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Temporal genetic structure in a poecilogonous polychaete: the interplay of developmental mode and environmental stochasticity

BACKGROUND: Temporal variation in the genetic structure of populations can be caused by multiple factors, including natural selection, stochastic environmental variation, migration, or genetic drift. In benthic marine species, the developmental mode of larvae may indicate a possibility for temporal...

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Autores principales: Kesäniemi, Jenni E, Mustonen, Marina, Boström, Christoffer, Hansen, Benni W, Knott, K Emily
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3905951/
https://www.ncbi.nlm.nih.gov/pubmed/24447386
http://dx.doi.org/10.1186/1471-2148-14-12
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author Kesäniemi, Jenni E
Mustonen, Marina
Boström, Christoffer
Hansen, Benni W
Knott, K Emily
author_facet Kesäniemi, Jenni E
Mustonen, Marina
Boström, Christoffer
Hansen, Benni W
Knott, K Emily
author_sort Kesäniemi, Jenni E
collection PubMed
description BACKGROUND: Temporal variation in the genetic structure of populations can be caused by multiple factors, including natural selection, stochastic environmental variation, migration, or genetic drift. In benthic marine species, the developmental mode of larvae may indicate a possibility for temporal genetic variation: species with dispersive planktonic larvae are expected to be more likely to show temporal genetic variation than species with benthic or brooded non-dispersive larvae, due to differences in larval mortality and dispersal ability. We examined temporal genetic structure in populations of Pygospio elegans, a poecilogonous polychaete with within-species variation in developmental mode. P. elegans produces either planktonic, benthic, or intermediate larvae, varying both among and within populations, providing a within-species test of the generality of a relationship between temporal genetic variation and larval developmental mode. RESULTS: In contrast to our expectations, our microsatellite analyses of P. elegans revealed temporal genetic stability in the UK population with planktonic larvae, whereas there was variation indicative of drift in temporal samples of the populations from the Baltic Sea, which have predominantly benthic and intermediate larvae. We also detected temporal variation in relatedness within these populations. A large temporal shift in genetic structure was detected in a population from the Netherlands, having multiple developmental modes. This shift could have been caused by local extiction due to extreme environmental conditions and (re)colonization by planktonic larvae from neighboring populations. CONCLUSIONS: In our study of P. elegans, temporal genetic variation appears to be due to not only larval developmental mode, but also the stochastic environment of adults. Large temporal genetic shifts may be more likely in marine intertidal habitats (e.g. North Sea and Wadden Sea) which are more prone to environmental stochasticity than the sub-tidal Baltic habitats. Sub-tidal and/or brackish (less saline) habitats may support smaller P. elegans populations and these may be more susceptible to the effects of random genetic drift. Moreover, higher frequencies of asexual reproduction and the benthic larval developmental mode in these populations leads to higher relatedness and contributes to drift. Our results indicate that a general relationship between larval developmental mode and temporal genetic variation may not exist.
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spelling pubmed-39059512014-01-30 Temporal genetic structure in a poecilogonous polychaete: the interplay of developmental mode and environmental stochasticity Kesäniemi, Jenni E Mustonen, Marina Boström, Christoffer Hansen, Benni W Knott, K Emily BMC Evol Biol Research Article BACKGROUND: Temporal variation in the genetic structure of populations can be caused by multiple factors, including natural selection, stochastic environmental variation, migration, or genetic drift. In benthic marine species, the developmental mode of larvae may indicate a possibility for temporal genetic variation: species with dispersive planktonic larvae are expected to be more likely to show temporal genetic variation than species with benthic or brooded non-dispersive larvae, due to differences in larval mortality and dispersal ability. We examined temporal genetic structure in populations of Pygospio elegans, a poecilogonous polychaete with within-species variation in developmental mode. P. elegans produces either planktonic, benthic, or intermediate larvae, varying both among and within populations, providing a within-species test of the generality of a relationship between temporal genetic variation and larval developmental mode. RESULTS: In contrast to our expectations, our microsatellite analyses of P. elegans revealed temporal genetic stability in the UK population with planktonic larvae, whereas there was variation indicative of drift in temporal samples of the populations from the Baltic Sea, which have predominantly benthic and intermediate larvae. We also detected temporal variation in relatedness within these populations. A large temporal shift in genetic structure was detected in a population from the Netherlands, having multiple developmental modes. This shift could have been caused by local extiction due to extreme environmental conditions and (re)colonization by planktonic larvae from neighboring populations. CONCLUSIONS: In our study of P. elegans, temporal genetic variation appears to be due to not only larval developmental mode, but also the stochastic environment of adults. Large temporal genetic shifts may be more likely in marine intertidal habitats (e.g. North Sea and Wadden Sea) which are more prone to environmental stochasticity than the sub-tidal Baltic habitats. Sub-tidal and/or brackish (less saline) habitats may support smaller P. elegans populations and these may be more susceptible to the effects of random genetic drift. Moreover, higher frequencies of asexual reproduction and the benthic larval developmental mode in these populations leads to higher relatedness and contributes to drift. Our results indicate that a general relationship between larval developmental mode and temporal genetic variation may not exist. BioMed Central 2014-01-22 /pmc/articles/PMC3905951/ /pubmed/24447386 http://dx.doi.org/10.1186/1471-2148-14-12 Text en Copyright © 2014 Kesäniemi et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 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
Kesäniemi, Jenni E
Mustonen, Marina
Boström, Christoffer
Hansen, Benni W
Knott, K Emily
Temporal genetic structure in a poecilogonous polychaete: the interplay of developmental mode and environmental stochasticity
title Temporal genetic structure in a poecilogonous polychaete: the interplay of developmental mode and environmental stochasticity
title_full Temporal genetic structure in a poecilogonous polychaete: the interplay of developmental mode and environmental stochasticity
title_fullStr Temporal genetic structure in a poecilogonous polychaete: the interplay of developmental mode and environmental stochasticity
title_full_unstemmed Temporal genetic structure in a poecilogonous polychaete: the interplay of developmental mode and environmental stochasticity
title_short Temporal genetic structure in a poecilogonous polychaete: the interplay of developmental mode and environmental stochasticity
title_sort temporal genetic structure in a poecilogonous polychaete: the interplay of developmental mode and environmental stochasticity
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3905951/
https://www.ncbi.nlm.nih.gov/pubmed/24447386
http://dx.doi.org/10.1186/1471-2148-14-12
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