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

Type Article
Date 2022-09
Language English
Author(s) Thomas-Bulle Camille1, Bertrand Denis2, Nagarajan Niranjan2, 3, Copley Richard R.4, Corre Erwan5, Hourdez Stéphane6, Bonnivard Éric1, Claridge-Chang Adam7, 8, 9, Jollivet Didier1
Affiliation(s) 1 : Dynamique de la Diversité Marine (DyDiv) Lab, Station Biologique de Roscoff, Sorbonne Université, CNRS, UMR 7144 AD2M, Place G. Teissier CS90074, 29680, Roscoff, France
2 : Genome Institute of Singapore, Agency for Science, Technology, and Research, Singapore, Singapore
3 : Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore
4 : Laboratoire de Biologie du Développement de Villefranche-Sur-Mer (LBDV), Sorbonne Université, CNRS, 06230, Villefranche-sur-mer, France
5 : ABiMS Bioinformatics Facility, Station Biologique de Roscoff, Sorbonne Université, CNRS, R2424, Place G. Teissier, 29680, Roscoff, France
6 : Laboratoire d’Ecogéochimie des Environnements Benthiques, Observatoire Océanologique de Banyuls, Sorbonne Université, CNRS, UMR 8222, Avenue Pierre Fabre, 66650, Banyuls-sur-Mer, France
7 : Program in Neuroscience and Behavioral Disorders, Duke-NUS Medical School, Singapore, Singapore
8 : Institute for Molecular and Cell Biology, A*STAR, Singapore, Singapore
9 : Department of Physiology, National University of Singapore, Singapore, Singapore
Source Bmc Ecology And Evolution (2730-7182) (Springer Science and Business Media LLC), 2022-09 , Vol. 22 , N. 1 , P. 106 (17p.)
DOI 10.1186/s12862-022-02057-y
WOS© Times Cited 3
Keyword(s) Divergence, Genome architecture, Speciation, Ecological species, Habitat specialization, Selection, Hydrothermal vents
Abstract

Background The 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 separate of vent populations, promoting local adaptation and contributing to 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. Results We explored genomic patterns of divergence in the early and late stages 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. Conclusion Our analyses highlight the non-negligible role of natural selection on both the early and late stages of speciation in the iconic thermophilic worms living on the walls of deep-sea hydrothermal chimneys. They shed light on the evolution of gene divergence during the process of speciation and species specialization over a very long period of time.

Full Text
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Publisher's official version 17 2 MB Open access
Supplementary table 1. Annotation of the divergent genes and genes under selection based on the Megablast match (blastn). 44 KB Open access
Supplementary table 2. Metrics of the genomic data used for the study. 9 KB Open access
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How to cite 

Thomas-Bulle Camille, Bertrand Denis, Nagarajan Niranjan, Copley Richard R., Corre Erwan, Hourdez Stéphane, Bonnivard Éric, Claridge-Chang Adam, Jollivet Didier (2022). Genomic patterns of divergence in the early and late steps of speciation of the deep-sea vent thermophilic worms of the genus Alvinella. Bmc Ecology And Evolution, 22(1), 106 (17p.). Publisher's official version : https://doi.org/10.1186/s12862-022-02057-y , Open Access version : https://archimer.ifremer.fr/doc/00791/90325/