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North Atlantic phylogeography and large-scale population differentiation of the seagrass Zostera marina L.

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  • JEANINE L. OLSEN,

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    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
      J.L. Olsen. Fax: +31 50 363 2261; E-mail: j.l.olsen@biol.rug.nl
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  • WYTZE T. STAM,

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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  • JAMES A. COYER,

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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  • THORSTEN B. H. REUSCH,

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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  • MARTIN BILLINGHAM,

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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  • CHRISTOFFER BOSTRÖM,

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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  • ELIZABETH CALVERT,

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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  • HARTVIG CHRISTIE,

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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  • STEPHEN GRANGER,

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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  • RICHARD LA LUMIÈRE,

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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  • NATALIYA MILCHAKOVA,

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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  • MARIE-PIERRE OUDOT-LE SECQ,

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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  • GABRIELE PROCACCINI,

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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  • BAHRAM SANJABI,

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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  • ESTER SERRÃO,

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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  • JAN VELDSINK,

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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  • STEPHEN WIDDICOMBE,

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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  • SANDY WYLLIE-ECHEVERRIA

    1. Authors after Thorsten Reusch are listed in alphabetical order
      *Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, †Max Planck Institute for Limnology, Plön, Germany, ‡Center for Marine Sciences, University of Algarve, Faro, Portugal, §Department of Environmental and Marine Biology, Åbo Akademi University, Åbo, Finland, ¶University of Alaska-Fairbanks, Juneau, AK, USA, ||Norwegian Institute for Nature Research, Oslo, Norway, **Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, USA, ††Groupe conseil GENIVAR Inc., Québec, Canada, ‡‡Institute of Biology of the Southern Seas, Sevastopol, Ukraine, §§Laboratorio di Ecologia del Benthos, SZN, Ischia, Italy, ¶¶Plymouth Marine Laboratory, Plymouth, UK, ||||School of Marine Affairs, University of Washington, Seattle, WA, USA
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J.L. Olsen. Fax: +31 50 363 2261; E-mail: j.l.olsen@biol.rug.nl

Abstract

As the most widespread seagrass in temperate waters of the Northern Hemisphere, Zostera marina provides a unique opportunity to investigate the extent to which the historical legacy of the last glacial maximum (LGM18 000–10 000 years bp) is detectable in modern population genetic structure. We used sequences from the nuclear rDNA–internal transcribed spacer (ITS) and chloroplast matK-intron, and nine microsatellite loci to survey 49 populations (> 2000 individuals) from throughout the species’ range. Minimal sequence variation between Pacific and Atlantic populations combined with biogeographical groupings derived from the microsatellite data, suggest that the trans-Arctic connection is currently open. The east Pacific and west Atlantic are more connected than either is to the east Atlantic. Allelic richness was almost two-fold higher in the Pacific. Populations from putative Atlantic refugia now represent the southern edges of the distribution and are not genetically diverse. Unexpectedly, the highest allelic diversity was observed in the North Sea–Wadden Sea–southwest Baltic region. Except for the Mediterranean and Black Seas, significant isolation-by-distance was found from ~150 to 5000 km. A transition from weak to strong isolation-by-distance occurred at ~150 km among northern European populations suggesting this scale as the natural limit for dispersal within the metapopulation. Links between historical and contemporary processes are discussed in terms of the projected effects of climate change on coastal marine plants. The identification of a high genetic diversity hotspot in Northern Europe provides a basis for restoration decisions.

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