Exploring the impact of multidecadal environmental changes on the population genetic structure of a marine primary producer

Abstract Many marine protists form resting stages that can remain viable in coastal sediments for several decades. Their long‐term survival offers the possibility to explore the impact of changes in environmental conditions on population dynamics over multidecadal time scales. Resting stages of the phototrophic dinoflagellate Pentapharsodinium dalei were isolated and germinated from five layers in dated sediment cores from Koljö fjord, Sweden, spanning ca. 1910–2006. This fjord has, during the last century, experienced environmental fluctuations linked to hydrographic variability mainly driven by the North Atlantic Oscillation. Population genetic analyses based on six microsatellite markers revealed high genetic diversity and suggested that samples belonged to two clusters of subpopulations that have persisted for nearly a century. We observed subpopulation shifts coinciding with changes in hydrographic conditions. The large degree of genetic diversity and the potential for both fluctuation and recovery over longer time scales documented here, may help to explain the long‐term success of aquatic protists that form resting stages.

• Publication year

  2017

• Venue

  Ecology and Evolution

• Publication date

  2017-03-30

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1002/ece3.2906PMID 28480012PMCID 5415532
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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• Bacterial and fungal symbionts of parasitic Dendroctonus bark beetles.

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• Competitive advantage and higher fitness in native populations of genetically structured planktonic diatoms.

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• Local adaptation and oceanographic connectivity patterns explain genetic differentiation of a marine diatom across the North Sea–Baltic Sea salinity gradient

  2015cited by this paper
• R: A language and environment for statistical computing.

  2014influential reference
• The temporal distribution of directional gradients under selection for an optimum

  2014cited by this paper
• Microsatellite markers for the palaeo-temperature indicator Pentapharsodinium dalei (Dinophyceae)

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• Towards an Ecological Understanding of Dinoflagellate Cyst Functions

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  2014influential reference
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  2013influential reference
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  2013cited by this paper
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  2012influential reference
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  2012influential reference
• Climate variability in West Greenland during the past 1500 years: evidence from a high‐resolution marine palynological record from Disko Bay

  2012cited by this paper
• The interplay between habitat availability and population differentiation

  2012cited by this paper
• Genetic diversity within and genetic differentiation between blooms of a microalgal species

  2012cited by this paper
• Diversity and Dynamics of a Widespread Bloom of the Toxic Dinoflagellate Alexandrium fundyense

  2011influential reference
• Preservation potential of ancient plankton DNA in Pleistocene marine sediments

  2011cited by this paper
• Buried alive – germination of up to a century-old marine protist resting stages

  2011influential reference
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  2011cited by this paper
• Contrasting sea-surface responses between the western Mediterranean Sea and eastern subtropical lati

  2011cited by this paper
• Marine primary production in relation to climate variability and change.

  2011cited by this paper
• Hundred years of genetic structure in a sediment revived diatom population

  2011influential reference
• Fluctuating selection: the perpetual renewal of adaptation in variable environments

  2010cited by this paper
• Dinoflagellate cysts as proxies for palaeoceanographic conditions in Arctic fjords

  2010cited by this paper
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  2010cited by this paper
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  2010influential reference
• Linking the planktonic and benthic habitat: genetic structure of the marine diatom Skeletonema marinoi

  2010influential reference
• Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows

  2010influential reference
• Limits to gene flow in a cosmopolitan marine planktonic diatom

  2010influential reference
• Genetic structuring and transfer of marine dinoflagellate Cochlodinium polykrikoides in Japanese and Korean coastal waters revealed by microsatellites

  2009cited by this paper
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  2009influential reference
• Inferring weak population structure with the assistance of sample group information

  2009cited by this paper
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  2009cited by this paper
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  2007cited by this paper
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  2007cited by this paper
• Interactive Multivariate Data Analysis in R with the ade4 and ade4TkGUI Packages

  2007influential reference
• At-sea distribution and scale-dependent foraging behaviour of petrels and albatrosses: a comparative study.

  2007cited by this paper
• Global molecular phylogeography reveals persistent Arctic circumpolar isolation in a marine planktonic protist

  2007cited by this paper
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  2006cited by this paper
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  2006influential reference
• HIGH LEVELS OF GENETIC DIVERSITY AND LOW LEVELS OF GENETIC DIFFERENTIATION IN NORTH SEA PSEUDO‐NITZSCHIA PUNGENS (BACILLARIOPHYCEAE) POPULATIONS 1

  2005cited by this paper
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  2005cited by this paper
• hp-rare 1.0: a computer program for performing rarefaction on measures of allelic richness

  2005cited by this paper
• Detecting the number of clusters of individuals using the software structure: a simulation study

  2005cited by this paper
• A major change in the phytoplankton of a Swedish sill fjord—A consequence of engineering work?

