Geography is more important than life history in the recent diversification of the tiger salamander complex

Kathryn M. Everson; Levi N. Gray; Angela G. Jones; Nicolette M. Lawrence; Mary E. Foley; Kelly L. Sovacool; Justin D. Kratovil; Scott Hotaling; Paul M. Hime; Andrew Storfer; Gabriela Parra-Olea; Ruth Percino-Daniel; X. Aguilar-Miguel; Eric M. O’Neill; Luis Zambrano; H. Bradley Shaffer; David W. Weisrock

doi:10.1073/pnas.2014719118

Geography is more important than life history in the recent diversification of the tiger salamander complex

Kathryn M. Everson, Levi N. Gray, Angela G. Jones, Nicolette M. Lawrence, Mary E. Foley, Kelly L. Sovacool, Justin D. Kratovil, Scott Hotaling, Paul M. Hime, Andrew Storfer, Gabriela Parra-Olea, Ruth Percino-Daniel, X. Aguilar-Miguel, Eric M. O’Neill, Luis Zambrano, H. Bradley Shaffer, David W. Weisrock

Research output: Contribution to journal › Article › peer-review

25 Scopus citations

Abstract

The North American tiger salamander species complex, including its best-known species, the Mexican axolotl, has long been a source of biological fascination. The complex exhibits a wide range of variation in developmental life history strategies, including populations and individuals that undergo metamorphosis; those able to forego metamorphosis and retain a larval, aquatic lifestyle (i.e., paedomorphosis); and those that do both. The evolution of a paedomorphic life history state is thought to lead to increased population genetic differentiation and ultimately reproductive isolation and speciation, but the degree to which it has shaped population- and species-level divergence is poorly understood. Using a large multilocus dataset from hundreds of samples across North America, we identified genetic clusters across the geographic range of the tiger salamander complex. These clusters often contain a mixture of paedomorphic and metamorphic taxa, indicating that geographic isolation has played a larger role in lineage divergence than paedomorphosis in this system. This conclusion is bolstered by geography-informed analyses indicating no effect of life history strategy on population genetic differentiation and by model-based population genetic analyses demonstrating gene flow between adjacent metamorphic and paedomorphic populations. This fine-scale genetic perspective on life history variation establishes a framework for understanding how plasticity, local adaptation, and gene flow contribute to lineage divergence. Many members of the tiger salamander complex are endangered, and the Mexican axolotl is an important model system in regenerative and biomedical research. Our results chart a course for more informed use of these taxa in experimental, ecological, and conservation research.

Original language	English
Article number	e2014719118
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	118
Issue number	17
DOIs	https://doi.org/10.1073/pnas.2014719118
State	Published - Apr 27 2021

Bibliographical note

Publisher Copyright:
© 2021 National Academy of Sciences. All rights reserved.

Funding

This project was supported by grants from the NSF (DEB-0949532, DEB-1355000, and DEB-1406876 [DDIG awarded to J.D.K.]) and by a University Research Fellowship awarded to K.M.E. from the University of Kentucky. We thank Chris Beachy, Jim Bogart, Ken Carbale, Sheri Church, Jeff LeClere, Carol Hall, Paul Moler, Nancy Staub, and Ken Wray for genetic samples and Jose Bocanegra, Ben Browning, Mackenzie Humphrey, Mary Virginia Gibbs, Ricky Grewelle, Alan Lemmon, Emily Moriarty Lemmon, Deborah Lu, Stephanie Mitchell, Alex Noble, Tolu Odukoya, Ben Tuttle, and Josh Williams for assistance with data collection and analyses. ACKNOWLEDGMENTS. This project was supported by grants from the NSF (DEB-0949532, DEB-1355000, and DEB-1406876 [DDIG awarded to J.D.K.]) and by a University Research Fellowship awarded to K.M.E. from the University of Kentucky. We thank Chris Beachy, Jim Bogart, Ken Carbale, Sheri Church, Jeff LeClere, Carol Hall, Paul Moler, Nancy Staub, and Ken Wray for genetic samples and Jose Bocanegra, Ben Browning, Mackenzie Humphrey, Mary Virginia Gibbs, Ricky Grewelle, Alan Lemmon, Emily Moriarty Lemmon, Deborah Lu, Stephanie Mitchell, Alex Noble, Tolu Odukoya, Ben Tuttle, and Josh Williams for assistance with data collection and analyses.

