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A Pleistocene legacy structures variation in modern seagrass ecosystems

J. Emmett Duffy Orcid Logo, John J. Stachowicz Orcid Logo, Pamela L. Reynolds, Kevin A. Hovel, Marlene Jahnke, Erik E. Sotka Orcid Logo, Christoffer Boström, Katharyn E. Boyer Orcid Logo, Mathieu Cusson Orcid Logo, Johan Eklöf, Aschwin H. Engelen Orcid Logo, Britas Klemens Eriksson, F. Joel Fodrie Orcid Logo, John Griffin Orcid Logo, Clara M. Hereu Orcid Logo, Masakazu Hori, A. Randall Hughes Orcid Logo, Mikhail V. Ivanov Orcid Logo, Pablo Jorgensen Orcid Logo, Claudia Kruschel, Kun-Seop Lee Orcid Logo, Jonathan S. Lefcheck Orcid Logo, Per-Olav Moksnes, Masahiro Nakaoka Orcid Logo, Mary I. O’Connor Orcid Logo, Nessa E. O’Connor Orcid Logo, Robert J. Orth Orcid Logo, Bradley J. Peterson, Henning Reiss, Katrin Reiss, J. Paul Richardson, Francesca Rossi Orcid Logo, Jennifer L. Ruesink, Stewart T. Schultz, Jonas Thormar Orcid Logo, Fiona Tomas, Richard Unsworth Orcid Logo, Erin Voigt, Matthew A. Whalen, Shelby L. Ziegler Orcid Logo, Jeanine L. Olsen

Proceedings of the National Academy of Sciences, Volume: 119, Issue: 32

Swansea University Authors: John Griffin Orcid Logo, Richard Unsworth Orcid Logo

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DOI (Published version): 10.1073/pnas.2121425119

Abstract

Distribution of Earth’s biomes is structured by the match between climate and plant traits, which in turn shape associated communities and ecosystem processes and services. However, that climate–trait match can be disrupted by historical events, with lasting ecosystem impacts. As Earth’s environment...

