Temporal genomic contrasts reveal rapid evolutionary responses in an alpine mammal during recent climate change
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Many species have experienced dramatic changes in their abundance and distribution during recent climate change, but it is often unclear whether such ecological responses are accompanied by evolutionary change. We used targeted exon sequencing of 294 museum specimens (160 historic, 134 modern) to generate independent temporal genomic contrasts spanning a century of climate change (1911–2012) for two co-distributed chipmunk species: an endemic alpine specialist (Tamias alpinus) undergoing severe range contraction and a stable mid-elevation species (T. speciosus). Using a novel analytical approach, we reconstructed the demographic histories of these populations and tested for evidence of recent positive directional selection. Only the retracting species showed substantial population genetic fragmentation through time and this was coupled with positive selection and substantial shifts in allele frequencies at a gene, Alox15, involved in regulation of inflammation and response to hypoxia. However, these rapid population and gene-level responses were not detected in an analogous temporal contrast from another area where T. alpinus has also undergone severe range contraction. Collectively, these results highlight that evolutionary responses may be variable and context dependent across populations, even when they show seemingly synchronous ecological shifts. Our results demonstrate that temporal genomic contrasts can be used to detect very recent evolutionary responses within and among contemporary populations, even in the face of complex demographic changes. Given the wealth of specimens archived in natural history museums, comparative analyses of temporal population genomic data have the potential to improve our understanding of recent and ongoing evolutionary responses to rapidly changing environments.
Originalsprog | Engelsk |
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Artikelnummer | e1008119 |
Tidsskrift | PLOS Genetics |
Vol/bind | 15 |
Udgave nummer | 5 |
Antal sider | 22 |
ISSN | 1553-7390 |
DOI | |
Status | Udgivet - 2019 |
Eksternt udgivet | Ja |
Bibliografisk note
Funding Information:
This research was supported by an NSERC postdoctoral fellowship (KB), University of California Berkeley VCR-BiGCB, and the Gordon and Betty Moore Foundation (GBMF2983). TL was supported in part by the NIH Genomics Training Grant (Grant T32HG000047-13). Fieldwork was supported by grants from the Yosemite Conservancy, the National Park Service Inventory and Monitoring Program, the National Geographic Society (Grant 8190-07), and the National Science Foundation (DEB 0640859). Additional instrumentation, laboratory, and computational support was provided by the University of Montana Genomics Core, supported by a grant from the M. J. Murdock Charitable Trust, the Vincent J. Coates Genomics Sequencing Laboratory at UC Berkeley, supported by NIH S10 Instrumentation Grants S10RR029668 and S10RR027303, and the Texas Advanced Computing Center (TACC) at the University of Texas at Austin. Grants from the Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD073439; JMG) and the National Institute of General Medical Sciences (R01GM098536; JMG) supported the development of experimental protocols for exome capture in mice that were utilized in the current study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors would like to thank Chris Conroy, Eileen Lacey, Karen Rowe, Kevin Rowe, and Jack Sullivan for providing access to samples, A.-P. Assis, L. Chow, P. Moore, and C. Patton for and field assistance, Sara Keeble for lab support at the University of Montana, Tali Hammond for identification of candidate genes, and Maria Santos for assistance with maps. We thank the Evolutionary Genetics Lab (EGL) and its manager, Lydia Smith, for providing help and support throughout this study and members of the University of Montana UNVEIL network for helpful discussion.
Publisher Copyright:
© 2019 Bi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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