Funders	Funder number
Ken Wray
University of Kentucky
U.S. Department of Energy Chinese Academy of Sciences Guangzhou Municipal Science and Technology Project Oak Ridge National Laboratory Extreme Science and Engineering Discovery Environment National Science Foundation National Energy Research Scientific Computing Center National Natural Science Foundation of China	0949532, DEB-0949532, DEB-1355000, DEB-1406876
U.S. Department of Energy Chinese Academy of Sciences Guangzhou Municipal Science and Technology Project Oak Ridge National Laboratory Extreme Science and Engineering Discovery Environment National Science Foundation National Energy Research Scientific Computing Center National Natural Science Foundation of China
National Institute of General Medical Sciences DP2GM119177 Sophie Dumont National Institute of General Medical Sciences	T32GM070449
National Institute of General Medical Sciences DP2GM119177 Sophie Dumont National Institute of General Medical Sciences

Keywords

Ambystoma
Life history
Phylogenetics
Population genomics
Salamanders

ASJC Scopus subject areas

General

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10.1073/pnas.2014719118

Cite this

Everson, K. M., Gray, L. N., Jones, A. G., Lawrence, N. M., Foley, M. E., Sovacool, K. L., Kratovil, J. D., Hotaling, S., Hime, P. M., Storfer, A., Parra-Olea, G., Percino-Daniel, R., Aguilar-Miguel, X., O’Neill, E. M., Zambrano, L., Bradley Shaffer, H., & Weisrock, D. W. (2021). Geography is more important than life history in the recent diversification of the tiger salamander complex. Proceedings of the National Academy of Sciences of the United States of America, 118(17), Article e2014719118. https://doi.org/10.1073/pnas.2014719118

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title = "Geography is more important than life history in the recent diversification of the tiger salamander complex",

abstract = "The North American tiger salamander species complex, including its best-known species, the Mexican axolotl, has long been a source of biological fascination. The complex exhibits a wide range of variation in developmental life history strategies, including populations and individuals that undergo metamorphosis; those able to forego metamorphosis and retain a larval, aquatic lifestyle (i.e., paedomorphosis); and those that do both. The evolution of a paedomorphic life history state is thought to lead to increased population genetic differentiation and ultimately reproductive isolation and speciation, but the degree to which it has shaped population- and species-level divergence is poorly understood. Using a large multilocus dataset from hundreds of samples across North America, we identified genetic clusters across the geographic range of the tiger salamander complex. These clusters often contain a mixture of paedomorphic and metamorphic taxa, indicating that geographic isolation has played a larger role in lineage divergence than paedomorphosis in this system. This conclusion is bolstered by geography-informed analyses indicating no effect of life history strategy on population genetic differentiation and by model-based population genetic analyses demonstrating gene flow between adjacent metamorphic and paedomorphic populations. This fine-scale genetic perspective on life history variation establishes a framework for understanding how plasticity, local adaptation, and gene flow contribute to lineage divergence. Many members of the tiger salamander complex are endangered, and the Mexican axolotl is an important model system in regenerative and biomedical research. Our results chart a course for more informed use of these taxa in experimental, ecological, and conservation research.",

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Everson, KM, Gray, LN, Jones, AG, Lawrence, NM, Foley, ME, Sovacool, KL, Kratovil, JD, Hotaling, S, Hime, PM, Storfer, A, Parra-Olea, G, Percino-Daniel, R, Aguilar-Miguel, X, O’Neill, EM, Zambrano, L, Bradley Shaffer, H & Weisrock, DW 2021, 'Geography is more important than life history in the recent diversification of the tiger salamander complex', Proceedings of the National Academy of Sciences of the United States of America, vol. 118, no. 17, e2014719118. https://doi.org/10.1073/pnas.2014719118

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T1 - Geography is more important than life history in the recent diversification of the tiger salamander complex

AU - Everson, Kathryn M.

