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Unravelling population genetic structure with mitochondrial DNA in a notional panmictic coastal crab species: sample size makes the difference

BACKGROUND: The extent of genetic structure of a species is determined by the amount of current gene flow and the impact of historical and demographic factors. Most marine invertebrates have planktonic larvae and consequently wide potential dispersal, so that genetic uniformity should be common. How...

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Autores principales: Fratini, Sara, Ragionieri, Lapo, Deli, Temim, Harrer, Alexandra, Marino, Ilaria A. M., Cannicci, Stefano, Zane, Lorenzo, Schubart, Christoph D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4960869/
https://www.ncbi.nlm.nih.gov/pubmed/27455997
http://dx.doi.org/10.1186/s12862-016-0720-2
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author Fratini, Sara
Ragionieri, Lapo
Deli, Temim
Harrer, Alexandra
Marino, Ilaria A. M.
Cannicci, Stefano
Zane, Lorenzo
Schubart, Christoph D.
author_facet Fratini, Sara
Ragionieri, Lapo
Deli, Temim
Harrer, Alexandra
Marino, Ilaria A. M.
Cannicci, Stefano
Zane, Lorenzo
Schubart, Christoph D.
author_sort Fratini, Sara
collection PubMed
description BACKGROUND: The extent of genetic structure of a species is determined by the amount of current gene flow and the impact of historical and demographic factors. Most marine invertebrates have planktonic larvae and consequently wide potential dispersal, so that genetic uniformity should be common. However, phylogeographic investigations reveal that panmixia is rare in the marine realm. Phylogeographic patterns commonly coincide with geographic transitions acting as barriers to gene flow. In the Mediterranean Sea and adjoining areas, the best known barriers are the Atlantic-Mediterranean transition, the Siculo-Tunisian Strait and the boundary between Aegean and Black seas. Here, we perform the so far broadest phylogeographic analysis of the crab Pachygrapsus marmoratus, common across the north-eastern Atlantic Ocean, Mediterranean and Black seas. Previous studies revealed no or weak genetic structuring at meso-geographic scale based on mtDNA, while genetic heterogeneity at local scale was recorded with microsatellites, even if without clear geographic patterns. Continuing the search for phylogeographic signal, we here enlarge the mtDNA dataset including 51 populations and covering most of the species’ distribution range. RESULTS: This enlarged dataset provides new evidence of three genetically separable groups, corresponding to the Portuguese Atlantic Ocean, Mediterranean Sea plus Canary Islands, and Black Sea. Surprisingly, hierarchical AMOVA and Principal Coordinates Analysis agree that our Canary Islands population is closer to western Mediterranean populations than to mainland Portugal and Azores populations. Within the Mediterranean Sea, we record genetic homogeneity, suggesting that population connectivity is unaffected by the transition between the western and eastern Mediterranean. The Mediterranean metapopulation seems to have experienced a relatively recent expansion around 100,000 years ago. CONCLUSIONS: Our results suggest that the phylogeographic pattern of P. marmoratus is shaped by the geological history of Mediterranean and adjacent seas, restricted current gene flow among different marginal seas, and incomplete lineage sorting. However, they also caution from exclusively testing well-known biogeographic barriers, thereby neglecting other possible phylogeographic patterns. Mostly, this study provides evidence that a geographically exhaustive dataset is necessary to detect shallow phylogeographic structure within widespread marine species with larval dispersal, questioning all studies where species have been categorized as panmictic based on numerically and geographically limited datasets. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0720-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-49608692016-07-27 Unravelling population genetic structure with mitochondrial DNA in a notional panmictic coastal crab species: sample size makes the difference Fratini, Sara Ragionieri, Lapo Deli, Temim Harrer, Alexandra Marino, Ilaria A. M. Cannicci, Stefano Zane, Lorenzo Schubart, Christoph D. BMC Evol Biol Research Article BACKGROUND: The extent of genetic structure of a species is determined by the amount of current gene flow and the impact of historical and demographic factors. Most marine invertebrates have planktonic larvae and consequently wide potential dispersal, so that genetic uniformity should be common. However, phylogeographic investigations reveal that panmixia is rare in the marine realm. Phylogeographic patterns commonly coincide with geographic transitions acting as barriers to gene flow. In the Mediterranean Sea and adjoining areas, the best known barriers are the Atlantic-Mediterranean transition, the Siculo-Tunisian Strait and the boundary between Aegean and Black seas. Here, we perform the so far broadest phylogeographic analysis of the crab Pachygrapsus marmoratus, common across the north-eastern Atlantic Ocean, Mediterranean and Black seas. Previous studies revealed no or weak genetic structuring at meso-geographic scale based on mtDNA, while genetic heterogeneity at local scale was recorded with microsatellites, even if without clear geographic patterns. Continuing the search for phylogeographic signal, we here enlarge the mtDNA dataset including 51 populations and covering most of the species’ distribution range. RESULTS: This enlarged dataset provides new evidence of three genetically separable groups, corresponding to the Portuguese Atlantic Ocean, Mediterranean Sea plus Canary Islands, and Black Sea. Surprisingly, hierarchical AMOVA and Principal Coordinates Analysis agree that our Canary Islands population is closer to western Mediterranean populations than to mainland Portugal and Azores populations. Within the Mediterranean Sea, we record genetic homogeneity, suggesting that population connectivity is unaffected by the transition between the western and eastern Mediterranean. The Mediterranean metapopulation seems to have experienced a relatively recent expansion around 100,000 years ago. CONCLUSIONS: Our results suggest that the phylogeographic pattern of P. marmoratus is shaped by the geological history of Mediterranean and adjacent seas, restricted current gene flow among different marginal seas, and incomplete lineage sorting. However, they also caution from exclusively testing well-known biogeographic barriers, thereby neglecting other possible phylogeographic patterns. Mostly, this study provides evidence that a geographically exhaustive dataset is necessary to detect shallow phylogeographic structure within widespread marine species with larval dispersal, questioning all studies where species have been categorized as panmictic based on numerically and geographically limited datasets. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0720-2) contains supplementary material, which is available to authorized users. BioMed Central 2016-07-26 /pmc/articles/PMC4960869/ /pubmed/27455997 http://dx.doi.org/10.1186/s12862-016-0720-2 Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Fratini, Sara
Ragionieri, Lapo
Deli, Temim
Harrer, Alexandra
Marino, Ilaria A. M.
Cannicci, Stefano
Zane, Lorenzo
Schubart, Christoph D.
Unravelling population genetic structure with mitochondrial DNA in a notional panmictic coastal crab species: sample size makes the difference
title Unravelling population genetic structure with mitochondrial DNA in a notional panmictic coastal crab species: sample size makes the difference
title_full Unravelling population genetic structure with mitochondrial DNA in a notional panmictic coastal crab species: sample size makes the difference
title_fullStr Unravelling population genetic structure with mitochondrial DNA in a notional panmictic coastal crab species: sample size makes the difference
title_full_unstemmed Unravelling population genetic structure with mitochondrial DNA in a notional panmictic coastal crab species: sample size makes the difference
title_short Unravelling population genetic structure with mitochondrial DNA in a notional panmictic coastal crab species: sample size makes the difference
title_sort unravelling population genetic structure with mitochondrial dna in a notional panmictic coastal crab species: sample size makes the difference
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4960869/
https://www.ncbi.nlm.nih.gov/pubmed/27455997
http://dx.doi.org/10.1186/s12862-016-0720-2
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