Regional differentiation and extensive hybridization between mitochondrial clades of the Southern Ocean giant sea spider Colossendeis megalonyx.

Lars Dietz,Nerida G Wilson,Christoph Held,Andrew R Mahon,Jana S Dömel,Andrea Weis,Roland R Melzer,Kenneth M Halanych,Christoph Mayer,Claudia P Arango,Florian Leese,Greg W Rouse,Avril M Harder

doi:10.1098/rsos.140424

Abstract

Assessing the enormous diversity of Southern Ocean benthic species and their evolutionary histories is a central task in the era of global climate change. Based on mitochondrial markers, it was recently suggested that the circumpolar giant sea spider Colossendeis megalonyx comprises a complex of at least six cryptic species with mostly small and non-overlapping distribution ranges. Here, we expand the sampling to include over 500 mitochondrial COI sequences of specimens from around the Antarctic. Using multiple species delimitation approaches, the number of distinct mitochondrial OTUs increased from six to 15–20 with our larger dataset. In contrast to earlier studies, many of these clades show almost circumpolar distributions. Additionally, analysis of the nuclear internal transcribed spacer region for a subset of these specimens showed incongruence between nuclear and mitochondrial results. These mito-nuclear discordances suggest that several of the divergent mitochondrial lineages can hybridize and should not be interpreted as cryptic species. Our results suggest survival of C. megalonyx during Pleistocene glaciations in multiple refugia, some of them probably located on the Antarctic shelf, and emphasize the importance of multi-gene datasets to detect the presence of cryptic species, rather than their inference based on mitochondrial data alone.

Highlights

Species diversity in the marine Antarctic benthos is severely underestimated [1,2,3]
Our results suggest survival of C. megalonyx during Pleistocene glaciations in multiple refugia, some of them probably located on the Antarctic shelf, and emphasize the importance of multi-gene datasets to detect the presence of cryptic species, rather than their inference based on mitochondrial data alone
A 658 bp fragment of the mitochondrial c oxidase subunit I (COI) gene was sequenced for a total of 418 putative C. megalonyx specimens from different parts of the Southern Ocean and for an additional 82 specimens belonging to other colossendeid species

Summary

Introduction

Species diversity in the marine Antarctic benthos is severely underestimated [1,2,3]. One of the main reasons for this problem is still the limited sampling of remote regions and habitats such as the continental slope [4]. Another major challenge is the presence of cryptic or overlooked species, i.e. species that are currently not distinguished morphologically but are genetically distinct (see [5] for a review). Identification of cryptic species with molecular-based tools in a variety of Antarctic invertebrates has questioned this concept as several of these cryptic species show a very strong regional differentiation, in brooders with a holobenthic lifestyle (i.e. no planktonic dispersal stage, see [15] for a review). Morphological investigations support the distinction of previously unrecognized species that were identified with molecular data (e.g. [25,26,27,28,29])

Methods

Results

Conclusion