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Published in: Proceedings of the National Academy of Sciences
ISSN: 0027-8424 1091-6490
Published: Proceedings of the National Academy of Sciences 2022
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However, that climate&#x2013;trait match can be disrupted by historical events, with lasting ecosystem impacts. As Earth&#x2019;s environment changes faster than at any time in human history, critical questions are whether and how organismal traits and ecosystems can adjust to altered conditions. We quantified the relative importance of current environmental forcing versus evolutionary history in shaping the growth form (stature and biomass) and associated community of eelgrass (Zostera marina), a widespread foundation plant of marine ecosystems along Northern Hemisphere coastlines, which experienced major shifts in distribution and genetic composition during the Pleistocene. We found that eelgrass stature and biomass retain a legacy of the Pleistocene colonization of the Atlantic from the ancestral Pacific range and of more recent within-basin bottlenecks and genetic differentiation. This evolutionary legacy in turn influences the biomass of associated algae and invertebrates that fuel coastal food webs, with effects comparable to or stronger than effects of current environmental forcing. Such historical lags in phenotypic acclimatization may constrain ecosystem adjustments to rapid anthropogenic climate change, thus altering predictions about the future functioning of ecosystems.</abstract><type>Journal Article</type><journal>Proceedings of the National Academy of Sciences</journal><volume>119</volume><journalNumber>32</journalNumber><paginationStart/><paginationEnd/><publisher>Proceedings of the National Academy of Sciences</publisher><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint>0027-8424</issnPrint><issnElectronic>1091-6490</issnElectronic><keywords/><publishedDay>1</publishedDay><publishedMonth>8</publishedMonth><publishedYear>2022</publishedYear><publishedDate>2022-08-01</publishedDate><doi>10.1073/pnas.2121425119</doi><url/><notes>Data Availability:All data used in the analyses, and associated R code, are available at https://doi.org/10.5281/zenodo.6808753(64), with the exception ofthe genetic data, available at https://doi.org/10.5281/zenodo.3660013(65).</notes><college>COLLEGE NANME</college><department>Biosciences</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>SBI</DepartmentCode><institution>Swansea University</institution><apcterm/><funders>This work was supported by the US NSF (OCE-1031061, OCE-1336206, OCE0-1336741, OCE-1336905) and the Smithsonian Institution. J.L.O. thanks Jan Veldsink for DNA extractions and microsatellite gen-otyping. F.T. was supported by Jose Castillejo Award CAS14/00177. A.H.E. was supported by the FCT (Foundation for Science and Technology) through ProjectUIDB/04326/2020 and Contract CEECINST/00114/2018.</funders><projectreference/><lastEdited>2022-08-24T10:05:05.6630288</lastEdited><Created>2022-08-11T09:38:48.3471297</Created><path><level id="1">Faculty of Science and Engineering</level><level id="2">School of Biosciences, Geography and Physics - Biosciences</level></path><authors><author><firstname>J. Emmett</firstname><surname>Duffy</surname><orcid>0000-0001-8595-6391</orcid><order>1</order></author><author><firstname>John J.</firstname><surname>Stachowicz</surname><orcid>0000-0003-2735-0564</orcid><order>2</order></author><author><firstname>Pamela L.</firstname><surname>Reynolds</surname><order>3</order></author><author><firstname>Kevin A.</firstname><surname>Hovel</surname><order>4</order></author><author><firstname>Marlene</firstname><surname>Jahnke</surname><order>5</order></author><author><firstname>Erik E.</firstname><surname>Sotka</surname><orcid>0000-0001-5167-8549</orcid><order>6</order></author><author><firstname>Christoffer</firstname><surname>Bostr&#xF6;m</surname><order>7</order></author><author><firstname>Katharyn E.</firstname><surname>Boyer</surname><orcid>0000-0003-2680-2493</orcid><order>8</order></author><author><firstname>Mathieu</firstname><surname>Cusson</surname><orcid>0000-0002-2111-4803</orcid><order>9</order></author><author><firstname>Johan</firstname><surname>Ekl&#xF6;f</surname><order>10</order></author><author><firstname>Aschwin H.</firstname><surname>Engelen</surname><orcid>0000-0002-9579-9606</orcid><order>11</order></author><author><firstname>Britas Klemens</firstname><surname>Eriksson</surname><order>12</order></author><author><firstname>F. 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Randall</firstname><surname>Hughes</surname><orcid>0000-0001-5072-7310</orcid><order>17</order></author><author><firstname>Mikhail V.