Congruence between fine-scale genetic breaks and dispersal potential in an estuarine seaweed across multiple transition zones
Abstract
Abstract Genetic structure in biogeographical transition zones can be shaped by several factors including limited dispersal across barriers, admixture following secondary contact, differential selection, and mating incompatibility. A striking example is found in Northwest France and Northwest Spain, where the estuarine seaweed Fucus ceranoides L. exhibits sharp, regional genetic clustering. This pattern has been related to historical population fragmentation and divergence into distinct glacial refugia, followed by post-glacial expansion and secondary contact. The contemporary persistence of sharp ancient genetic breaks between nearby estuaries has been attributed to prior colonization effects (density barriers) but the effect of oceanographic barriers has not been tested. Here, through a combination of mesoscale sampling (15 consecutive populations) and population genetic data (mtIGS) in NW France, we define regional genetic disjunctions similar to those described in NW Iberia. Most importantly, using high resolution dispersal simulations for Brittany and Iberian populations, we provide evidence for a central role of contemporary hydrodynamics in maintaining genetic breaks across these two major biogeographic transition zones. Our findings further show the importance of a comprehensive understanding of oceanographic regimes in hydrodynamically complex coastal regions to explain the maintenance of sharp genetic breaks along continuously populated coastlines.
- Authors:
-
[2];
[3];
- CCMAR-CIMAR—Associated Laboratory, University of Algarve, Campus de Gambelas, Faro 8005-139, Portugal
- UMI 3614 Evolutionary Biology and Ecology of Algae, CNRS, Sciences Sorbonne Université, UC, UACH, Station Biologique de Roscoff, Roscoff Cedex, France
- Department of Zoology and Entomology, Rhodes University, Grahamstown 6140, South Africa
- Publication Date:
- Sponsoring Org.:
- USDOE Office of Nuclear Energy (NE), Nuclear Fuel Cycle and Supply Chain
- OSTI Identifier:
- 1596180
- Grant/Contract Number:
- SFRH/BPD/111003/2015
- Resource Type:
- Published Article
- Journal Name:
- ICES Journal of Marine Science
- Additional Journal Information:
- Journal Name: ICES Journal of Marine Science Journal Volume: 77 Journal Issue: 1; Journal ID: ISSN 1054-3139
- Publisher:
- Oxford University Press
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Nicastro, Katy R., Assis, Jorge, Serrão, Ester A., Pearson, Gareth A., Neiva, João, Valero, Myriam, Jacinto, Rita, Zardi, Gerardo I., and Kaplan, ed., David. Congruence between fine-scale genetic breaks and dispersal potential in an estuarine seaweed across multiple transition zones. United Kingdom: N. p., 2019.
Web. doi:10.1093/icesjms/fsz179.
Nicastro, Katy R., Assis, Jorge, Serrão, Ester A., Pearson, Gareth A., Neiva, João, Valero, Myriam, Jacinto, Rita, Zardi, Gerardo I., & Kaplan, ed., David. Congruence between fine-scale genetic breaks and dispersal potential in an estuarine seaweed across multiple transition zones. United Kingdom. https://doi.org/10.1093/icesjms/fsz179
Nicastro, Katy R., Assis, Jorge, Serrão, Ester A., Pearson, Gareth A., Neiva, João, Valero, Myriam, Jacinto, Rita, Zardi, Gerardo I., and Kaplan, ed., David. Fri .
"Congruence between fine-scale genetic breaks and dispersal potential in an estuarine seaweed across multiple transition zones". United Kingdom. https://doi.org/10.1093/icesjms/fsz179.