AU - Gray, Levi N.

AU - Jones, Angela G.

AU - Lawrence, Nicolette M.

AU - Foley, Mary E.

AU - Sovacool, Kelly L.

AU - Kratovil, Justin D.

AU - Hotaling, Scott

AU - Hime, Paul M.

AU - Storfer, Andrew

AU - Parra-Olea, Gabriela

AU - Percino-Daniel, Ruth

AU - Aguilar-Miguel, X.

AU - O’Neill, Eric M.

AU - Zambrano, Luis

AU - Bradley Shaffer, H.

AU - Weisrock, David W.

PY - 2021/4/27

Y1 - 2021/4/27

N2 - The North American tiger salamander species complex, including its best-known species, the Mexican axolotl, has long been a source of biological fascination. The complex exhibits a wide range of variation in developmental life history strategies, including populations and individuals that undergo metamorphosis; those able to forego metamorphosis and retain a larval, aquatic lifestyle (i.e., paedomorphosis); and those that do both. The evolution of a paedomorphic life history state is thought to lead to increased population genetic differentiation and ultimately reproductive isolation and speciation, but the degree to which it has shaped population- and species-level divergence is poorly understood. Using a large multilocus dataset from hundreds of samples across North America, we identified genetic clusters across the geographic range of the tiger salamander complex. These clusters often contain a mixture of paedomorphic and metamorphic taxa, indicating that geographic isolation has played a larger role in lineage divergence than paedomorphosis in this system. This conclusion is bolstered by geography-informed analyses indicating no effect of life history strategy on population genetic differentiation and by model-based population genetic analyses demonstrating gene flow between adjacent metamorphic and paedomorphic populations. This fine-scale genetic perspective on life history variation establishes a framework for understanding how plasticity, local adaptation, and gene flow contribute to lineage divergence. Many members of the tiger salamander complex are endangered, and the Mexican axolotl is an important model system in regenerative and biomedical research. Our results chart a course for more informed use of these taxa in experimental, ecological, and conservation research.

AB - The North American tiger salamander species complex, including its best-known species, the Mexican axolotl, has long been a source of biological fascination. The complex exhibits a wide range of variation in developmental life history strategies, including populations and individuals that undergo metamorphosis; those able to forego metamorphosis and retain a larval, aquatic lifestyle (i.e., paedomorphosis); and those that do both. The evolution of a paedomorphic life history state is thought to lead to increased population genetic differentiation and ultimately reproductive isolation and speciation, but the degree to which it has shaped population- and species-level divergence is poorly understood. Using a large multilocus dataset from hundreds of samples across North America, we identified genetic clusters across the geographic range of the tiger salamander complex. These clusters often contain a mixture of paedomorphic and metamorphic taxa, indicating that geographic isolation has played a larger role in lineage divergence than paedomorphosis in this system. This conclusion is bolstered by geography-informed analyses indicating no effect of life history strategy on population genetic differentiation and by model-based population genetic analyses demonstrating gene flow between adjacent metamorphic and paedomorphic populations. This fine-scale genetic perspective on life history variation establishes a framework for understanding how plasticity, local adaptation, and gene flow contribute to lineage divergence. Many members of the tiger salamander complex are endangered, and the Mexican axolotl is an important model system in regenerative and biomedical research. Our results chart a course for more informed use of these taxa in experimental, ecological, and conservation research.

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KW - Phylogenetics

KW - Population genomics

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Geography is more important than life history in the recent diversification of the tiger salamander complex

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

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