Phylogenomic resolution of the root of Panpulmonata, a hyperdiverse radiation of gastropods: new insight into the evolution of air breathing

Abstract

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.

Parallel duplication and loss of aquaporin‐coding genes during the “out of the sea” transition as potential key drivers of animal terrestrialization

“…It is noteworthy that the exclusively terrestrial Aqp3-ann2 clade clustered together with Aqp3-mol3, which contains aquaporins from mostly terrestrial panpulmonate gastropods, Caudofoveata and Cephalopoda. Concerning molluscs, we report a duplication of Aqp3-mol2 in the freshwater-origin molluscan subclass Caenogastropoda (Figure 4a, Krug et al, 2022), that was subsequently lost in the only marine species we included in our data set (Hinea brasiliana, HBRA1). The presence or absence of this duplication in other Caenogastropoda marine species remains to be studied, but the presence of both copies in the terrestrial P. elegans (PELE1) suggests that it was at least retained in the common ancestor of this species with other marine members of the group.…”

“…The ecological transitions of gastropods to land, either through a freshwater path or marginal environments (Krug et al, 2022; van Straalen, 2021; Vermeij & Watson‐Zink, 2022), could have been facilitated by aquaporins evolution. Our independent comparative phylogenetic analyses for each type of Aqp‐coding gene revealed a significantly higher number in nonmarine species of Aqp1‐like and Aqp8‐like (Figure 2b, right).…”

“…Other terrestrialization events that have recently gained interest are the ones in molluscs and annelids. In the case of molluscs, gastropods have independently colonized land more than nine times (Kameda & Kato, 2011), with the latest estimates suggesting up to 30 times (Vermeij & Watson‐Zink, 2022), either following a freshwater route or through marginal environments such as brackish water (Krug et al, 2022; van Straalen, 2021; Vermeij & Watson‐Zink, 2022). Among them, the most successful terrestrial gastropod lineage is the Stylommatophora, an order of air‐breathing pulmonate land gastropods that contains most living terrestrial snails and slugs.…”

Parallel duplication and loss of aquaporin-coding genes during the ‘out of the sea’ transition as potential key drivers of animal terrestrialization

“…The transition of gastropods to land, either through a freshwater path or marginal environments (Krug et al, 2022; van Straalen, 2021; Vermeij & Watson-Zink, 2022), could have been facilitated by aquaporins evolution. Our independent comparative phylogenetic analyses for each type of Aqp-coding gene revealed a significantly higher number in non-marine species of Aqp1-like and Aqp8-like (Fig 2B, right).…”

“…Other terrestrialization events that have recently gained interest are the ones in molluscs and annelids. In the case of molluscs, gastropods have independently colonised land more than 9 times (Kameda & Kato, 2011), with the latest estimates suggesting up to 30 times (Vermeij & Watson-Zink, 2022), either following a freshwater route or through marginal environments such as brackish water (Krug et al, 2022; van Straalen, 2021; Vermeij & Watson-Zink, 2022). Among them, the most successful terrestrial gastropod lineage is the Stylommatophora, an order of air-breathing pulmonate land gastropods that contains most living snails and slugs.…”