Dynamique de la Diversité Marine (DyDiv) Lab, Station Biologique de Roscoff, Sorbonne Université, CNRS, UMR 7144 AD2M, Place G. Teissier CS90074, 29680, Roscoff, France.
Division of Biological Sciences, University of Montana, Missoula, MT, USA.
BMC Ecol Evol. 2022 Sep 3;22(1):106. doi: 10.1186/s12862-022-02057-y.
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.
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.
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.
深海热液环境由海脊俯冲、板块碰撞和新裂隙的出现组成，其具有短暂和分散的特点，目前正在促使喷口种群分离，促进局部适应，并促成物种形成和物种特化的爆发。管栖蠕虫 Alvinella pompejana 被称为庞贝蠕虫及其姐妹种 A. caudata 生活在东太平洋海隆深海热液烟囱最热的部分。它们暴露在极端的热和化学梯度中，这些梯度在空间和时间上变化很大，因此是了解在喷口动物群进化中起作用的进化机制的理想候选者。
我们使用转录组组装和第一个基因组草案探索了这些标志性蠕虫在物种形成的早期和晚期的基因组分化模式，以更好地了解地理隔离和栖息地偏好在其基因组进化中的相对作用。对 Alvinella pompejana 的异地种群（分离的早期阶段）和 A. pompejana 与其同域种 Alvinella caudata 之间（物种形成的晚期阶段）进行了分析。我们首先确定了分化的基因组区域和选择的靶标及其在基因组中的位置，然后通过记录参与隔离过程的最分化和/或正选择基因的注释，描述了物种形成的动态。基因映射清楚地表明，与物种形成的早期阶段相关的分化基因，尽管占基因的近 30%，但在基因组中高度分散，没有任何分化岛，也不参与配子识别或线粒体核不相容性。相比之下，A. pompejana 和 A. caudata 的基因组明显分离，几乎所有基因（96%）都表现出高度的分化。然而，这种凝固效应似乎与栖息地特化有关，并且仍然允许对参与配子识别的基因进行正选择，这可能是一个长期的物种强化过程。
我们的分析强调了自然选择在标志性嗜热蠕虫生活在深海热液烟囱壁上的物种形成的早期和晚期阶段都发挥了不可忽视的作用。它们揭示了在非常长的时间内物种形成和物种特化过程中基因分化的演变。
