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Opposing genetic patterns of range shifting temperate and tropical gastropods in an area undergoing tropicalisation

Opposing genetic patterns of range shifting temperate and tropical gastropods in an area undergoing tropicalisation
Opposing genetic patterns of range shifting temperate and tropical gastropods in an area undergoing tropicalisation
Aim: the poleward range expansion of tropical species, and range contraction of temperate species (known as tropicalisation) has mainly been studied from an ecological perspective, with little research on its genetic consequences. Here, we used distributional and genetic data to document the consequences of tropicalisation in rocky shore gastropods and assess more broadly the future implications of tropicalisation on phylogeographic patterns.

Location: nineteen sampling sites along >3000 km of the eastern Pacific rocky intertidal zone, from the tip of the Baja California Peninsula to southern California.

Taxon
Temperate gastropods: Lottia conus, L. strigatella, Fissurella volcano and Tegula gallina.

Tropical gastropods: Fissurella rubropicta, Nerita funiculata and N. scabricosta.

Methods: we determine historical and modern distributions of tropical and temperate species by combining historical records with current field surveys. Using a section of the cytochrome oxidase subunit I gene, we utilised comparative phylogeography, analysis of molecular variance, FST pairwise comparison, mismatch distributions of haplotype differences and neutrality tests to detect genetic signatures of tropicalisation and to better understand its consequences.

Results: we identified range contractions in two temperate species and range expansion in all three tropical species. We detected genetic signatures of range expansion in the tropical species through unimodal distributions of pairwise haplotype differences and strongly negative values for the Fu and Li D and F* statistics. We found population subdivision and phylogeographic breaks in three temperate species, although the geographic location of the breaks differed among species.

Main conclusions: genetic signatures and field surveys indicate recent range expansions in tropical species, supporting tropicalisation along the studied coastline. Conversely, we found phylogeographic breaks in temperate species, suggesting that tropicalisation may cause genetic erosion of evolutionary distinct lineages with range-contraction. The different locations of the phylogeographic breaks among temperate species suggests that some barriers are species specific.
Eastern Pacific, Gulf of California, biogeographic barriers, landscape genetics, range shifts, rocky shores, tropicalisation
0305-0270
246-262
Zarzyczny, Karolina Magdalena
f413d318-ce7a-4899-8502-88989b9af01a
Hellberg, Michael E.
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Lugli, Elena B.
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Maclean, Moira
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Paz-Garcia, David A.
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Rius, Marc
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Ross, Ethan G.
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Treviño Balandra, Erick X.
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Vanstone, James
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Williams, Suzanne T.
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Fenberg, Phillip B.
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Zarzyczny, Karolina Magdalena
f413d318-ce7a-4899-8502-88989b9af01a
Hellberg, Michael E.
da2fb3b9-556c-4943-9520-e19524a16aaa
Lugli, Elena B.
1e93b87c-878c-42ff-abc9-20ba3edb27af
Maclean, Moira
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Paz-Garcia, David A.
dd1aed4c-901e-4a93-b06f-ce4922f0415c
Rius, Marc
c4e88345-4b4e-4428-b4b2-37229155f68d
Ross, Ethan G.
aa81f807-2dfd-4e73-ab8f-125ac923ff8b
Treviño Balandra, Erick X.
ead1d7ed-8410-493a-9995-961143030719
Vanstone, James
16b95649-7244-4829-a00c-021723af3640
Williams, Suzanne T.
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Fenberg, Phillip B.
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Zarzyczny, Karolina Magdalena, Hellberg, Michael E., Lugli, Elena B., Maclean, Moira, Paz-Garcia, David A., Rius, Marc, Ross, Ethan G., Treviño Balandra, Erick X., Vanstone, James, Williams, Suzanne T. and Fenberg, Phillip B. (2024) Opposing genetic patterns of range shifting temperate and tropical gastropods in an area undergoing tropicalisation. Journal of Biogeography, 51 (2), 246-262. (doi:10.1111/jbi.14744).

Record type: Article

Abstract

Aim: the poleward range expansion of tropical species, and range contraction of temperate species (known as tropicalisation) has mainly been studied from an ecological perspective, with little research on its genetic consequences. Here, we used distributional and genetic data to document the consequences of tropicalisation in rocky shore gastropods and assess more broadly the future implications of tropicalisation on phylogeographic patterns.

Location: nineteen sampling sites along >3000 km of the eastern Pacific rocky intertidal zone, from the tip of the Baja California Peninsula to southern California.

Taxon
Temperate gastropods: Lottia conus, L. strigatella, Fissurella volcano and Tegula gallina.

Tropical gastropods: Fissurella rubropicta, Nerita funiculata and N. scabricosta.

