Genomic resolution of cryptic species diversity in chipmunks

Nathanael D. Herrera; Kayce C. Bell; Colin M. Callahan; Erin Nordquist; Brice A.J. Sarver; Jack Sullivan; John R. Demboski; Jeffrey M. Good

doi:10.1111/evo.14546

Genomic resolution of cryptic species diversity in chipmunks

Nathanael D. Herrera, Kayce C. Bell, Colin M. Callahan, Erin Nordquist, Brice A.J. Sarver, Jack Sullivan, John R. Demboski, Jeffrey M. Good

Division of Biological and Biomedical Sciences

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

11 Scopus citations

Abstract

Discovery of cryptic species is essential to understand the process of speciation and assessing the impacts of anthropogenic stressors. Here, we used genomic data to test for cryptic species diversity within an ecologically well-known radiation of North American rodents, western chipmunks (Tamias). We assembled a de novo reference genome for a single species (Tamias minimus) combined with new and published targeted sequence-capture data for 21,551 autosomal and 493 X-linked loci sampled from 121 individuals spanning 22 species. We identified at least two cryptic lineages corresponding with an isolated subspecies of least chipmunk (T. minimus grisescens) and with a restricted subspecies of the yellow-pine chipmunk (Tamias amoenus cratericus) known only from around the extensive Craters of the Moon lava flow. Additional population-level sequence data revealed that the so-called Crater chipmunk is a distinct species that is abundant throughout the coniferous forests of southern Idaho. This cryptic lineage does not appear to be most closely related to the ecologically and phenotypically similar yellow-pine chipmunk but does show evidence for recurrent hybridization with this and other species.

Original language	English
Pages (from-to)	2004-2019
Number of pages	16
Journal	Evolution
Volume	76
Issue number	9
DOIs	https://doi.org/10.1111/evo.14546
State	Published - Sep 2022

Funding

Our research would not be possible without the irreplaceable support of natural history museums. We are grateful to the collections staff of The Denver Museum of Nature & Science, the UC Berkeley Museum of Vertebrate Zoology, and Joseph A. Cook and the University of New Mexico Museum of Southwest Biology for providing tissue loans. We also thank Michael Fazekas, Roger Rodriguez, Patricia McDonald, Randle McCain, Bryan McLean, Schuyler Liphardt, and Lois Alexander for help with fieldwork. We thank David Xing, Jessi Kopperdahl, Mickael Fazekas, and Sara Keeble for assisting with molecular work. We thank members of the Good lab, the University of Montana UNVEIL network, Ke Bi, and Craig Moritz for helpful discussions. Funding support for this research was provided by a grant from the National Science Foundation (NSF) EPSCoR (OIA‐1736249 to JMG), NSF (DEB‐0716200 to JRD), a travel grant from the Drollinger‐Dial Foundation, the Gordon and Betty Moore Foundation (GBMF2983), the Rose Community Foundation, and research funds from the University of Montana and Denver Museum of Nature & Science. This study included research conducted in the University of Montana Genomics Core, supported by a grant from the M. J. Murdock Charitable Trust (to JMG). Computational resources and support from the University of Montana's Griz Shared Computing Cluster (GSCC), supported by grants from the Nation Science Foundation (CC‐2018112 and OAC‐1925267), contributed to this research. The DNA isolation, library preparation, and sequencing of the draft genome was carried out at the DNA Technologies and Expression Analysis Core at the UC Davis Genome Center, supported by NIH Shared Instrument Grant 1S10OD010786‐01. Tamias minimus Our research would not be possible without the irreplaceable support of natural history museums. We are grateful to the collections staff of The Denver Museum of Nature & Science, the UC Berkeley Museum of Vertebrate Zoology, and Joseph A. Cook and the University of New Mexico Museum of Southwest Biology for providing tissue loans. We also thank Michael Fazekas, Roger Rodriguez, Patricia McDonald, Randle McCain, Bryan McLean, Schuyler Liphardt, and Lois Alexander for help with fieldwork. We thank David Xing, Jessi Kopperdahl, Mickael Fazekas, and Sara Keeble for assisting with molecular work. We thank members of the Good lab, the University of Montana UNVEIL network, Ke Bi, and Craig Moritz for helpful discussions. Funding support for this research was provided by a grant from the National Science Foundation (NSF) EPSCoR (OIA-1736249 to JMG), NSF (DEB-0716200 to JRD), a travel grant from the Drollinger-Dial Foundation, the Gordon and Betty Moore Foundation (GBMF2983), the Rose Community Foundation, and research funds from the University of Montana and Denver Museum of Nature & Science. This study included research conducted in the University of Montana Genomics Core, supported by a grant from the M. J. Murdock Charitable Trust (to JMG). Computational resources and support from the University of Montana's Griz Shared Computing Cluster (GSCC), supported by grants from the Nation Science Foundation (CC-2018112 and OAC-1925267), contributed to this research. The DNA isolation, library preparation, and sequencing of the draft Tamias minimus genome was carried out at the DNA Technologies and Expression Analysis Core at the UC Davis Genome Center, supported by NIH Shared Instrument Grant 1S10OD010786-01.

