Department of Biological Sciences, California State University, Los Angeles, CA 90032-8201, USA.
University of California at Davis, Davis, CA, USA.
Proc Biol Sci. 2022 Apr 13;289(1972):20211855. doi: 10.1098/rspb.2021.1855. Epub 2022 Apr 6.
Transitions to terrestriality have been associated with major animal radiations including land snails and slugs in Stylommatophora (>20 000 described species), the most successful lineage of 'pulmonates' (a non-monophyletic assemblage of air-breathing gastropods). However, phylogenomic studies have failed to robustly resolve relationships among traditional pulmonates and affiliated marine lineages that comprise clade Panpulmonata (Mollusca, Gastropoda), especially two key taxa: Sacoglossa, a group including photosynthetic sea slugs, and Siphonarioidea, intertidal limpet-like snails with a non-contractile pneumostome (narrow opening to a vascularized pallial cavity). To clarify the evolutionary history of the panpulmonate radiation, we performed phylogenomic analyses on datasets of up to 1160 nuclear protein-coding genes for 110 gastropods, including 40 new transcriptomes for Sacoglossa and Siphonarioidea. All 18 analyses recovered Sacoglossa as the sister group to a clade we named Pneumopulmonata, within which Siphonarioidea was sister to the remaining lineages in most analyses. Comparative modelling indicated shifts to marginal habitat (estuarine, mangrove and intertidal zones) preceded and accelerated the evolution of a pneumostome, present in the pneumopulmonate ancestor along with a one-sided plicate gill. These findings highlight key intermediate stages in the evolution of air-breathing snails, supporting the hypothesis that adaptation to marginal zones played an important role in major sea-to-land transitions.
从海洋过渡到陆地与主要的动物辐射有关，包括陆地蜗牛和石磺目（Stylommatophora）中的石磺（超过 20,000 个已描述的物种），这是“肺螺类”（呼吸空气的腹足动物的一个非单系集合）中最成功的谱系。然而，系统基因组学研究未能可靠地解决传统肺螺类和包括泛肺螺类（Mollusca，Gastropoda）在内的相关海洋谱系之间的关系，特别是两个关键分类群：有肺螺类中的 Sacoglossa，这是一个包括光合海蜗牛的类群，以及前鳃类中的笠贝目，是一类具有非伸缩性肺口（通向血管化套膜腔的狭窄开口）的潮间带帽贝状蜗牛。为了阐明泛肺螺类辐射的进化历史，我们对 110 种腹足动物的多达 1160 个核蛋白编码基因数据集进行了系统基因组学分析，其中包括 Sacoglossa 和笠贝目 40 个新转录组。所有 18 个分析都将 Sacoglossa 恢复为我们命名为 Pneumopulmonata 的分支的姐妹群，在大多数分析中，笠贝目是该分支中其余谱系的姐妹群。比较建模表明，边缘生境（河口、红树林和潮间带）的转移先于并加速了肺口的进化，肺口存在于肺螺类的祖先中，同时还有单侧褶皱鳃。这些发现突出了呼吸空气蜗牛进化的关键中间阶段，支持了适应边缘带在主要的海到陆过渡中发挥重要作用的假说。