@article{osti_1596180,
title = {Congruence between fine-scale genetic breaks and dispersal potential in an estuarine seaweed across multiple transition zones},
author = {Nicastro, Katy R. and Assis, Jorge and Serrão, Ester A. and Pearson, Gareth A. and Neiva, João and Valero, Myriam and Jacinto, Rita and Zardi, Gerardo I. and Kaplan, ed., David},
abstractNote = {Abstract Genetic structure in biogeographical transition zones can be shaped by several factors including limited dispersal across barriers, admixture following secondary contact, differential selection, and mating incompatibility. A striking example is found in Northwest France and Northwest Spain, where the estuarine seaweed Fucus ceranoides L. exhibits sharp, regional genetic clustering. This pattern has been related to historical population fragmentation and divergence into distinct glacial refugia, followed by post-glacial expansion and secondary contact. The contemporary persistence of sharp ancient genetic breaks between nearby estuaries has been attributed to prior colonization effects (density barriers) but the effect of oceanographic barriers has not been tested. Here, through a combination of mesoscale sampling (15 consecutive populations) and population genetic data (mtIGS) in NW France, we define regional genetic disjunctions similar to those described in NW Iberia. Most importantly, using high resolution dispersal simulations for Brittany and Iberian populations, we provide evidence for a central role of contemporary hydrodynamics in maintaining genetic breaks across these two major biogeographic transition zones. Our findings further show the importance of a comprehensive understanding of oceanographic regimes in hydrodynamically complex coastal regions to explain the maintenance of sharp genetic breaks along continuously populated coastlines.},
doi = {10.1093/icesjms/fsz179},
journal = {ICES Journal of Marine Science},
number = 1,
volume = 77,
place = {United Kingdom},
year = {2019},
month = {11}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1093/icesjms/fsz179
https://doi.org/10.1093/icesjms/fsz179
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 1 work
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Dispersal of Hormosira Banksii (Phaeophyceae) via Detached Fragments: Reproductive Viability and Longevity 1
journal, October 2008
- McKenzie, Prudence F.; Bellgrove, Alecia
- Journal of Phycology, Vol. 44, Issue 5
A general view of the hydrographic and dynamical patterns of the Rías Baixas adjacent sea area
journal, February 2005
- Varela, Ramiro A.; Rosón, Gabriel; Herrera, Juan L.
- Journal of Marine Systems, Vol. 54, Issue 1-4
The effects of past, present and future climate change on range-wide genetic diversity in northern North Atlantic marine species
journal, April 2013
- Provan, Jim
- Frontiers of Biogeography, Vol. 5, Issue 1
The Lessonia Nigrescens Species Complex (Laminariales, Phaeophyceae) Shows Strict Parapatry and Complete Reproductive Isolation in a Secondary Contact Zone1: Reproductive Isolation Between kelp Species
journal, July 2011
- Tellier, Florence; Tapia, Javier; Faugeron, Sylvain
- Journal of Phycology, Vol. 47, Issue 4
Local Coastal Configuration Rather Than Latitudinal Gradient Shape Clonal Diversity and Genetic Structure of Phymatolithon calcareum Maerl Beds in North European Atlantic
journal, March 2019
- Pardo, Cristina; Guillemin, Marie-Laure; Peña, Viviana
- Frontiers in Marine Science, Vol. 6
Hydrographical variability on the French continental shelf in the Bay of Biscay, during the 1990s
journal, June 2004
- Puillat, I.; Lazure, P.; Jégou, A. M.
- Continental Shelf Research, Vol. 24, Issue 10
The change in genetic diversity down the core-edge gradient in the eastern spadefoot toad (Pelobates syriacus): GENETIC DIVERSITY IN PERIPHERAL POPULATIONS
journal, June 2010
- Munwes, Inbar; Geffen, Eli; Roll, Uri
- Molecular Ecology, Vol. 19, Issue 13
Oceanographic Conditions Limit the Spread of a Marine Invader along Southern African Shores
journal, June 2015
- Assis, Jorge; Zupan, Mirta; Nicastro, Katy R.
- PLOS ONE, Vol. 10, Issue 6
The HYCOM (HYbrid Coordinate Ocean Model) data assimilative system
journal, March 2007
- Chassignet, Eric P.; Hurlburt, Harley E.; Smedstad, Ole Martin
- Journal of Marine Systems, Vol. 65, Issue 1-4
Twenty years of observed and predicted changes in subtidal red seaweed assemblages along a biogeographical transition zone: inferring potential causes from environmental data
journal, August 2014
- Gallon, Régis K.; Robuchon, Marine; Leroy, Boris
- Journal of Biogeography, Vol. 41, Issue 12
Reproductive strategies and population genetic structure of Fucus spp . across a northeast Atlantic biogeographic transition
journal, January 2017
- Almeida, Susana C.; Nicastro, Katy R.; Zardi, Gerardo I.
- Aquatic Living Resources, Vol. 30
Shift happens: trailing edge contraction associated with recent warming trends threatens a distinct genetic lineage in the marine macroalga Fucus vesiculosus
journal, January 2013
- Nicastro, Katy R.; Zardi, Gerardo I.; Teixeira, Sara
- BMC Biology, Vol. 11, Issue 1
Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species: SEASCAPE GENETICS
journal, August 2010
- Selkoe, Kimberly A.; Watson, James R.; White, Crow
- Molecular Ecology, Vol. 19, Issue 17
Analysis of Hybrid Zones
journal, November 1985
- Barton, N. H.; Hewitt, G. M.
