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.