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Jollivet, D.

Publications and source records attributed to Jollivet, D..

11 recordsLinked to original sources

Ecological Diversification into Broad Thermal Niches Revealed by Protein Resurrection and Proteome-Wide Ancestral Reconstruction During the Rapid Radiation of Alvinellid Worms

In the deep Pacific and Indian oceans, Alvinellid worms diversified about 100 million years ago to colonize a variety of hydrothermal vent environments. It has been suggested that the last common ancestor of this family was a thermophilic species. However, the evolutionary history of these worms is complex, with putative gene flow among ancestors. In this study, we investigated the early evolution of the family in relation to the diversification of thermal niches. We demonstrated that phylogenetic histories of alvinellid species greatly vary along chromosomes, possibly due to allele introgression between nascent ecotypes. We performed sequence reconstructions of ancestral cytosolic MDH and Cu/Zn SOD under the two most frequent phylogenies encountered along the genome. In silico simulations of folding stability for these two enzymes were highly correlated with their biophysical characterization (micro-calorimetry and differential scanning fluorimetry), and were used to predict the thermostability of thousands of alternatively reconstructed proteins. We further generalized the reconstruction at the proteome scale, taking the amino-acid usage bias as a proxy for folding stability in a new phylogenetic model accounting for amino-acid variations over time. Both approaches agree that the last common ancestors of Alvinellidae gained highly stable proteins, comparable to proteins of present-day thermotolerant species. Our computational protocol allowed us to validate this scenario under multiple phylogenetic hypotheses and different sequence reconstruction models. Considered together, Alvinellidae shed light on how metazoan species diversify in order to colonize different thermal niches, combining adaptive mutation and selection on genetic variants. SignificanceDeep-sea hydrothermal vents are among the most extreme environments on Earth. They, however, represent oases of life for a restricted number of highly specialized species. As such, Alvinellid worms constitute an exceptional family, including highly thermotolerant animals such as the Pompeii worm. Despite their vent endemicity, Alvinellidae thrive under contrasting ecological conditions, particularly regarding temperature. Understanding how this family diversified to colonize broad thermal regimes is of major importance for dissecting the mechanisms by which species adapt in highly unstable environments. Combining experimental protein resurrection, proteome-wide predictions, and new phylogenetic models, we assess the reliability of ancestral sequence reconstructions that represent molecular thermometers to evaluate past environmental conditions.

evolutionary biology↗

High gene flow in Atlantic vent shrimp species with multiple ridge colonizations by ecotypic lineages with contrasting symbioses

Conservation concerns regarding potential mineral extraction near deep-sea hydrothermal vents have emphasised the need for a better understanding of the contemporary connectivity of various vent-endemic species, accounting for the specifics of their life-history traits and habitat requirements. Rimicaris shrimps are a major component of vent communities in the Atlantic Ocean, both along the Mid-Atlantic Ridge (MAR) and at the Mid-Cayman Spreading Center (MCSC). Using ddRAD sequencing, we examined the genetic differentiation of three Atlantic Rimicaris species to better understand their past and present migration pathways and the possible demographic history that led to their current distribution and ecology. Rimicaris exoculata and R. chacei inhabit the MAR and exhibit widespread gene flow along the ridge with no areas of restricted connectivity. R. hybisae occurs at the MCSC and exhibits almost no genetic difference with its congeneric from the MAR, R. chacei, despite the geographic distance between them and their contrasting ecologies and morphologies. Demographic inferences support a scenario of a very recent (less than 2000 generations) separation between MCSC and MAR shrimp populations, followed by a rapid expansion in both regions, possibly triggered by symbiotic development. Analyses further suggest recent or ongoing secondary contacts involving two-way migration, which is more pronounced from the MCSC towards the MAR. All together these results suggest that R. chacei and R. hybisae represent distinct forms of the same species, which we hereby synonymise as R. chacei, highlighting their morphological plasticity in relation to symbiosis.

evolutionary biology↗

Discovery of a chemosynthetic community at the serpentinite-hosted seep on the Quaker Seamount, Mariana Forearc