- Annual Review of Ecology and Systematics, Vol. 16, Issue 1
Poppr : an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction
journal, January 2014
- Kamvar, Zhian N.; Tabima, Javier F.; Grünwald, Niklaus J.
- PeerJ, Vol. 2
The role of historical and contemporary processes on phylogeographic structure and genetic diversity in the Northern Cardinal, Cardinalis cardinalis
journal, May 2011
- Smith, Brian Tilston; Escalante, Patricia; Hernández Baños, Blanca E.
- BMC Evolutionary Biology, Vol. 11, Issue 1
A Comparative Study of Asymmetric Migration Events Across a Marine Biogeographic Boundary
journal, February 2001
- Wares, John P.; Gaines, StevenD.; Cunningham, Clifford W.
- Evolution, Vol. 55, Issue 2
Unexpected genetic structure of mussel populations in South Africa: indigenous Perna perna and invasive Mytilus galloprovincialis
journal, May 2007
- Zardi, Gi; McQuaid, Cd; Teske, Pr
- Marine Ecology Progress Series, Vol. 337
The coupling hypothesis: why genome scans may fail to map local adaptation genes: THE COUPLING HYPOTHESIS
journal, April 2011
- Bierne, Nicolas; Welch, John; Loire, Etienne
- Molecular Ecology, Vol. 20, Issue 10
Distribution, reproduction, and ecology of Fucus ceranoides L. (Phaeophyceae) in Norway
journal, October 1984
- Lein, Tor Eiliv
- Sarsia, Vol. 69, Issue 2
A biologist’s guide to assessing ocean currents: a review
journal, June 2012
- Fossette, S.; Putman, Nf; Lohmann, Kj
- Marine Ecology Progress Series, Vol. 457
The Geography of Marine Larval Dispersal: Coupling Genetics with Fine-Scale Physical Oceanography
journal, November 2003
- Gilg, Matthew R.; Hilbish, Thomas J.
- Ecology, Vol. 84, Issue 11
Drifting fronds and drifting alleles: range dynamics, local dispersal and habitat isolation shape the population structure of the estuarine seaweed Fucus ceranoides: Population structure of Fucus ceranoides
journal, January 2012
- Neiva, João; Pearson, Gareth A.; Valero, Myriam
- Journal of Biogeography, Vol. 39, Issue 6
Tracking the long-distance dispersal of marine organisms: sensitivity to ocean model resolution
journal, April 2013
- Putman, Nathan F.; He, Ruoying
- Journal of The Royal Society Interface, Vol. 10, Issue 81
Fine-scale genetic breaks driven by historical range dynamics and ongoing density-barrier effects in the estuarine seaweed Fucus ceranoides L.
journal, January 2012
- Neiva, João; Pearson, Gareth A.; Valero, Myriam
- BMC Evolutionary Biology, Vol. 12, Issue 1
Oceanographic conditions in North and Northwest Iberia and their influence on the Prestige oil spill
journal, January 2006
- Ruiz-Villarreal, M.; González-Pola, C.; Diaz del Rio, G.
- Marine Pollution Bulletin, Vol. 53, Issue 5-7
Phylogeography of an estuarine mysid, Neomysis integer (Crustacea, Mysida), along the north-east Atlantic coasts
journal, January 2009
- Remerie, Thomas; Vierstraete, Andy; Weekers, Peter H. H.
- Journal of Biogeography, Vol. 36, Issue 1
Temporal windows of reproductive opportunity reinforce species barriers in a marine broadcast spawning assemblage
journal, July 2016
- Monteiro, Carla A.; Paulino, Cristina; Jacinto, Rita
- Scientific Reports, Vol. 6, Issue 1
Meroplankton distribution and its relationship to coastal mesoscale hydrological structure in the northern Bay of Biscay (NE Atlantic)
journal, April 2011
- Ayata, Sakina-Dorothée; Stolba, Robin; Comtet, Thierry
- Journal of Plankton Research, Vol. 33, Issue 8
Natural Hybridization and Hybrid Zones
journal, September 1973
- Woodruff, D. S.
- Systematic Biology, Vol. 22, Issue 3
Limits to gene flow in marine animals with planktonic larvae: models of Littorina species around Point Conception, California: GENE FLOW IN LITTORINA
journal, June 2004
- Hohenlohe, Paul A.
- Biological Journal of the Linnean Society, Vol. 82, Issue 2
Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula: GENETIC CLINES: THE BARNACLE BALANUS GLANDULA
journal, June 2004
- Sotka, Erik E.; Wares, John P.; Barth, John A.