</firstname><surname>Ivanov</surname><orcid>0000-0002-8277-7387</orcid><order>18</order></author><author><firstname>Pablo</firstname><surname>Jorgensen</surname><orcid>0000-0002-6018-7124</orcid><order>19</order></author><author><firstname>Claudia</firstname><surname>Kruschel</surname><order>20</order></author><author><firstname>Kun-Seop</firstname><surname>Lee</surname><orcid>0000-0003-0431-1829</orcid><order>21</order></author><author><firstname>Jonathan S.</firstname><surname>Lefcheck</surname><orcid>0000-0002-8787-1786</orcid><order>22</order></author><author><firstname>Per-Olav</firstname><surname>Moksnes</surname><order>23</order></author><author><firstname>Masahiro</firstname><surname>Nakaoka</surname><orcid>0000-0002-5722-3585</orcid><order>24</order></author><author><firstname>Mary I.</firstname><surname>O&#x2019;Connor</surname><orcid>0000-0001-9583-1592</orcid><order>25</order></author><author><firstname>Nessa E.</firstname><surname>O&#x2019;Connor</surname><orcid>0000-0002-3133-0913</orcid><order>26</order></author><author><firstname>Robert J.</firstname><surname>Orth</surname><orcid>0000-0003-2491-7430</orcid><order>27</order></author><author><firstname>Bradley J.</firstname><surname>Peterson</surname><order>28</order></author><author><firstname>Henning</firstname><surname>Reiss</surname><order>29</order></author><author><firstname>Katrin</firstname><surname>Reiss</surname><order>30</order></author><author><firstname>J. 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spelling 2022-08-24T10:05:05.6630288 v2 60794 2022-08-11 A Pleistocene legacy structures variation in modern seagrass ecosystems 9814fbffa76dd9c9a207166354cd0b2f 0000-0003-3295-6480 John Griffin John Griffin true false b0f33acd13a3ab541cf2aaea27f4fc2f 0000-0003-0036-9724 Richard Unsworth Richard Unsworth true false 2022-08-11 SBI Distribution of Earth’s biomes is structured by the match between climate and plant traits, which in turn shape associated communities and ecosystem processes and services. However, that climate–trait match can be disrupted by historical events, with lasting ecosystem impacts. As Earth’s environment changes faster than at any time in human history, critical questions are whether and how organismal traits and ecosystems can adjust to altered conditions. We quantified the relative importance of current environmental forcing versus evolutionary history in shaping the growth form (stature and biomass) and associated community of eelgrass (Zostera marina), a widespread foundation plant of marine ecosystems along Northern Hemisphere coastlines, which experienced major shifts in distribution and genetic composition during the Pleistocene. We found that eelgrass stature and biomass retain a legacy of the Pleistocene colonization of the Atlantic from the ancestral Pacific range and of more recent within-basin bottlenecks and genetic differentiation. This evolutionary legacy in turn influences the biomass of associated algae and invertebrates that fuel coastal food webs, with effects comparable to or stronger than effects of current environmental forcing. Such historical lags in phenotypic acclimatization may constrain ecosystem adjustments to rapid anthropogenic climate change, thus altering predictions about the future functioning of ecosystems. Journal Article Proceedings of the National Academy of Sciences 119 32 Proceedings of the National Academy of Sciences 0027-8424 1091-6490 1 8 2022 2022-08-01 10.1073/pnas.2121425119 Data Availability:All data used in the analyses, and associated R code, are available at https://doi.org/10.5281/zenodo.6808753(64), with the exception ofthe genetic data, available at https://doi.org/10.5281/zenodo.3660013(65). COLLEGE NANME Biosciences COLLEGE CODE SBI Swansea University This work was supported by the US NSF (OCE-1031061, OCE-1336206, OCE0-1336741, OCE-1336905) and the Smithsonian Institution. J.L.O. thanks Jan Veldsink for DNA extractions and microsatellite gen-otyping. F.T. was supported by Jose Castillejo Award CAS14/00177. A.H.E. was supported by the FCT (Foundation for Science and Technology) through ProjectUIDB/04326/2020 and Contract CEECINST/00114/2018. 