Deep-sea chemosynthesis-based ecosystems in the Mariana Region include hydrothermal vents on the Mariana Arc and in the Mariana Back-Arc, and serpentinite-hosted seeps on the Mariana Forearc - with the latter being by far the least studied. Here, we surveyed the biodiversity of the serpentine seep on the Quaker Seamount. At first glance, the area appears to be devoid of megafauna, but examination of the carbonates revealed dense aggregations of animals dominated by the limpets Bathyacmaea and Pyropelta on brucite-carbonate chimney structures exhibiting visible fluid venting. Sorting of recovered material yielded a total of 14 species and together with an observation of a Munidopsis squat lobster we report a total of 15 species; six of these are considered endemics of chemosynthetic ecosystems. The occurrence of taxa such as the snail Lurifax cf. japonicus and the limpet Pyropelta ryukyuensis, otherwise only known from distant vents in the Izu-Ogasawara Arc and Okinawa Trough off Japan, strengthens the hypothesis that serpentine seeps may function as dispersal stepping-stones across arc and back-arc systems.

ecology↗

Chromosome-scale genome assembly and gene annotation of the hydrothermal vent annelid Alvinella pompejana yield insight into animal evolution in extreme environments

The types of genomic change needed for environmental adaptation are of great interest. Annelid worms are a large phylum found in a rich diversity of habitats, giving opportunities to explore this issue. We report the chromosome level genome sequence of the Pompeii worm, the annelid Alvinella pompejana, an inhabitant of an extreme deep-sea hydrothermal vent environment. We find strong but heterogeneously distributed genetic divergence between populations taken from either side of the equator. Using transcript data, we produced a set of gene models and analysed the predicted protein set in the light of past hypotheses about the thermotolerance of Alvinella, and compared it to other recently sequenced annelid vent worms. We do not find evidence of a more extreme genome wide amino acid composition than other species, neither do we find evidence for rapid genome evolution in the form of disrupted synteny. We discount the hypothesis of loss of amino acid biosynthesis genes associated with obligate symbioses reported in siboglinid annelids. We do find evidence of a parallel increase in the number of globin encoding genes and loss of light sensitive opsins and cryptochromes. Alvinella encodes several respiratory enzymes unusual for bilaterian animals, suggesting an ability to better tolerate hypoxic environments.

genomics↗

Comparative population genomics unveils congruent secondary suture zone in Southwest Pacific Hydrothermal Vents

How the interplay of biotic and abiotic factors shapes current genetic diversity at the community level remains an open question, particularly in the deep sea. Comparative phylogeography of multiple species can reveal the influence of past climatic events, geographic barriers, and species life history traits on spatial patterns of genetic structure across lineages. To shed light on the factors that shape community-level genetic variation and to improve our understanding of deep-sea biogeographic patterns, we conducted a comparative population genomics study on seven hydrothermal vent species co-distributed in the Back-Arc Basins (BABs) of the Southwest Pacific region. Using ddRAD-seq, we compared the range-wide distribution of genomic diversity across species and discovered a shared phylogeographic break. Demogenetic inference revealed shared histories of lineage divergence and a secondary contact. Low levels of asymmetric gene flow probably occurred in most species between the Woodlark and North Fiji basins, but the exact location of contact zones varied from species to species. For two species, we found individuals from the two lineages co-occurring in sympatry in Woodlark Basin. Although species exhibit congruent patterns of spatial structure (Eastern vs Western sites), they also show variation in the degree of divergence among lineages across the suture zone. Our results also show heterogeneous gene flow across the genome, indicating possible partial reproductive isolation between lineages and early speciation. Our comparative study highlights the pivotal role of historical and contemporary factors, underscoring the need for a comprehensive approach--especially in addressing knowledge gaps on the life history traits of deep-sea species.

evolutionary biology↗

A step in the deep evolution of Alvinellidae (Annelida: Polychaeta): a phylogenomic comparative approach based on transcriptomes

The Alvinellidae are a family of worms that are endemic to deep-sea hydrothermal vents in the Pacific and Indian Oceans. These annelid worms, a sister group to the Ampharetidae, occupy a wide range of thermal habitats. The family includes the most thermotolerant marine animals described to date such as the Pompeii worm Alvinella pompejana, and other species living at much lower temperatures such as Paralvinella grasslei or Paralvinella pandorae. The phylogeny of this family has not been studied extensively. It is, however, a complex case where molecular phylogenies have given conflicting results, especially concerning the monophyletic or polyphyletic nature of the genus Paralvinella. We carried out a comprehensive study of the phylogeny of this family using the best molecular data currently available from RNAseq datasets, leading to several hundred orthologous transcripts for 11 of the 14 species currently described or in description. The results obtained by the two most popular phylogenetic inference models (using either gene concatenation with maximum likelihood, or a coalescent-based model from gene trees) were compared using a series of ampharetid and terebellid outgroups. Our study shows that the global phylogenetic signal favors the hypothesis of paraphyly for the Paralvinella genus, with P. pandorae being sister species of the other Alvinellidae. However, a high number of gene trees also supports the hypothesis of alternative trees in which the monophyly of the Paralvinella genus, as initially proposed by Desbruyeres and Laubier, is valid with the species P. pandorae and Paralvinella unidentata being sister species. According to molecular dating, the radiation of the Alvinellidae was rapid and took place in a short period of time between 80 and 110 million years ago. This is reflected at the genomic scale by gene trees equally separated between different phylogenetic hypothesis, showing high rates of incomplete lineage sorting between the first lineages of the Alvinellidae and probable gene transfers. Although different genomic regions seem to have different phylogenetic stories in the early step of the alvinellid radiation, our study supports the view that the two P. pandorae species can be grouped into a separate genus (possibly Nautalvinella) and that the Miralvinella subgenus, defined by Desbruyeres and Laubier, is not valid anymore.

