Multiple paedomorphic lineages of soft-substrate burrowing invertebrates: parallels in the origin of Xenocratena and Xenoturbella

• Published in: PloS one 2020-01, Vol.15 (1), p.e0227173
• Main Authors: Martynov, Alexander, Lundin, Kennet, Picton, Bernard, Fletcher, Karin, Malmberg, Klas, Korshunova, Tatiana
• Format: Article
• Language: English
• Subjects: Animals; Arctic Regions; Bayes Theorem; Biodiversity; Biological diversity; Biological Evolution; Biology and Life Sciences; Computer and Information Sciences; Cumanotidae; DNA, Ribosomal - genetics; Environment; Environments; Evolution; Fjords; Funding; Gastropoda - anatomy & histology; Gastropoda - classification; Gastropoda - genetics; Invertebrates; Larva; Marine invertebrates; Markov Chains; Medicine and Health Sciences; Mollusks; Museums; Natural history; Nudibranchia; Oceans and Seas; Ontogeny; Phylogenetics; Phylogeny; Polymerase Chain Reaction; Shellfish; Subgroups; Substrates; Zoology
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0227173

Paedomorphosis is an important evolutionary force. It has previously been suggested that a soft-substrate sediment-dwelling (infaunal) environment facilitates paedomorphic evolution in marine invertebrates. However, until recently this proposal was never rigorously tested with robust phylogeny and broad taxon selection. Here, for the first time, we present a molecular phylogeny for a majority of the 21 families of one of the largest nudibranch subgroups (Aeolidacea) and show that the externally highly simplified vermiform nudibranch family, Pseudovermidae, with clearly defined paedomorphic traits and inhabiting a soft-substrata environment, is a sister group to the complex nudibranch family, Cumanotidae. We also report the rediscovery of one of the most enigmatic nudibranchs-Xenocratena suecica-on the Swedish and Norwegian coasts 70 years after it was first found. Xenocratena was described from the same location and environment in the Swedish Gullmar fjord as one of the most enigmatic vermiform organisms, Xenoturbella bocki, which represents either an original simple bilaterian body plan or secondary simplification of a more complex organisation. Our results show that Xenocratena suecica reveals an onset of parallel paedomorphic evolution so we have proposed the new family, Xenocratenidae fam. n., to accommodate the molecular and morphological disparities we discovered. The paedomorphic origin of another aeolidacean family, Embletoniidae, is also demonstrated for the first time. Thus, by presenting three independent lineages from non-closely related aeolidacean families, Xenocratenidae fam. n., Cumanotidae and Embletoniidae, we confirm with phylogenetic data that a soft-substrata burrowing-related environment strongly favours paedomorphic evolution. We suggest criteria to distinguish ancestral and derived characters in the context of modifications of ontogenetic cycles. Applying an evolutionary model of the soft substrate-driven multiple paedomorphic origin of several families of nudibranch molluscs we propose that it is plausible to extend this model to other marine invertebrates and suggest that the ancestral organisation of the enigmatic metazoan, Xenoturbella, might correspond to the larval part of a complex ancestral bilaterian ontogenetic cycle with sedentary/semi-sedentary adult stages and planula-like larval stages.