2022-08-24T10:05:05.6630288 2022-08-11T09:38:48.3471297 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences J. Emmett Duffy 0000-0001-8595-6391 1 John J. Stachowicz 0000-0003-2735-0564 2 Pamela L. Reynolds 3 Kevin A. Hovel 4 Marlene Jahnke 5 Erik E. Sotka 0000-0001-5167-8549 6 Christoffer Boström 7 Katharyn E. Boyer 0000-0003-2680-2493 8 Mathieu Cusson 0000-0002-2111-4803 9 Johan Eklöf 10 Aschwin H. Engelen 0000-0002-9579-9606 11 Britas Klemens Eriksson 12 F. Joel Fodrie 0000-0001-8253-9648 13 John Griffin 0000-0003-3295-6480 14 Clara M. Hereu 0000-0002-2088-9295 15 Masakazu Hori 16 A. Randall Hughes 0000-0001-5072-7310 17 Mikhail V. Ivanov 0000-0002-8277-7387 18 Pablo Jorgensen 0000-0002-6018-7124 19 Claudia Kruschel 20 Kun-Seop Lee 0000-0003-0431-1829 21 Jonathan S. Lefcheck 0000-0002-8787-1786 22 Per-Olav Moksnes 23 Masahiro Nakaoka 0000-0002-5722-3585 24 Mary I. O’Connor 0000-0001-9583-1592 25 Nessa E. O’Connor 0000-0002-3133-0913 26 Robert J. Orth 0000-0003-2491-7430 27 Bradley J. Peterson 28 Henning Reiss 29 Katrin Reiss 30 J. Paul Richardson 31 Francesca Rossi 0000-0003-1928-9193 32 Jennifer L. Ruesink 33 Stewart T. Schultz 34 Jonas Thormar 0000-0002-7925-3822 35 Fiona Tomas 36 Richard Unsworth 0000-0003-0036-9724 37 Erin Voigt 38 Matthew A. Whalen 39 Shelby L. Ziegler 0000-0001-7218-0811 40 Jeanine L. Olsen 41 60794__25002__9b657b669cf14710808c6147ab704b86.pdf 60794_VoR.pdf 2022-08-24T10:03:29.1065990 Output 2200550 application/pdf Version of Record true Copyright © 2022 the Author(s). This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). true eng https://creativecommons.org/licenses/by-nc-nd/4.0/
title A Pleistocene legacy structures variation in modern seagrass ecosystems
spellingShingle A Pleistocene legacy structures variation in modern seagrass ecosystems
John Griffin
Richard Unsworth
title_short A Pleistocene legacy structures variation in modern seagrass ecosystems
title_full A Pleistocene legacy structures variation in modern seagrass ecosystems
title_fullStr A Pleistocene legacy structures variation in modern seagrass ecosystems
title_full_unstemmed A Pleistocene legacy structures variation in modern seagrass ecosystems
title_sort A Pleistocene legacy structures variation in modern seagrass ecosystems
author_id_str_mv 9814fbffa76dd9c9a207166354cd0b2f
b0f33acd13a3ab541cf2aaea27f4fc2f
author_id_fullname_str_mv 9814fbffa76dd9c9a207166354cd0b2f_***_John Griffin
b0f33acd13a3ab541cf2aaea27f4fc2f_***_Richard Unsworth
author John Griffin
Richard Unsworth
author2 J. Emmett Duffy
John J. Stachowicz
Pamela L. Reynolds
Kevin A. Hovel
Marlene Jahnke
Erik E. Sotka
Christoffer Boström
Katharyn E. Boyer
Mathieu Cusson
Johan Eklöf
Aschwin H. Engelen
Britas Klemens Eriksson
F. Joel Fodrie
John Griffin
Clara M. Hereu
Masakazu Hori
A. Randall Hughes
Mikhail V. Ivanov
Pablo Jorgensen
Claudia Kruschel
Kun-Seop Lee
Jonathan S. Lefcheck
Per-Olav Moksnes
Masahiro Nakaoka
Mary I. O’Connor
Nessa E. O’Connor
Robert J. Orth
Bradley J. Peterson
Henning Reiss
Katrin Reiss
J. Paul Richardson
Francesca Rossi
Jennifer L. Ruesink
Stewart T. Schultz
Jonas Thormar
Fiona Tomas
Richard Unsworth
Erin Voigt
Matthew A. Whalen
Shelby L. Ziegler
Jeanine L. Olsen
format Journal article
container_title Proceedings of the National Academy of Sciences
container_volume 119
container_issue 32
publishDate 2022
institution Swansea University
issn 0027-8424
1091-6490
doi_str_mv 10.1073/pnas.2121425119
publisher Proceedings of the National Academy of Sciences
college_str Faculty of Science and Engineering
hierarchytype
hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
document_store_str 1
active_str 0
description Distribution of Earth’s biomes is structured by the match between climate and plant traits, which in turn shape associated communities and ecosystem processes and services. However, that climate–trait match can be disrupted by historical events, with lasting ecosystem impacts. As Earth’s environment changes faster than at any time in human history, critical questions are whether and how organismal traits and ecosystems can adjust to altered conditions. We quantified the relative importance of current environmental forcing versus evolutionary history in shaping the growth form (stature and biomass) and associated community of eelgrass (Zostera marina), a widespread foundation plant of marine ecosystems along Northern Hemisphere coastlines, which experienced major shifts in distribution and genetic composition during the Pleistocene. We found that eelgrass stature and biomass retain a legacy of the Pleistocene colonization of the Atlantic from the ancestral Pacific range and of more recent within-basin bottlenecks and genetic differentiation. This evolutionary legacy in turn influences the biomass of associated algae and invertebrates that fuel coastal food webs, with effects comparable to or stronger than effects of current environmental forcing. Such historical lags in phenotypic acclimatization may constrain ecosystem adjustments to rapid anthropogenic climate change, thus altering predictions about the future functioning of ecosystems.
published_date 2022-08-01T04:19:12Z
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