- Molecular Ecology, Vol. 13, Issue 8
Past climate changes and strong oceanographic barriers structured low‐latitude genetic relics for the golden kelp Laminaria ochroleuca
journal, August 2018
- Assis, Jorge; Serrão, Ester Álvares; Coelho, Nelson Castilho
- Journal of Biogeography, Vol. 45, Issue 10
Surfing the wave on a borrowed board: range expansion and spread of introgressed organellar genomes in the seaweed Fucus ceranoides L.
journal, October 2010
- Neiva, JoÃO; Pearson, Gareth A.; Valero, Myriam
- Molecular Ecology, Vol. 19, Issue 21
A Lagrangian tool for modelling ichthyoplankton dynamics
journal, September 2008
- Lett, C.; Verley, P.; Mullon, C.
- Environmental Modelling & Software, Vol. 23, Issue 9
Holocene evolution on Galician coast (NW Spain): an example of paraglacial dynamics
journal, July 2002
- Blanco Chao, Ramón; Costa Casais, Manuela; Martı́nez Cortizas, Antonio
- Quaternary International, Vol. 93-94
Dynamics of Pleistocene Population Extinctions in Beringian Brown Bears
journal, March 2002
- Barnes, I.
- Science, Vol. 295, Issue 5563
Contrasting genetic effects of red mangrove ( Rhizophora mangle L.) range expansion along West and East Florida
journal, June 2016
- Kennedy, John Paul; Garavelli, Lysel; Truelove, Nathan K.
- Journal of Biogeography, Vol. 44, Issue 2
OpenStreetMap: User-Generated Street Maps
journal, October 2008
- Haklay, M.; Weber, P.
- IEEE Pervasive Computing, Vol. 7, Issue 4
Seascape drivers of Macrocystis pyrifera population genetic structure in the northeast Pacific
journal, September 2015
- Johansson, Mattias L.; Alberto, Filipe; Reed, Daniel C.
- Molecular Ecology, Vol. 24, Issue 19
A review of marine phylogeography in southern Africa
journal, May 2011
- Teske, Peter R.; Von der Heyden, Sophie; McQuaid, Christopher D.
- South African Journal of Science, Vol. 107, Issue 5/6
Marine Ecoregions of the World: A Bioregionalization of Coastal and Shelf Areas
journal, July 2007
- Spalding, Mark D.; Fox, Helen E.; Allen, Gerald R.
- BioScience, Vol. 57, Issue 7
Biogeographical transition zones: a search for conceptual synthesis: Biogeographical Transition Zones
journal, July 2014
- Ferro, Ignacio; Morrone, Juan J.
- Biological Journal of the Linnean Society, Vol. 113, Issue 1
Phylogeographic studies of schizothoracine fishes on the central Qinghai-Tibet Plateau reveal the highest known glacial microrefugia
journal, September 2017
- Liang, Yangyang; He, Dekui; Jia, Yintao
- Scientific Reports, Vol. 7, Issue 1
Population genetic consequences of larval dispersal mode and hydrography: a case study with bryozoans
journal, May 2001
- Goldson, A. J.; Hughes, R. N.; Gliddon, C. J.
- Marine Biology, Vol. 138, Issue 5
Implications of life history for genetic structure and migration rates of southern African coastal invertebrates: planktonic, abbreviated and direct development
journal, May 2007
- Teske, P. R.; Papadopoulos, I.; Zardi, G. I.
- Marine Biology, Vol. 152, Issue 3
Some genetic consequences of ice ages, and their role in divergence and speciation
journal, July 1996
- Hewitt, G.
- Biological Journal of the Linnean Society, Vol. 58, Issue 3
Glacial refugia and recolonization pathways in the brown seaweed Fucus serratus
journal, September 2007
- Hoarau, G.; Coyer, J. A.; Veldsink, J. H.
- Molecular Ecology, Vol. 16, Issue 17
Sharp genetic break between Atlantic and English Channel populations of the polychaete Pectinaria koreni, along the North coast of France
journal, August 2004
- Jolly, M. T.; Jollivet, D.; Gentil, F.
- Heredity, Vol. 94, Issue 1
Coastal topography drives genetic structure in marine mussels
journal, September 2008
- Nicastro, Kr; Zardi, Gi; McQuaid, Cd
- Marine Ecology Progress Series, Vol. 368
Glacial vicariance drives phylogeographic diversification in the amphi-boreal kelp Saccharina latissima
journal, January 2018
- Neiva, João; Paulino, Cristina; Nielsen, Mette M.
