid, the consequences on sperm cells and on the physiological and behavioral effects towards females. The work evidences the crucial role of seminal fluid in the postcopulatory interactions between the sexes and illustrates the selective effects in the male-female coevolution.