Genetic and Morphological Divergences in the Cosmopolitan Deep-Sea Amphipod Eurythenes gryllus Reveal a Diverse Abyss and a Bipolar Species

Charlotte Havermans,Torben Riehl,Cédric d’Udekem d’Acoz,Shobhit Agrawal,Zoltán T. Nagy,Gontran Sonet,Patrick Martin,Saskia Brix,Christoph Held,Diego Fontaneto

doi:10.1371/journal.pone.0074218

Abstract

Eurythenes gryllus is one of the most widespread amphipod species, occurring in every ocean with a depth range covering the bathyal, abyssal and hadal zones. Previous studies, however, indicated the existence of several genetically and morphologically divergent lineages, questioning the assumption of its cosmopolitan and eurybathic distribution. For the first time, its genetic diversity was explored at the global scale (Arctic, Atlantic, Pacific and Southern oceans) by analyzing nuclear (28S rDNA) and mitochondrial (COI, 16S rDNA) sequence data using various species delimitation methods in a phylogeographic context. Nine putative species-level clades were identified within E. gryllus. A clear distinction was observed between samples collected at bathyal versus abyssal depths, with a genetic break occurring around 3,000 m. Two bathyal and two abyssal lineages showed a widespread distribution, while five other abyssal lineages each seemed to be restricted to a single ocean basin. The observed higher diversity in the abyss compared to the bathyal zone stands in contrast to the depth-differentiation hypothesis. Our results indicate that, despite the more uniform environment of the abyss and its presumed lack of obvious isolating barriers, abyssal populations might be more likely to show population differentiation and undergo speciation events than previously assumed. Potential factors influencing species’ origins and distributions, such as hydrostatic pressure, are discussed. In addition, morphological findings coincided with the molecular clades. Of all specimens available for examination, those of the bipolar bathyal clade seemed the most similar to the ‘true’ E. gryllus. We present the first molecular evidence for a bipolar distribution in a macro-benthic deep-sea organism.

Highlights

The deep sea represents the largest ecosystem on our planet, yet our awareness of its fauna is remarkably recent, dating back to the Challenger expedition (1872–1876) (e.g. [1])
The supposed lack of isolating barriers in the deep sea and the global uniformity of its environment contributed to the belief in cosmopolitan distributions of taxa (e.g. [6])
The aligned characterized by low genetic divergences (COI) sequences consisted of 658 bases, of which 119 were parsimonyinformative

Summary

Introduction

The deep sea represents the largest ecosystem on our planet, yet our awareness of its fauna is remarkably recent, dating back to the Challenger expedition (1872–1876) (e.g. [1]). The deep sea represents the largest ecosystem on our planet, yet our awareness of its fauna is remarkably recent, dating back to the Challenger expedition (1872–1876) The supposed lack of isolating barriers in the deep sea and the global uniformity of its environment contributed to the belief in cosmopolitan distributions of taxa Observed bathymetric patterns in diversity suggest a maximal diversity at bathyal depths, decreasing towards the abyss [7,8]. The bathyal region is characterized by stronger abiotic and biotic gradients and greater habitat heterogeneity in comparison to the abyss. Population differentiation, and speciation events, are supposed to be more common in the bathyal zone (i.e. the depth-differentiation hypothesis, reviewed in [9])

Methods

Results

Discussion

Conclusion