The genetic legacy of a global marine invader

E Erik E. Sotka (Department of Biology, College of Charleston) R Ryan B. Carnegie (Virginia Institute of Marine Science, College of William and Mary) J James T. Carlton (Williams College-Mystic Seaport Coastal and Ocean Studies Program) L Lucia Couceiro (Facultade de Ciencias, Departamento de Bioloxía, Universidade da Coruña) J Jeffrey A. Crooks (Tijuana River National Estuarine Research Reserve) H Hikaru Endo (Faculty of Fisheries, Kagoshima University) H Hilary Hayford (Puget Sound Restoration Fund) M Masakazu Hori (Japan Fisheries Research and Education Agency) M Mitsunobu Kamiya (Department of Ocean Sciences, Tokyo University of Marine Science and Technology) G Gen Kanaya (National Institute for Environmental Studies) J Judith Kochmann (Faculty of Biology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg University) K Kun-Seop Lee (Department of Biological Sciences, Pusan National University) L Lauren Lees (Department of Ecology and Evolutionary Biology, University of California) H Hannah Miller (Department of Biology, College of Charleston) M Masahiro Nakaoka (Akkeshi Marine Station, Field Science Center for Northern Biosphere, Hokkaido University) E Eric Pante (CNRS, IRD, Ifremer, UMR 6539, Laboratory of Environmental Marine Sciences (LEMAR), Université de Bretagne) J Jennifer L. Ruesink (Department of Biology, University of Washington) E Evangelina Schwindt (Instituto de Biología de Organismos Marinos, Consejo Nacional de Investigaciones Científicas y Técnicas (IBIOMAR-CONICET)) Åsa Strand (Department of Environmental Intelligence, IVL Swedish Environmental Research Institute) R Richard B. Taylor (Leigh Marine Laboratory and Institute of Marine Science, University of Auckland) R Ryuta Terada (Faculty of Fisheries, Kagoshima University) M Martin Thiel T Takefumi Yorisue (Nature and Environment Division, Institute of Natural and Environmental Sciences, University of Hyogo) D Danielle Zacherl (Department of Biological Science, California State University) A Allan E. Strand (Department of Biology, College of Charleston)

Abstract

The massive geographic expansion of terrestrial plant crops, livestock, and marine aquacultured species during the 19th and 20th centuries provided local economic benefits, stabilized food demands, and altered local ecosystems. The invasion history of these translocations remains uncertain for most species, limiting our understanding of their future adaptive potential and historical roles as vectors for coinvaded species. We provide a framework for filling this gap in invasion biology using the widely transplanted Pacific oyster as a case study. A two-dimensional summary of population-level variation in single nucleotide polymorphisms in native Japan reflected the geographical map of Japan and allowed identification of the source regions for the worldwide expansion. Pacific oysters proliferate in nonnative areas with environmental temperatures similar to those areas where native lineages evolved. Using Approximate Bayesian Computation, we ranked the likelihood of historical oyster or shipping vectors to explain current-day distribution of genotypes in 14 coinvaded algal and animal species. Oyster transplants were a more likely vector than shipping for six species, shipping activity was more likely for five species, and a vector was ambiguous for three species. Applying this approach to other translocated species should reveal similar legacy effects, especially for economically important foundation species that also served as vectors for nonnative species.

Article Details

Volume / Issue Vol. 122, Issue 15
Published April 15, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (25)

E

Erik E. Sotka

Department of Biology, College of Charleston

R

Ryan B. Carnegie

Virginia Institute of Marine Science, College of William and Mary

J

James T. Carlton

Williams College-Mystic Seaport Coastal and Ocean Studies Program

L

Lucia Couceiro

Facultade de Ciencias, Departamento de Bioloxía, Universidade da Coruña

J

Jeffrey A. Crooks

Tijuana River National Estuarine Research Reserve

H

Hikaru Endo

Faculty of Fisheries, Kagoshima University

H

Hilary Hayford

Puget Sound Restoration Fund

M

Masakazu Hori

Japan Fisheries Research and Education Agency

M

Mitsunobu Kamiya

Department of Ocean Sciences, Tokyo University of Marine Science and Technology

G

Gen Kanaya

National Institute for Environmental Studies

J

Judith Kochmann

Faculty of Biology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg University

K

Kun-Seop Lee

Department of Biological Sciences, Pusan National University

L

Lauren Lees

Department of Ecology and Evolutionary Biology, University of California

H

Hannah Miller

Department of Biology, College of Charleston

M

Masahiro Nakaoka

Akkeshi Marine Station, Field Science Center for Northern Biosphere, Hokkaido University

E

Eric Pante

CNRS, IRD, Ifremer, UMR 6539, Laboratory of Environmental Marine Sciences (LEMAR), Université de Bretagne

J

Jennifer L. Ruesink

Department of Biology, University of Washington

E

Evangelina Schwindt

Instituto de Biología de Organismos Marinos, Consejo Nacional de Investigaciones Científicas y Técnicas (IBIOMAR-CONICET)

Åsa Strand

Department of Environmental Intelligence, IVL Swedish Environmental Research Institute

R

Richard B. Taylor

Leigh Marine Laboratory and Institute of Marine Science, University of Auckland

R

Ryuta Terada

Faculty of Fisheries, Kagoshima University

M

Martin Thiel

T

Takefumi Yorisue

Nature and Environment Division, Institute of Natural and Environmental Sciences, University of Hyogo

D

Danielle Zacherl

Department of Biological Science, California State University

A

Allan E. Strand

Department of Biology, College of Charleston