Methods: we determine historical and modern distributions of tropical and temperate species by combining historical records with current field surveys. Using a section of the cytochrome oxidase subunit I gene, we utilised comparative phylogeography, analysis of molecular variance, FST pairwise comparison, mismatch distributions of haplotype differences and neutrality tests to detect genetic signatures of tropicalisation and to better understand its consequences.

Results: we identified range contractions in two temperate species and range expansion in all three tropical species. We detected genetic signatures of range expansion in the tropical species through unimodal distributions of pairwise haplotype differences and strongly negative values for the Fu and Li D and F* statistics. We found population subdivision and phylogeographic breaks in three temperate species, although the geographic location of the breaks differed among species.

Main conclusions: genetic signatures and field surveys indicate recent range expansions in tropical species, supporting tropicalisation along the studied coastline. Conversely, we found phylogeographic breaks in temperate species, suggesting that tropicalisation may cause genetic erosion of evolutionary distinct lineages with range-contraction. The different locations of the phylogeographic breaks among temperate species suggests that some barriers are species specific.

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Journal of Biogeography - 2023 - Zarzyczny - Opposing genetic patterns of range shifting temperate and tropical gastropods - Version of Record
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Accepted/In Press date: 28 September 2023
Published date: February 2024
Additional Information: Funding Information: We thank Lindsey T. Groves (Natural History Museum of Los Angeles), John Slapcinsky (University of Florida Museum) and Alex Kittle (Delaware Museum of Nature and Science) for providing collection images which allowed us to confirm species occurrences. We thank Eva Gallardo who supported some of the fieldwork in Mexico, Louise Cooke who assisted with DNA extraction of some Lottia strigatella samples, Dr Scott Herke (Louisiana State University) who provided support with PCR of tricky samples and carried out some of the sequencing, and Dr John Gittins who provided troubleshooting advice throughout the molecular work. Finally, we thank Dr Karine Posbic and Erick Bolaños Duran for support with some of the genetic analysis. This work was supported by the Natural Environmental Research Council (NE/S007210/1) to KMZ and (NE/X011518/1) to PBF; an Early Career Research Grant from the Malacological Society of London, and a Heredity Fieldwork Grant from the Genetics Society to KMZ; and The Royal Society (RG2017R1) to PBF. The permit to collect the samples was provided by the Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación (SAGARPA, Permiso de Pesca de Fomento No. PPF/DGOPA-291/17 and PPF/DGOPA-010/19). Funding Information: We thank Lindsey T. Groves (Natural History Museum of Los Angeles), John Slapcinsky (University of Florida Museum) and Alex Kittle (Delaware Museum of Nature and Science) for providing collection images which allowed us to confirm species occurrences. We thank Eva Gallardo who supported some of the fieldwork in Mexico, Louise Cooke who assisted with DNA extraction of some samples, Dr Scott Herke (Louisiana State University) who provided support with PCR of tricky samples and carried out some of the sequencing, and Dr John Gittins who provided troubleshooting advice throughout the molecular work. Finally, we thank Dr Karine Posbic and Erick Bolaños Duran for support with some of the genetic analysis. This work was supported by the Natural Environmental Research Council (NE/S007210/1) to KMZ and (NE/X011518/1) to PBF; an Early Career Research Grant from the Malacological Society of London, and a Heredity Fieldwork Grant from the Genetics Society to KMZ; and The Royal Society (RG2017R1) to PBF. The permit to collect the samples was provided by the Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación (SAGARPA, Permiso de Pesca de Fomento No. PPF/DGOPA‐291/17 and PPF/DGOPA‐010/19). Lottia strigatella Publisher Copyright: © 2023 The Authors. Journal of Biogeography published by John Wiley & Sons Ltd.
Keywords: Eastern Pacific, Gulf of California, biogeographic barriers, landscape genetics, range shifts, rocky shores, tropicalisation

Identifiers

Local EPrints ID: 483055
URI: http://eprints.soton.ac.uk/id/eprint/483055
ISSN: 0305-0270
PURE UUID: ce63dae4-bf3d-4679-9288-377830adf5ad
ORCID for Moira Maclean: ORCID iD orcid.org/0000-0002-0821-5781
ORCID for Phillip B. Fenberg: ORCID iD orcid.org/0000-0003-4474-176X

Catalogue record

Date deposited: 20 Oct 2023 16:55
Last modified: 15 Jun 2024 01:46

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Contributors

Author: Michael E. Hellberg
Author: Elena B. Lugli
Author: Moira Maclean ORCID iD
Author: David A. Paz-Garcia
Author: Marc Rius
Author: Ethan G. Ross
Author: Erick X. Treviño Balandra
Author: James Vanstone
Author: Suzanne T. Williams

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