Funders	Funder number
Denver Museum of Nature & Science
CC‐2018112, OAC‐1925267
S10OD010786
GBMF2983
OIA‐1736249, DEB‐0716200
Denver Museum of Nature & Science

Keywords

Hybridization
Neotamias
Tamias
introgression
phylogenomics
speciation

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10.1111/evo.14546

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title = "Genomic resolution of cryptic species diversity in chipmunks",

abstract = "Discovery of cryptic species is essential to understand the process of speciation and assessing the impacts of anthropogenic stressors. Here, we used genomic data to test for cryptic species diversity within an ecologically well-known radiation of North American rodents, western chipmunks (Tamias). We assembled a de novo reference genome for a single species (Tamias minimus) combined with new and published targeted sequence-capture data for 21,551 autosomal and 493 X-linked loci sampled from 121 individuals spanning 22 species. We identified at least two cryptic lineages corresponding with an isolated subspecies of least chipmunk (T. minimus grisescens) and with a restricted subspecies of the yellow-pine chipmunk (Tamias amoenus cratericus) known only from around the extensive Craters of the Moon lava flow. Additional population-level sequence data revealed that the so-called Crater chipmunk is a distinct species that is abundant throughout the coniferous forests of southern Idaho. This cryptic lineage does not appear to be most closely related to the ecologically and phenotypically similar yellow-pine chipmunk but does show evidence for recurrent hybridization with this and other species.",

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AU - Sarver, Brice A.J.

AU - Sullivan, Jack

AU - Demboski, John R.

AU - Good, Jeffrey M.

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N2 - Discovery of cryptic species is essential to understand the process of speciation and assessing the impacts of anthropogenic stressors. Here, we used genomic data to test for cryptic species diversity within an ecologically well-known radiation of North American rodents, western chipmunks (Tamias). We assembled a de novo reference genome for a single species (Tamias minimus) combined with new and published targeted sequence-capture data for 21,551 autosomal and 493 X-linked loci sampled from 121 individuals spanning 22 species. We identified at least two cryptic lineages corresponding with an isolated subspecies of least chipmunk (T. minimus grisescens) and with a restricted subspecies of the yellow-pine chipmunk (Tamias amoenus cratericus) known only from around the extensive Craters of the Moon lava flow. Additional population-level sequence data revealed that the so-called Crater chipmunk is a distinct species that is abundant throughout the coniferous forests of southern Idaho. This cryptic lineage does not appear to be most closely related to the ecologically and phenotypically similar yellow-pine chipmunk but does show evidence for recurrent hybridization with this and other species.

AB - Discovery of cryptic species is essential to understand the process of speciation and assessing the impacts of anthropogenic stressors. Here, we used genomic data to test for cryptic species diversity within an ecologically well-known radiation of North American rodents, western chipmunks (Tamias). We assembled a de novo reference genome for a single species (Tamias minimus) combined with new and published targeted sequence-capture data for 21,551 autosomal and 493 X-linked loci sampled from 121 individuals spanning 22 species. We identified at least two cryptic lineages corresponding with an isolated subspecies of least chipmunk (T. minimus grisescens) and with a restricted subspecies of the yellow-pine chipmunk (Tamias amoenus cratericus) known only from around the extensive Craters of the Moon lava flow. Additional population-level sequence data revealed that the so-called Crater chipmunk is a distinct species that is abundant throughout the coniferous forests of southern Idaho. This cryptic lineage does not appear to be most closely related to the ecologically and phenotypically similar yellow-pine chipmunk but does show evidence for recurrent hybridization with this and other species.

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KW - introgression

KW - phylogenomics

KW - speciation

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SN - 0014-3820

VL - 76

SP - 2004

EP - 2019

JO - Evolution

JF - Evolution

IS - 9

ER -

Genomic resolution of cryptic species diversity in chipmunks

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Keywords

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