Diet-driven ecological radiation and allopatric speciation result in high species diversity in a temperate-cold water marine genus Dendronotus (Gastropoda: Nudibranchia)

Abstract

While the majority nudibranch clades are more species rich in the tropics, the genus Dendronotus is mainly represented in Arctic and boreal regions. This distribution pattern remains poorly understood. An integrative approach and novel data provided valuable insights into processes driving Dendronotus radiation and speciation. We propose an evolutionary scenario based on molecular phylogenetics and morphological, ecological, ontogenetic data, combined with data on complex geology and paleoclimatology of this region. Estimated phylogenetic relationships based on four molecular markers (COI, 16S, H3 and 28S) shows strong correlation with radular morphology, diet and biogeographical pattern. Ancestral area reconstruction (AAR) provides evidence for a tropical Pacific origin of the genus. Based on AAR and divergence time estimates we conclude that the evolution of Dendronotus has been shaped by different processes: initial migration out of the tropics, diet-driven adaptive radiation in the North Pacific influenced by Miocene climate change, and subsequent allopatric speciation resulting from successive closings of the Bering strait and cooling of the Arctic Ocean during the Pliocene-Pleistocene. At the same time, contemporary amphiboreal species appear to have dispersed into the Atlantic fairly recently.