Scaling the high latitudes: evolution, diversification, and dispersal of Coryphella nudibranchs across the Northern Hemisphere

Abstract

Nudibranch molluscs Coryphella are widely distributed and species-rich gastropod group lacking fossil record and displaying a complex distribution across both Southern and Northern hemispheres. In this paper we provide a detailed review of the morphology, ecology, and distribution of Coryphella, estimation of divergence times between species, an ancestral area reconstruction, and a population analysis of widely distributed trans-Arctic species Coryphella verrucosa to investigate the evolution, phylogeographic patterns and reconstruct possible historical routes of oceanic dispersal. The inclusion of a larger sample size and five molecular markers has revealed a complex evolutionary history of Coryphella, shaped by transgression, vicariance, and dietary shifts, and overall driven by the pervasive effect of glacial cycles. We also revealed the presence of additional cryptic diversity, which suggests that further sampling may produce additional species in this group of nudibranchs. Tree calibration indicates the genus Coryphella originates in the middle Miocene in the Pacific Ocean and the early divergence within this group also occurred in the Pacific, specifically in different regions of the North Pacific. The ancestral area reconstruction inferred five independent instances of transgression from the Pacific Ocean to the Atlantic via different migration routes, including the Panamanian seaway and the Bering Strait. Among them, we identified three cases of successful transition to the Arctic waters from the North Pacific via the Bering Strait, associated with interglacial conditions of middle Pleistocene. Consequently, Pleistocene glacial cycles likely prompted pulses of boreal faunal elements to disperse southwards followed by range disjunction and temporary isolation of distant populations and resulting in allopatric speciation. Evidence from the population structure of contemporary trans-Arctic species suggests an occurrence of independent recolonization pathways of Arctic waters from both southernly and northernly refugia after the Last Glacial Maximum.