evolutionary biology↗

Genetic sex determination in three closely related hydrothermal vent gastropods, one of which has intersex individuals

Molluscs have a wide variety of sexual systems and have undergone many transitions from separate sexes to hermaphroditism or vice versa, which is of interest for studying the evolution of sex determination and differentiation. Following the serendipitous observation that sex was the primary driver of genetic structure in the hydrothermal vent gastropod Alviniconcha boucheti, we investigated sexual systems and sex determination in this species and two others of the same genus. We combined genome-wide multi-locus genotypes obtained from RAD sequencing with anatomical observations of the gonads of the three Alviniconcha species occurring in the southwest Pacific Ocean: A. boucheti (n=199), A. strummeri (n=41 ind.) and A. kojimai (n=246). In two of the species (A. boucheti and A. strummeri), the sexes are separate and genetically determined by a male-heterogametic (XY) system. External observation of the gonads in the third species (A. kojimai) also suggested that the sexes were separate, but histological analyses revealed that 76% of the individuals classified as females from external observation of the gonads presented a mosaic of male and female reproductive tissue. Empirical analyses and simulations showed nonetheless that 14 RAD loci were sex-linked with an XY signature in A. kojimai (as compared with 64 in A. strummeri and 373 in A. boucheti). Comparison across species and mapping of RAD loci to a non-contiguous reference genome assembly of the related species A. marisindica showed that all sex-linked loci identified in A. kojimai are located on five scaffolds that also contain 15 and 67 sex-linked RAD loci in the other two species, respectively. These results suggest that all three Alviniconcha species share the same XY sex determination system, but that the gonad of XX A. kojimai individuals are invaded by a variable proportion of male reproductive tissue. It remains to be seen whether the male tissue in these intersex individuals is functional or not. The identification of Y-specific RAD loci (found only in A. boucheti) and the phylogenetic analysis of three sex-linked loci shared by all species suggested that X-Y recombination has evolved differently within each species. This situation of three species showing variation in gonadal development around a probably common sex determination system provides new insights into the reproductive mode of poorly known deep-sea species and questions the evolution of gametogenetic polymorphism in these species.

evolutionary biology↗

A step towards measuring connectivity in the deep-sea: elemental fingerprints of mollusk larval shells discriminate hydrothermal sites

Deep-sea hydrothermal-vent systems are under investigation for base and precious metal exploitations. The impact of mining will depend critically on the ability of larval dispersal to connect and replenish endemic populations. However, assessing connectivity is extremely challenging, especially in the deep sea. Here, we investigate the potential of elemental fingerprinting of mollusc larval shells to discriminate larval origins between multiple hydrothermal sites in the Southwest Pacific Ocean. The gastropod Shinkailepas tollmanni represents a suitable candidate as it uses capsules to hold larvae before dispersal, which facilitates sampling and ensures mineralization occurs on the site of origin. Multielemental microchemistry was performed using cutting-edge femtosecond laser ablation Inductively Coupled Plasma Mass Spectrometry analysis to obtain individual measurements on 600 encapsulated larval shells. We used classification methods to discriminate the origin of individuals from 14 hydrothermal sites spanning over 3,500 km, with an overall success rate of 70%. When considering less sites within more restricted areas, reflecting dispersal distances reported by genetic and modelling approaches, the success rate increased up to 86%. We conclude that individual larval shells register site-specific elemental signatures that can be used to assess their origin. These results open new perspectives to get direct estimates on population connectivity from the geochemistry of pre-dispersal shell of recently settled juveniles.

ecology↗

Genomic patterns of divergence in the early and late steps of speciation of the deep-sea vent thermophilic worms of the genus Alvinella.

