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

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 1,160 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 modeling
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.