Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs

<p>Abstract</p> <p>Background</p> <p>Many marine meiofaunal species are reported to have wide distributions, which creates a paradox considering their hypothesized low dispersal abilities. Correlated with this paradox is an especially high taxonomic deficit for meiofaun...

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Main Authors: Jörger Katharina M, Norenburg Jon L, Wilson Nerida G, Schrödl Michael
Format: Article
Language:English
Published: BMC 2012-12-01
Series:BMC Evolutionary Biology
Online Access:http://www.biomedcentral.com/1471-2148/12/245
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author Jörger Katharina M
Norenburg Jon L
Wilson Nerida G
Schrödl Michael
author_facet Jörger Katharina M
Norenburg Jon L
Wilson Nerida G
Schrödl Michael
author_sort Jörger Katharina M
collection DOAJ
description <p>Abstract</p> <p>Background</p> <p>Many marine meiofaunal species are reported to have wide distributions, which creates a paradox considering their hypothesized low dispersal abilities. Correlated with this paradox is an especially high taxonomic deficit for meiofauna, partly related to a lower taxonomic effort and partly to a high number of putative cryptic species. Molecular-based species delineation and barcoding approaches have been advocated for meiofaunal biodiversity assessments to speed up description processes and uncover cryptic lineages. However, these approaches show sensitivity to sampling coverage (taxonomic and geographic) and the success rate has never been explored on mesopsammic Mollusca.</p> <p>Results</p> <p>We collected the meiofaunal sea-slug <it>Pontohedyle</it> (Acochlidia, Heterobranchia) from 28 localities worldwide. With a traditional morphological approach, all specimens fall into two morphospecies. However, with a multi-marker genetic approach, we reveal multiple lineages that are reciprocally monophyletic on single and concatenated gene trees in phylogenetic analyses. These lineages are largely concordant with geographical and oceanographic parameters, leading to our primary species hypothesis (PSH). In parallel, we apply four independent methods of molecular based species delineation: General Mixed Yule Coalescent model (GMYC), statistical parsimony, Bayesian Species Delineation (BPP) and Automatic Barcode Gap Discovery (ABGD). The secondary species hypothesis (SSH) is gained by relying only on uncontradicted results of the different approaches (‘minimum consensus approach’), resulting in the discovery of a radiation of (at least) 12 mainly cryptic species, 9 of them new to science, some sympatric and some allopatric with respect to ocean boundaries. However, the meiofaunal paradox still persists in some <it>Pontohedyle</it> species identified here with wide coastal and trans-archipelago distributions.</p> <p>Conclusions</p> <p>Our study confirms extensive, morphologically cryptic diversity among meiofauna and accentuates the taxonomic deficit that characterizes meiofauna research. We observe for <it>Pontohedyle</it> slugs a high degree of morphological simplicity and uniformity, which we expect might be a general rule for meiofauna. To tackle cryptic diversity in little explored and hard-to-sample invertebrate taxa, at present, a combined approach seems most promising, such as multi-marker-barcoding (i.e., molecular systematics using mitochondrial and nuclear markers and the criterion of reciprocal monophyly) combined with a minimum consensus approach across independent methods of molecular species delineation to define candidate species.</p>
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spelling doaj.art-8879aea077824ef8903a5d60da9c0cca2022-12-22T04:07:42ZengBMCBMC Evolutionary Biology1471-21482012-12-0112124510.1186/1471-2148-12-245Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugsJörger Katharina MNorenburg Jon LWilson Nerida GSchrödl Michael<p>Abstract</p> <p>Background</p> <p>Many marine meiofaunal species are reported to have wide distributions, which creates a paradox considering their hypothesized low dispersal abilities. Correlated with this paradox is an especially high taxonomic deficit for meiofauna, partly related to a lower taxonomic effort and partly to a high number of putative cryptic species. Molecular-based species delineation and barcoding approaches have been advocated for meiofaunal biodiversity assessments to speed up description processes and uncover cryptic lineages. However, these approaches show sensitivity to sampling coverage (taxonomic and geographic) and the success rate has never been explored on mesopsammic Mollusca.</p> <p>Results</p> <p>We collected the meiofaunal sea-slug <it>Pontohedyle</it> (Acochlidia, Heterobranchia) from 28 localities worldwide. With a traditional morphological approach, all specimens fall into two morphospecies. However, with a multi-marker genetic approach, we reveal multiple lineages that are reciprocally monophyletic on single and concatenated gene trees in phylogenetic analyses. These lineages are largely concordant with geographical and oceanographic parameters, leading to our primary species hypothesis (PSH). In parallel, we apply four independent methods of molecular based species delineation: General Mixed Yule Coalescent model (GMYC), statistical parsimony, Bayesian Species Delineation (BPP) and Automatic Barcode Gap Discovery (ABGD). The secondary species hypothesis (SSH) is gained by relying only on uncontradicted results of the different approaches (‘minimum consensus approach’), resulting in the discovery of a radiation of (at least) 12 mainly cryptic species, 9 of them new to science, some sympatric and some allopatric with respect to ocean boundaries. However, the meiofaunal paradox still persists in some <it>Pontohedyle</it> species identified here with wide coastal and trans-archipelago distributions.</p> <p>Conclusions</p> <p>Our study confirms extensive, morphologically cryptic diversity among meiofauna and accentuates the taxonomic deficit that characterizes meiofauna research. We observe for <it>Pontohedyle</it> slugs a high degree of morphological simplicity and uniformity, which we expect might be a general rule for meiofauna. To tackle cryptic diversity in little explored and hard-to-sample invertebrate taxa, at present, a combined approach seems most promising, such as multi-marker-barcoding (i.e., molecular systematics using mitochondrial and nuclear markers and the criterion of reciprocal monophyly) combined with a minimum consensus approach across independent methods of molecular species delineation to define candidate species.</p>http://www.biomedcentral.com/1471-2148/12/245
spellingShingle Jörger Katharina M
Norenburg Jon L
Wilson Nerida G
Schrödl Michael
Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs
BMC Evolutionary Biology
title Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs
title_full Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs
title_fullStr Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs
title_full_unstemmed Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs
title_short Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs
title_sort barcoding against a paradox combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs
url http://www.biomedcentral.com/1471-2148/12/245
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