- Scientific Reports, Vol. 8, Issue 1
DnaSP v5: a software for comprehensive analysis of DNA polymorphism data
journal, April 2009
- Librado, P.; Rozas, J.
- Bioinformatics, Vol. 25, Issue 11
Management and conservation of the kelp species Laminaria digitata : using genetic tools to explore the potential exporting role of the MPA “ Parc naturel marin d’Iroise ”
journal, October 2012
- Couceiro, Lucía; Robuchon, Marine; Destombe, Christophe
- Aquatic Living Resources, Vol. 26, Issue 2
The genetic legacy of the Quaternary ice ages
journal, June 2000
- Hewitt, Godfrey
- Nature, Vol. 405, Issue 6789
A winter upwelling event in the Northern Galician Rias: Frequency and oceanographic implications
journal, May 2009
- Alvarez, I.; Ospina-Alvarez, N.; Pazos, Y.
- Estuarine, Coastal and Shelf Science, Vol. 82, Issue 4
Dispersal similarly shapes both population genetics and community patterns in the marine realm
journal, June 2016
- Chust, Guillem; Villarino, Ernesto; Chenuil, Anne
- Scientific Reports, Vol. 6, Issue 1
Genetic consequences of climatic oscillations in the Quaternary
journal, February 2004
- Hewitt, G. M.
- Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 359, Issue 1442
The influence of coastal topography, circulation patterns, and rafting in structuring populations of an intertidal alga
journal, March 2008
- Muhlin, J. F.; Engel, C. R.; Stessel, R.
- Molecular Ecology, Vol. 17, Issue 5
High Interannual Variability in Connectivity and Genetic Pool of a Temperate Clingfish Matches Oceanographic Transport Predictions
journal, December 2016
- Klein, Maria; Teixeira, Sara; Assis, Jorge
- PLOS ONE, Vol. 11, Issue 12
Major shifts at the range edge of marine forests: the combined effects of climate changes and limited dispersal
journal, March 2017
- Assis, J.; Berecibar, E.; Claro, B.
- Scientific Reports, Vol. 7, Issue 1
Broad scale agreement between intertidal habitats and adaptive traits on a basis of contrasting population genetic structure
journal, October 2013
- Zardi, G. I.; Nicastro, K. R.; Ferreira Costa, J.
- Estuarine, Coastal and Shelf Science, Vol. 131
Ecological strategies predict associations between aquatic and genetic connectivity for dryland amphibians
journal, May 2015
- Mims, Meryl C.; Phillipsen, Ivan C.; Lytle, David A.
- Ecology, Vol. 96, Issue 5
Phylogeographic analysis of the red seaweed Palmaria palmata reveals a Pleistocene marine glacial refugium in the English Channel: PHYLOGEOGRAPHY OF PALMARIA PALMATA
journal, February 2005
- Provan, Jim; Wattier, Remi A.; Maggs, Christine A.
- Molecular Ecology, Vol. 14, Issue 3
The combination of selection and dispersal helps explain genetic structure in intertidal mussels
journal, September 2010
- Zardi, G. I.; Nicastro, K. R.; McQuaid, C. D.
- Oecologia, Vol. 165, Issue 4
Modularity and community structure in networks
journal, May 2006
- Newman, M. E. J.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 23
The response of NW Iberian vegetation to North Atlantic climate oscillations during the last 65kyr
journal, August 2005
- Roucoux, K. H.; de Abreu, L.; Shackleton, N. J.
- Quaternary Science Reviews, Vol. 24, Issue 14-15
Isolation by Distance in Equilibrium and Non-Equilibrium Populations
journal, February 1993
- Slatkin, Montgomery
- Evolution, Vol. 47, Issue 1
TCS: a computer program to estimate gene genealogies
journal, October 2000
- Clement, M.; Posada, D.; Crandall, K. A.
- Molecular Ecology, Vol. 9, Issue 10
Mitochondrial DNA phylogeography and mating compatibility reveal marked genetic structuring and speciation in the NE Atlantic bryozoan Celleporella hyalina
journal, May 2007
- GÓMez, Africa; Hughes, Roger N.; Wright, Peter J.
- Molecular Ecology, Vol. 16, Issue 10
The phylogeographic architecture of the fucoid seaweed Ascophyllum nodosum : an intertidal ‘marine tree’ and survivor of more than one glacial-interglacial cycle
journal, May 2010
- Olsen, Jeanine L.; Zechman, Frederick W.; Hoarau, Galice
- Journal of Biogeography, Vol. 37, Issue 5