Adaptive introgression underlies polymorphic seasonal camouflage in snowshoe hares

  • Matthew R. Jones
  • , L. Scott Mills
  • , Paulo Célio Alves
  • , Colin M. Callahan
  • , Joel M. Alves
  • , Diana J.R. Lafferty
  • , Francis M. Jiggins
  • , Jeffrey D. Jensen
  • , José Melo-Ferreira
  • , Jeffrey M. Good

Research output: Contribution to journalArticlepeer-review

220 Scopus citations

Abstract

Snowshoe hares (Lepus americanus) maintain seasonal camouflage by molting to a white winter coat, but some hares remain brown during the winter in regions with low snow cover. We show that cis-regulatory variation controlling seasonal expression of the Agouti gene underlies this adaptive winter camouflage polymorphism. Genetic variation at Agouti clustered by winter coat color across multiple hare and jackrabbit species, revealing a history of recurrent interspecific gene flow. Brown winter coats in snowshoe hares likely originated from an introgressed black-tailed jackrabbit allele that has swept to high frequency in mild winter environments. These discoveries show that introgression of genetic variants that underlie key ecological traits can seed past and ongoing adaptation to rapidly changing environments.

Original languageEnglish
Pages (from-to)1355-1358
Number of pages4
JournalScience
Volume360
Issue number6395
DOIs
StatePublished - Jun 22 2018

Funding

We thank E. Cheng, K. Garrison, and P. Zevit for assistance with sample collection. We thank R. Bracewell, T. Brekke, M. Carneiro, Z. Clare-Salzler, M. Dean, E. Kopania, M. S. Ferreira, N. Herrera, E. Larson, M. Nachman, B. Payseur, B. Sarver, and members of the NSF EPSCoR UNVEIL network for helpful discussion. R. Bracewell, B. Cole, T. Cosart, L. Farelo, E. Larson, S. Laurent, T. Max, S. Pfeifer, B. Sarver, and K. Zarn provided computational or laboratory support. A. Kumar assisted with the preparation of Fig. 1. Sequencing was performed at the University of Montana Genomics Core (supported by a grant from the M. J. Murdock Charitable Trust), the CIBIO-InBIO University of Porto New-Gen sequencing platform, the University of Oregon Genomics and Cell Characterization Core Facility, the HudsonAlpha Institute for Biotechnology, and Novogene Technology Co., Ltd. Computational resources were provided by the University of Montana Genomics Core and the Vital-IT Center for high-performance computing of the SIB Swiss Institute of Bioinformatics. This work was funded by a National Science Foundation (NSF) Graduate Research Fellowship (DGE-1313190), a NSF Doctoral Dissertation Improvement Grant (DEB-1702043), NSF Graduate Research Opportunities Worldwide, Portuguese Fundação para a Ciência e a Tecnologia (FCT) project grant “CHANGE” (PTDC/BIA-EVF/1624/ 2014, supported by National Funds), NSF EPSCoR (OIA-1736249), NSF (DEB-1743871), a FCT Investigator Grant (IF/00033/2014, supported by POPH-QREN funds from ESF and Portuguese MCTES/FCT), FLAD (Luso-American Development Foundation; Portugal–U.S. Research Networks Program), the Drollinger-Dial Foundation, an American Society of Mammalogists Grant-in-Aid of Research, a Swiss Government Excellence Scholarship, and European Union’s Seventh Framework Programme (CIBIO New-Gen sequencing platform; grant agreement 286431).

FundersFunder number
HudsonAlpha Institute for Biotechnology
1702043, 0841884, 286431, 1313190, DEB-1702043, 1736249, DGE-1313190
OIA-1736249
IF/00033/2014
PTDC/BIA-EVF/1624/ 2014
DEB-1743871
Swiss Institute of Bioinformatics

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