Genetic architecture and evolution of color variation in American black bears

Emily E Puckett; Isis S Davis; Dawn C Harper; Kazumasa Wakamatsu; Gopal Battu; Jerrold L Belant; Dean E Beyer Jr; Colin Carpenter; Anthony P Crupi; Maria Davidson; Christopher S DePerno; Nicholas Forman; Nicholas L Fowler; David L Garshelis; Nicholas Gould; Kerry Gunther; Mark Haroldson; Shosuke Ito; David Kocka; Carl Lackey; Ryan Leahy; Caitlin Lee-Roney; Tania Lewis; Ashley Lutto; Kelly McGowan; Colleen Olfenbuttel; Mike Orlando; Alexander Platt; Matthew D Pollard; Megan Ramaker; Heather Reich; Jaime L Sajecki; Stephanie K Sell; Jennifer Strules; Seth Thompson; Frank van Manen; Craig Whitman; Ryan Williamson; Frederic Winslow; Christopher B Kaelin; Michael S Marks; Gregory S Barsh

doi:10.1016/j.cub.2022.11.042

Genetic architecture and evolution of color variation in American black bears

Curr Biol. 2023 Jan 9;33(1):86-97.e10. doi: 10.1016/j.cub.2022.11.042. Epub 2022 Dec 16.

Authors

Emily E Puckett¹, Isis S Davis², Dawn C Harper³, Kazumasa Wakamatsu⁴, Gopal Battu⁵, Jerrold L Belant⁶, Dean E Beyer Jr⁶, Colin Carpenter⁷, Anthony P Crupi⁸, Maria Davidson⁹, Christopher S DePerno¹⁰, Nicholas Forman¹¹, Nicholas L Fowler⁸, David L Garshelis¹², Nicholas Gould¹⁰, Kerry Gunther¹³, Mark Haroldson¹⁴, Shosuke Ito⁴, David Kocka¹⁵, Carl Lackey¹⁶, Ryan Leahy¹⁷, Caitlin Lee-Roney¹⁷, Tania Lewis¹⁸, Ashley Lutto¹⁹, Kelly McGowan²⁰, Colleen Olfenbuttel²¹, Mike Orlando²², Alexander Platt²³, Matthew D Pollard², Megan Ramaker⁵, Heather Reich¹⁶, Jaime L Sajecki¹⁵, Stephanie K Sell⁸, Jennifer Strules¹⁰, Seth Thompson¹⁵, Frank van Manen¹⁴, Craig Whitman¹⁴, Ryan Williamson²⁴, Frederic Winslow¹¹, Christopher B Kaelin²⁰, Michael S Marks²⁵, Gregory S Barsh²⁶

Affiliations

¹ Department of Biological Sciences, University of Memphis, Memphis, TN 38152, USA. Electronic address: emily.puckett@memphis.edu.
² Department of Biological Sciences, University of Memphis, Memphis, TN 38152, USA.
³ Department of Pathology and Laboratory Medicine, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA.
⁴ Institute for Melanin Chemistry, Fujita Health University, Toyoake, Japan.
⁵ HudsonAlpha Institute for Biotechnology, Huntsville, AL 35806, USA.
⁶ Department of Fisheries and Wildlife, Michigan State University, East Lansing, MI 48824, USA.
⁷ West Virginia Division of Natural Resources, Beckley, WV 25801, USA.
⁸ Division of Wildlife Conservation, Alaska Department of Fish and Game, Douglas, Juneau, AK 99824, USA.
⁹ The Louisiana Department of Wildlife and Fisheries, Baton Rouge, LA 70898, USA.
¹⁰ Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695-7646, USA.
¹¹ New Mexico Department of Game and Fish, Santa Fe, NM 87507, USA.
¹² Minnesota Department of Natural Resources, Grand Rapids, MN 55744, USA; IUCN SSC Bear Specialist Group.
¹³ National Park Service, Yellowstone National Park, WY 82190-0168, USA.
¹⁴ U.S. Geological Survey, Northern Rocky Mountain Science Center, Interagency Grizzly Bear Study Team, Bozeman, MT 59715, USA.
¹⁵ Virginia Department of Wildlife Resources, Verona, VA 24482, USA.
¹⁶ Nevada Department of Wildlife, Reno, NV 89512, USA.
¹⁷ National Park Service, Yosemite National Park Wildlife Management, Yosemite, CA 95389, USA.
¹⁸ National Park Service, Glacier Bay National Park, Gustavus, AK 99826, USA.
¹⁹ U.S. Fish and Wildlife Service, Kenai National Wildlife Refuge, Soldotna, AK 99669, USA.
²⁰ Department of Genetics, School of Medicine, Stanford University, Stanford, CA 94305, USA.
²¹ North Carolina Wildlife Resources Commission, Raleigh, NC 27699, USA.
²² Florida Fish and Wildlife Conservation Commission, Tallahassee, FL 32399, USA.
²³ Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
²⁴ National Park Service, Great Smoky Mountains National Park, Gatlinburg, TN 37738, USA.
²⁵ Department of Pathology and Laboratory Medicine, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA; Departments of Pathology and Laboratory Medicine and of Physiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
²⁶ HudsonAlpha Institute for Biotechnology, Huntsville, AL 35806, USA; Department of Genetics, School of Medicine, Stanford University, Stanford, CA 94305, USA.

Abstract

Color variation is a frequent evolutionary substrate for camouflage in small mammals, but the underlying genetics and evolutionary forces that drive color variation in natural populations of large mammals are mostly unexplained. The American black bear, Ursus americanus (U. americanus), exhibits a range of colors including the cinnamon morph, which has a similar color to the brown bear, U. arctos, and is found at high frequency in the American southwest. Reflectance and chemical melanin measurements showed little distinction between U. arctos and cinnamon U. americanus individuals. We used a genome-wide association for hair color as a quantitative trait in 151 U. americanus individuals and identified a single major locus (p < 10^-13). Additional genomic and functional studies identified a missense alteration (R153C) in Tyrosinase-related protein 1 (TYRP1) that likely affects binding of the zinc cofactor, impairs protein localization, and results in decreased pigment production. Population genetic analyses and demographic modeling indicated that the R153C variant arose 9.36 kya in a southwestern population where it likely provided a selective advantage, spreading both northwards and eastwards by gene flow. A different TYRP1 allele, R114C, contributes to the characteristic brown color of U. arctos but is not fixed across the range.

Keywords: GWAS; OCA3; TYRP1; functional phylogeography; melan-b; migration.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Gene Flow
Genetic Variation
Genome
Genome-Wide Association Study
Ursidae* / genetics

Abstract

Publication types

MeSH terms

Grants and funding