Unity in diversity: morphological and genetic variability, integrative systematics, and phylogeography of the widespread nudibranch mollusc Onchidoris muricata

Abstract

Onchidoris muricata (Gastropoda: Nudibranchia: Onchidorididae) is a well-known nudibranch species, which has a wide amphiboreal range confirmed by molecular data. However, O. muricata shows a high degree of variation in external morphology among distant populations, which may indicate the presence of cryptic diversity within this species. There are also two closely related species with an unconfirmed taxonomic status, which were recently described from the northwestern Pacific based on morphological data. In this paper we study the taxonomic status and population structure of O. muricata based on an integrative approach combining morphological and molecular data and using O. muricata as a model we explore issues of boreal marine fauna connectivity and glaciation-driven isolation. The external morphology, spicule composition, and features of the buccal armature and the reproductive system were studied using light microscopy, scanning electron microscopy and mCT scan technology. The molecular study included various population genetic analyses as well as divergence time estimation and ancestral area reconstruction analyses. Onchidoris muricata represents a true amphiboreal species, which shows a high degree of heterogeneity in morphological characters, especially in the radular morphology and in features of the reproductive system. Our new data question the validity of the North-West Pacific species O. macropompa and O. pavli as the morphology of both these species fall within the phenotypic diversity of O. muricata. Although our sampling does not include the type localities of these two species, the observed morphological variability in O. muricata and the lack of molecular data for the North Pacific species O. macropompa and O. pavli suggest the latter two species are in fact part of O. muricata morphological diversity. Phylogeographic analyses indicate a genetic separation of the North Pacific and North Atlantic-Arctic populations of O. muricata, suggesting restricted gene flow between these areas. We show that this divergence may be a result of glacial cycles during the late Pleistocene, which were a key factor in the reduction of gene flow across the Arctic Ocean. Our molecular results also suggest that the White Sea population experienced a bottleneck event during the last Glacial Maximum.

Key words:

• Arctic
• Mollusca
• North-West Pacific
• radula
• species concept
• species delimitation
• spicule complex

Acknowledgments

We are deeply grateful to all friends and colleagues who kindly collected and supplied specimens for this study: WSBS Dive Team, especially A.A. Semenov and A. Mikhlina; Yu.V. Deart, Egersund Dive Team 2019, Tine Kinn Kvamme, Nils Aukan, Erling Svensen, Anders Schouw, Ole Meldahl and Justine Sigwald. We want to express our special gratitude to Andrey Shpatak, who kindly hosted us during numerous field trips to the Sea of Japan and supplied diving facilities, and also shared with us his beautiful photos and extensive observations on nudibranchs’ ecology in the Sea of Japan. Cessa Rauch is thanked for sequencing of specimens from Norway. We also want to thank Valentina Tambovtseva (Institute of Developmental Biology, Russian Academy of Sciences) for assistance in Sanger sequencing. Dr. Natalya N. Shunatova and Valeria Khabibulina (SPbU) are warmly thanked for invaluable help with the identification of host bryozoans. The light microscopy and molecular studies were conducted using equipment of the Invertebrate zoology Department MSU, the electron microscopy studies—using equipment of the Electron Microscopy Laboratory of the Shared Facilities Center of Lomonosov Moscow State University sponsored by the Reuter Foundation Ministry of Education and Science and Joint Usage Centre of N.A. Pertsov White Sea Biological Station MSU. Sanger sequencing was conducted using equipment of the Core Centrum of Institute of Developmental Biology RAS. This study was conducted in frame of the scientific project of the State Order of the Russian Federation Government to Lomonosov Moscow State University No. 122012100155-8 with financial support of Russian Science Foundation grant no. 20-74-10012 for collecting samples in Russian waters, their morphological and molecular analysis. Several samples used in this work were obtained during the project ‘The sea slugs of southern Norway: diversity, barcoding and invasive species’, funded by the Norwegian Taxonomy Initiative, Artsdatabanken Proj. No. 812038.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Supplemental material

Supplemental material for this article can be accessed here: https://dx.doi.org/10.1080/14772000.2023.2246472.

Associate Editor: Dr Barna Pall-Gergely