Sequential introgression of a carotenoid processing gene underlies sexual ornament diversity in a genus of manakins
In a hybrid zone between two tropical lekking birds, yellow male plumage of one species has introgressed asymmetrically replacing white plumage of another via sexual selection. Here, we present a detailed analysis of the plumage trait to uncover its physical and genetic bases and trace its evolutionary history. We determine that the carotenoid lutein underlies the yellow phenotype and describe microstructural feather features likely to enhance color appearance. These same features reduce predicted water shedding capacity of feathers, a potential liability in the tropics. Through genome-scale DNA sequencing of hybrids and each species in the genus, we identify <i>BCO2</i> as the major gene responsible for the color polymorphism. The <i>BCO2</i> gene tree and genome-wide allele frequency patterns suggest that carotenoid-pigmented collars initially arose in a third species and reached the hybrid zone through historical gene flow. Complex interplay between sexual selection and hybridization has thus shaped phenotypes of these species, where conspicuous sexual traits are key to male reproductive success.
Authors
- Sarah E. Kingston (ORCID: https://orcid.org/0000-0003-1607-1789)
- Jeffrey D. Brawn (ORCID: https://orcid.org/0000-0002-5158-0055)
- Michael J. Braun (ORCID: https://orcid.org/0000-0001-8844-1756)
- Haw Chuan Lim (ORCID: https://orcid.org/0000-0002-6420-1667)
- Christopher N. Balakrishnan (ORCID: https://orcid.org/0000-0002-0788-0659)
- Kira M. Long (ORCID: https://orcid.org/0000-0002-7614-3388)
- Matthew J. Powers (ORCID: https://orcid.org/0000-0003-3499-0877)
- Willow R. Lindsay (ORCID: https://orcid.org/0000-0001-8581-2558)
- Peri E. Bolton (ORCID: https://orcid.org/0000-0002-2057-1973)
- Geoffrey E. Hill (ORCID: https://orcid.org/0000-0001-8864-6495)
- Nicholas M. Justyn (ORCID: https://orcid.org/0000-0002-6561-9889)
- James B. Pease (ORCID: https://orcid.org/0000-0003-0125-9156)
- Matthew J. Fuxjager (ORCID: https://orcid.org/0000-0003-0591-6854)
- Thomas J. Parsons (ORCID: https://orcid.org/0000-0001-8715-2231)
- Kevin F. P. Bennett (ORCID: https://orcid.org/0000-0002-4037-9399)
- Lainy B. Day (ORCID: https://orcid.org/0000-0002-9122-3044)
Institutions
- Smithsonian Institution (US)
- U.S. National Science Foundation (US)
- Illinois Department of Natural Resources (US)
- National Museum of Natural History (US)
- University of Illinois Urbana-Champaign (US)
- George Mason University (US)
- East Carolina University (US)
- Brown University (US)
- Smithsonian Conservation Biology Institute (US)
- University of Mississippi (US)
- Wake Forest University (US)
- Sea Education Association (US)
- University of Maryland, College Park (US)
- Auburn University (US)
Publication Details
- Journal
- Science Advances
- Published
- 2024-11-20
- DOI
- https://doi.org/10.1126/sciadv.adn8339
- Citations
- 11
- Primary Topic
- Animal Behavior and Reproduction
- Type
- article
- Field-Weighted Citation Impact
- 11.32
Funders
- National Science Foundation
- Smithsonian Institution
- U.S. Department of Agriculture
- Drexel University
- Louisiana State University
- Academy of Natural Sciences of Drexel University
- National Institute of Food and Agriculture
- National Museum of Natural History