  2005influential reference
• FAST‐TRACK: Integrating QTL mapping and genome scans towards the characterization of candidate loci under parallel selection in the lake whitefish (Coregonus clupeaformis)

  2004cited by this paper
• The Scandinavian Culture Centre for Algae and Protozoa

  2004cited by this paper
• The seasonal occurrence of dinoflagellate cysts in surface sediments from Koljö Fjord, west coast of Sweden – a note

  2004influential reference
• Counting Alleles with Rarefaction: Private Alleles and Hierarchical Sampling Designs

  2004cited by this paper
• Climate variations, an overlooked factor influencing the recent marine environment. An example from Gullmar Fjord, Sweden, illustrated by benthic foraminifera and hydrographic data

  2004cited by this paper
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  2004influential reference
• GENETIC DIFFERENTIATION AMONG POPULATIONS OF THE PLANKTONIC MARINE DIATOM DITYLUM BRIGHTWELLII (BACILLARIOPHYCEAE) 1

  2004cited by this paper
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  2004cited by this paper
• Climate over past millennia

  2004cited by this paper
• Temporal change in genetic structure and effective population size in steelhead trout (Oncorhynchus mykiss)

  2002cited by this paper
• Genetic Data Analysis II. Methods for Discrete Population Genentic Data

  2002influential reference
• Phylogeny of the Bacillariaceae with emphasis on the genus Pseudo-nitzschia (Bacillariophyceae) based on partial LSU rDNA

  2002cited by this paper
• Viability of phytoplankton resting stages in the sediments of a coastal Swedish fjord

  2002cited by this paper
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  2002cited by this paper
• Climate, hydrographic variations and marine benthic hypoxia in Koljö Fjord, Sweden

  2001influential reference
• The sedimentary record of dinoflagellate cysts: looking back into the future of phytoplankton blooms*

  2001cited by this paper
• The North Atlantic Oscillation: Past, present, and future

  2001cited by this paper
• Inference of population structure using multilocus genotype data.

  2000cited by this paper
• DNA fingerprinting reveals extensive genetic diversity in a field population of the centric diatom Ditylum brightwellii

  2000influential reference
• Distribution of recent dinoflagellate cysts in surface sediments from the North Atlantic Ocean and adjacent seas in relation to sea-surface parameters

  1999cited by this paper
• The use of sodium polytungstate for the separation and concentration of living dinoflagellate cysts from marine sediments

  1997influential reference
• Studies on the marine planktonic diatom Pseudo-nitzschia. 1. Isozyme variation among isolates of P. pseudodelicatissima during a bloom in Danish coastal waters

  1997cited by this paper
• Genetic characterisation of Emiliania huxleyi (Haptophyta)

  1996cited by this paper
• Zooplankton egg banks as biotic reservoirs in changing environments

  1996cited by this paper
• Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data.

  1992influential reference
• INTRASPECIFIC VARIATION IN THE DINOFLAGELLATE PERIDINIUM VOLZIP 1

  1987cited by this paper
• ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE

  1984influential reference
• A Simple Sequentially Rejective Multiple Test Procedure

  1979cited by this paper
• New observations on Peridinium faeroense Paulsen (1905), and classification of small orthoperidinioid dinoflagellates

  1977cited by this paper

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• Phytoplankton diversity explained by connectivity across a mesoscale frontal system in the open ocean

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• Cross‐contamination risks in sediment‐based resurrection studies of phytoplankton

  2022cites this paper
• Evolution of Phytoplankton as Estimated from Genetic Diversity

  2022cites this paper
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  2020cites this paper
• Revival of ancient marine dinoflagellates using molecular biostimulatio.

  2020cites this paper
• Dead or alive: sediment DNA archives as tools for tracking aquatic evolution and adaptation

  2020cites this paper
• Cyst-forming dinoflagellates in a warming climate.

  2020cites this paper
• Dinoflagellate cysts from the ‘Anthropocene’ of Gullmar Fjord, west coast of Sweden and their potential for monitoring climate change

  2019cites this paper
• A century of genetic variation inferred from a persistent soil‐stored seed bank

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  2018cites this paper
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