Phylogenomics supports Panpulmonata: opisthobranch paraphyly and key evolutionary steps in a major radiation of gastropod molluscs

Abstract

Pulmonates, with over 30,000 described species, represent the largest radiation of non-marine animals outside of Arthropoda. The pulmonate lung was a key evolutionary innovation enabling diversification of terrestrial and freshwater snails and slugs. However, recent studies drew conflicting conclusions about pulmonate monophyly, and support for a sister group is lacking, hindering our understanding of this major animal radiation. Analyses of mitochondrial protein-coding genes recovered a paraphyletic Pulmonata grading into a monophyletic Opisthobranchia, a traditional group of sea slugs long considered sister to pulmonates. Conversely, analyses of datsets dominated by nuclear rDNA indicated Opisthobranchia is paraphyletic with respect to Pulmonata. No study resolved the placement of two key taxa: Sacoglossa, an opisthobranch group including photosynthetic sea slugs, and Siphonarioidea, intertidal limpet-like snails traditionally in Pulmonata. To examine evolutionary relationships at the base of the pulmonate radiation, we performed a phylogenomic analysis of 102 nuclear protein-coding gene regions for 19 gastropods. Opisthobranchia was recovered as paraphyletic with respect to Panpulmonata, a clade in which Sacoglossa was sister to Pulmonata, with Siphonarioidea as the basal pulmonate lineage. Siphonarioideans share a similar gill structure with shelled sacoglossans but lack the contractile pneumostome of pulmonates, suggesting descent from an evolutionary intermediate that facilitated the pulmonate radiation into non-marine habitats.

Keywords: Gastropoda; Heterobranch; Opisthobranch; Phylogenomics; Pulmonate; Radiation.