BackgroundThe transient and fragmented nature of the deep-sea hydrothermal environment made of ridge subduction, plate collision and the emergence of new rifts is currently acting to the separation of vent populations, local adaptation and is likely to promote bursts of speciation and species specialization. The tube-dwelling worms Alvinella pompejana called the Pompeii worm and its sister species A. caudata live syntopically on the hottest part of deep-sea hydrothermal chimneys along the East Pacific Rise. They are exposed to extreme thermal and chemical gradients, which vary greatly in space and time, and thus represent ideal candidates for understanding the evolutionary mechanisms at play in the vent fauna evolution. ResultsIn the present study, we explored genomic patterns of divergence in the early and late steps of speciation of these emblematic worms using transcriptome assemblies and the first draft genome to better understand the relative role of geographic isolation and habitat preference in their genome evolution. Analyses were conducted on allopatric populations of Alvinella pompejana (early stage of separation) and between A. pompejana and its syntopic species Alvinella caudata (late stage of speciation). We first identified divergent genomic regions and targets of selection as well as their position in the genome over collections of orthologous genes and, then, described the speciation dynamics by documenting the annotation of the most divergent and/or positively selected genes involved in the isolation process. Gene mapping clearly indicated that divergent genes associated with the early stage of speciation, although accounting for nearly 30% of genes, are highly scattered in the genome without any island of divergence and not involved in gamete recognition or mito-nuclear incompatibilities. By contrast, genomes of A. pompejana and A. caudata are clearly separated with nearly all genes (96%) exhibiting high divergence. This congealing effect however seems to be linked to habitat specialization and still allows positive selection on genes involved in gamete recognition, as a possible long-duration process of species reinforcement. ConclusionOur analyses pointed out the non-negligible role of natural selection on both the early and late stages of speciation in the emblematic thermophilic worms living on the walls of deep-sea hydrothermal chimneys. They shed ligth on the evolution of gene divergence during the process of speciation and species specialization over a very long period of time.

evolutionary biology↗

The protected phosphoglucomutase polymorphism of the Pompeii worm Alvinella pompejana and its variant adaptability is only governed by two QE mutations at linked sites

The polychaete Alvinella pompejana lives exclusively on the walls of deep-sea hydrothermal chimneys along the East Pacific Rise and, display specific adaptations to withstand high temperature and hypoxia associated with this highly variable habitat. Previous studies revealed the existence of a balanced polymorphism on the enzyme phosphoglucomutase associated with thermal variations where allozymes 90 and 100 exhibited different optimal activities and thermostabilities. The exploration of the mutational landscape of the phosphoglucomutase1 revealed the maintenance of four highly divergent allelic lineages encoding the three most frequent electromorphs over the worms geographic range. This polymorphism is only governed by two linked amino-acid replacements located in exon 3 (E155Q and E190Q). A two-niches model of selection with cold and hot conditions represents the most likely way for the long-term persistence of these isoforms. Using directed mutagenesis, overexpression of the three recombinant variants allowed us to test the additive effect of these two mutations on the biochemical properties of this enzyme. Results are coherent with those previously obtained from native proteins and reveal a thermodynamic trade-off between the protein thermostability and catalysis, which is likely to have maintained these functional phenotypes prior to the geographic separation of populations across the Equator, about 1.2 Mya.

evolutionary biology↗

The genome of Ectocarpus subulatus highlights unique mechanisms for stress tolerance in brown algae

Brown algae are multicellular photosynthetic stramenopiles that colonize marine rocky shores worldwide. Ectocarpus sp. Ec32 has been established as a genomic model for brown algae. Here we present the genome and metabolic network of the closely related species, Ectocarpus subulatus Kutzing, which is characterized by high abiotic stress tolerance. Since their separation, both strains show new traces of viral sequences and the activity of large retrotransposons, which may also be related to the expansion of a family of chlorophyll-binding proteins. Further features suspected to contribute to stress tolerance include an expanded family of heat shock proteins, the reduction of genes involved in the production of halogenated defence compounds, and the presence of fewer cell wall polysaccharide-modifying enzymes. Overall, E. subulatus has mainly lost members of gene families down-regulated in low salinities, and conserved those that were up-regulated in the same condition. However, 96% of genes that differed between the two examined Ectocarpus species, as well as all genes under positive selection, were found to encode proteins of unknown function. This underlines the uniqueness of brown algal stress tolerance mechanisms as well as the significance of establishing E. subulatus as a comparative model for future functional studies.

genomics↗