Phylogenomic reconstruction of Solenogastres (Mollusca, Aplacophora) informs hypotheses on body size evolution.

ABSTRACT

Body size is a fundamental characteristic of animals that impacts every aspect of their biology from anatomical complexity to ecology. In Mollusca, Solenogastres has been considered important to understanding the group's early evolution as most morphology-based phylogenetic reconstructions placed it as an early branching molluscan lineage. Under this scenario, molluscs were thought to have evolved from a small, turbellarian-like ancestor and small (i.e., macrofaunal) body size was inferred to be plesiomorphic for Solenogastres. More recently, phylogenomic studies have shown that aplacophorans (Solenogastres + Caudofoveata) form a clade with chitons (Polyplacophora), which is sister to all other molluscs, suggesting a relatively large-bodied (i.e., megafaunal) ancestor for Mollusca. Meanwhile, recent investigations into aplacophoran phylogeny have called the assumption that the last common ancestor of Solenogastres was small-bodied into question, but sampling of meiofaunal species was limited, biasing these studies towards large-bodied taxa and leaving fundamental questions about solenogaster body size evolution unanswered. Here, we supplemented available data with transcriptomes from eight diverse meiofaunal species of Solenogastres and conducted phylogenomic analyses on datasets of up to 949 genes. Maximum likelihood analyses support the meiofaunal family Meiomeniidae as the sister group to all other solenogasters, congruent with earlier ideas of a small-bodied ancestor of Solenogastres. In contrast, Bayesian Inference analyses support the large-bodied family Amphimeniidae as the sister group to all other solenogasters. Investigation of phylogenetic signal by comparing site-wise likelihood scores for the two competing hypotheses support the Meiomeniidae-first topology. In light of these results, we performed ancestral character state reconstruction to explore the implications of both hypotheses on understanding of Solenogaster evolution and review previous hypotheses about body size evolution and its potential consequences for solenogaster biology. Both hypotheses imply that body size evolution has been highly dynamic over the course of solenogaster evolution and that their relatively static body plan has successfully allowed for evolutionary transitions between meio-, macro- and megafaunal size ranges.