Speciation in the dark: diversification and biogeography of the deep-sea gastropod genus Scaphander in the Atlantic Ocean.

Mari H Eilertsen,Manuel António E Malaquias

doi:10.1111/jbi.12471

Abstract

AimThe aim of this work was to improve understanding about the mode, geography and tempo of diversification in deep‐sea organisms, using a time‐calibrated molecular phylogeny of the heterobranch gastropod genus Scaphander.LocationAtlantic and Indo‐West Pacific (IWP) oceans.MethodsTwo mitochondrial gene markers (COI and 16S) and one nuclear ribosomal gene (28S) from six Atlantic species of Scaphander, and four IWP species were used to generate a multilocus phylogenetic hypothesis using uncorrelated relaxed‐clock Bayesian methods implemented in beast and calibrated with the first occurrence of Scaphander in the fossil record (58.7–55.8 Ma).ResultsTwo main clades were supported: clade A, with sister relationships between species and subclades from the Atlantic and IWP; and clade B, with two western Atlantic sister species. Our estimates indicate that the two earliest divergences in clade A occurred between the middle Eocene and late Miocene and the most recent speciation occurred within the middle Miocene to Pleistocene. The divergence between the two western Atlantic species in clade B was estimated at late Oligocene–Pliocene.Main conclusionsThe prevailing mode of speciation in Scaphander was allopatric, but one possible case of sympatric speciation was detected between two western Atlantic species. Sister relationships between IWP and Atlantic lineages suggest the occurrence both of vicariance events caused by the closure of the Tethyan Seaway and of dispersal between the two ocean basins, probably around South Africa during episodic disruptions of the deep‐sea regional current system caused by glacial–interglacial cycles. Cladogenetic estimates do not support comparatively older diversification of deep‐sea faunas, but corroborate the hypothesis of a pulse of diversification centred in the Oligocene and Miocene epochs. Amphi‐Atlantic species were found to occur at deeper depths (bathyal–abyssal) and we hypothesize that trans‐Atlantic connectivity is maintained by dispersal between neighbouring reproductive populations inhabiting the abyssal sea floor and by dispersal across the shelf and slope of Arctic and sub‐Arctic regions.

Highlights

Little is known about the biogeography and speciation mechanisms of deep-sea (> 200 m deep) organisms (Thistle, 2003)
Sister relationships between Indo-West Pacific (IWP) and Atlantic lineages suggest the occurrence both of vicariance events caused by the closure of the Tethyan Seaway and of dispersal between the two ocean basins, probably around South Africa during episodic disruptions of the deep-sea regional current system caused by glacial–interglacial cycles
Amphi-Atlantic species were found to occur at deeper depths and we hypothesize that trans-Atlantic connectivity is maintained by dispersal between neighbouring reproductive populations inhabiting the abyssal sea floor and by dispersal across the shelf and slope of Arctic and sub-Arctic regions

Summary

Introduction

Little is known about the biogeography and speciation mechanisms of deep-sea (> 200 m deep) organisms (Thistle, 2003) This is in sharp contrast with shallow-water faunas, where the advent of molecular phylogenetic methods during the last 20 years has led to a profusion of studies that improve our understanding of the origins of species and patterns of diversity E. Malaquias have the same impact in the deep sea, but a common period of diversification for both shallow and deep-water faunas was recently suggested around the Oligocene and Miocene epochs, probably influenced by global warming, high levels of tectonic activity and changes in oceanic currents (Williams & Duda, 2008; Cabezas et al, 2012; Williams et al, 2013)

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