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

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.

The diversification of the antimicrobial peptides from marine worms is driven by environmental conditions

“…pompejana and A. caudata) sharing the same hydrothermal vent conditions, showed no differences of the AMP sequence over a geographic range spanning the 6.000 km of the East Pacific Rise (Bulle et al, 2022) (Papot et al, 2017). Despite multiple genetic duplications the ALV precursor gene in both sister species (Papot et al, 2017), sharing the same biotic and abiotic environmental conditions constitutes a strong genetic purifying mean of maintaining exactly the same AMP to interact with common microbiome during the evolution race (Bulmer and Crozier, 2004;Fuller et al, 2011).…”

Chromosome-scale genome assembly and gene annotation of the hydrothermal vent annelidAlvinella pompejanayield insight into animal evolution in extreme environments

“…We confirmed this finding here using 3.33 million SNPs obtained after the WGS data processing. The genetic differentiation between individuals on either side of the Equator was much higher than expectation based on the divergence of genes [24] ( Figure 3a ), with an average 70% polymorphism identity between individuals of the same population but 50% between the southern and northern populations. The differentiation is, however, unevenly distributed with some portions of chromosome highly differentiated and others not ( Figure 3b ).…”

“…As episymbionts are found mainly on the dorsal surface of the worm body, it seems likely that we have avoided bacterial sequencing to a large extent. In contrast, an earlier draft of the A. pompejana genome, assembled from different sequence reads, does appear to contain an extensive set of proteins from Bacteria (see methods and Table S6 ), with best hits including sequences labelled as Alvinella pompejana symbionts, epsilonproteobacteria (Campylobacterota), the sulfate reducing Desulfobulbus and metabolically significant genes such as dissimilatory sulfite reductase ( Table S7 ) [24,40,41].…”

“…Recently, a fragmented whole genome sequence of Alvinella pompejana was analysed together with its transcriptome to explore the genomic patterns in the diversification of A. pompejana and the closely related A. caudata [24]. A sub-chromosome level genome of Paralvinella palmiformis has been reported and analysed within the context of an epigenome study, without extensive study of its protein coding gene set [25].…”

Genomic clustering by geography not species in taxonomically complex British and Irish eyebrights (Euphrasia)

“…Our study adds to our growing understanding of the extent of sequence similarity between closely related allopatric taxa, with a dramatic case where species are more closely related to neighbouring samples than other conspecific individuals. In the future, whole-genome sequencing of Euphrasia species at different stages of the speciation continuum (Thomas-Bulle et al, 2022) will help us understand the accumulation of genetic barriers to gene flow and the factors that promote or prevent divergence.…”