Carotenoid Coloration & Color Genetics
Carotenoid pigmentation presents a fascinating research topic. Any consideration of ornamental plumage coloration begins with the fundamental question that Darwin and Wallace pondered for decades: why do small birds, subject to predation, put colorful and conspicuous pigments in their feathers? The question gets even more interesting when one considers that carotenoid pigments cannot be synthesized by birds or other vertebrates; they have to be ingested and moved to the tissue to be pigmented. Furthermore, most birds eat only yellow pigments and to produce red pigments they have to modify ingested carotenoids from yellow to red. The complexities of this signaling system make it a fascinating focus for study. Expression of carotenoid coloration by House Finches and other animals is dependent on condition, and exploring the links between ornamentation, condition, and performance is a major focus of my lab group.
For the first twenty years of my career, my students and I worked on the basic patterns of mate choice and color production. In recent years, the focus has shifted to the genetic and cellular mechanisms that control production of red feather pigmentation. New discoveries in cell biology, particularly related to vitamin A physiology and biochemistry of redox pathways, along with the fantastic new genetic tools now available, are allowing for fundamentally better understanding of the mechanisms involved with carotenoid pigmentation and how, in a biochemical sense, carotenoid pigmentation serves as a signal of individual quality. In 2016, in collaboration with the Carniero lab at the Univ. of Porto in Portugal and the Corbo lab at Wash U. St. Louis, we discovered the ketolase that allows birds to convert yellow dietary carotenoids to red carotenoids used for ornamental feather coloration. This ketolase, CYP2J19, is a cytochrome P450. More recently this research team identified the genetic basis for sexual dichromatism in canaries and other cardeuline finches. That study landed on the cover of Science in 2020. We also discovered the genetic basis for novel red bill coloration in canaries.
In 2017, a study led by Matt Toomey in the Corbo lab at Wash U and Carneiro at Porto, discovered the primary gene responsible for uptake of carotenoids across the gut lining: SCARB1. Up and down regulation of SCARB1 likely plays a key role in expression of ornamental carotenoid coloration. Understanding how CYP2J19 and SCARB1 operate in the cells of birds to produce red coloration will provide unprecedented insights into how red carotenoid pigmentation serves as a signal of condition in birds and other vertebrates.
In 2019, the Hill lab teamed with the Wendy Hood and Andreas Kavazis labs to conduct a breakthrough study on the mechanisms that link carotenoid coloration to condition. We first showed that red ketolated carotenoids are not just associated with the liver mitochondria of molting male house finches, they are concentrated in the inner mitochondrial membrane. This observation is of huge significance to studies of condition dependent signaling via carotenoid coloration because it strongly suggests that ketolation occurs in the inner mitochondrial membrane in close association with the electron transport system. In 2021, with Hill doctoral student Matt Powers as lead author and in collaboration with the Ron Burton lab, we published evidence that production of red carotenoid coloration is also tied to mitochondrial function in a marine copepod. Taken together, these observations suggest that red coloration is an honest signal of male performance because it serves as an honest signal of mitochondrial function. Following up on these observations is central focus of the Hill lab going into 2022.
Key recent citations related to carotenoid coloration from the Hill Lab:
Powers, M. Weaver, R. J., Barreto, F. S., Burton, R. S., and Hill G E. 2021. Evidence for hybrid breakdown in production of red carotenoids in the marine invertebrate Tigriopus californicus. PLoS One 16(11), e0259371.
Koch, R.E., Buchanan, K.L., Casagrande, S., Crino, O., Dowling, D.K., Hill, G.E., Hood, W.R., McKenzie, M., Mariette, M.M., Noble, D.W. and Pavlova, A. 2021. Integrating Mitochondrial Aerobic Metabolism into Ecology and Evolution. Trends in Ecology and Evolution 36: 321-332.
Gazda, M.A., Araújo, P.M., Lopes, R.J., Toomey, M.B., Andrade, P., Afonso, S., Marques, C., Nunes, L., Pereira, P., Trigo, S., Hill, G.E, Corbo, J. Carneiro, M. 2020. A genetic mechanism for sexual dichromatism in birds. Science, 368(6496), pp.1270-1274.
Gazda, M. A., Toomey, M. B., P. M. Araújo, R. J. Lopes, S. Afonso, C. A. Meyers, K. Serress, P. D. Kiser, G. E. Hill, J. C. Corbo and M. Carneiro. 2020. Genetic Basis of De Novo Appearance of Carotenoid Ornamentation in Bare-Parts of Canaries. Molecular Ecology and Evolution 37: 1317–1328.
Powers, M. J., Hill, G. E., and Weaver, R. J. 2019. An experimental test of mate choice for red carotenoid coloration in the marine copepod, Tigriopus Californicus. Ethology DOI: 10.1111/eth.12976.
Hill, G.E., Hood, W.R., Ge, Z., Grinter, R., Greening, C., Johnson, J.D., Park, N.R., Taylor, H.A., Andreasen, V.A., Powers, M.J., Justyn, N.M. and Zhang, Y, 2019. Plumage redness signals mitochondrial function in the House Finch. Proceedings Royal Society of London B. 286: 20191354.
Koch, R. E and G. E. Hill. 2019. Loss of carotenoid plumage coloration is associated with loss of choice for plumage coloration in domestic canaries. Frontiers in Ecology and Evolution 7:106.
Koch, R.E., M. Staley, A. N. Kavazis, D. Hasselquist, M. B. Toomey, and G.E. Hill. 2019. Testing the resource tradeoff hypothesis for carotenoid-based signal honesty using genetic variants of the domestic canary. J. Experimental Biology 222(6).
Koch, R.E. A. N. Kavazis, D. Hasselquist, W. R. Hood, Y. Zhang, and G.E. Hill. 2018. No evidence that carotenoid pigments boost either immune or antioxidant defenses in a songbird. Nature Communications 9:491.
Weaver, R. J., P. Wang, G. E. Hill, P. A. Cobine. 2018. An in vivo test of the biologically relevant roles of carotenoids as antioxidants in animals. J. Experimental Biology 221: jeb183665.
Koch, R.E. and G.E. Hill. 2018. Do carotenoid-based ornaments entail resource tradeoffs? An evaluation of theory and data. Functional Ecology.
Weaver, R.J., Santos, E.S., Tucker, A.M., Wilson, A.E. and Hill, G.E., 2018. Carotenoid metabolism strengthens the link between feather coloration and individual quality. Nature communications, 9(1), p.73.
Matthew B. Toomey, Ricardo J. Lopes, Pedro M. Araújo, James D. Johnson, Małgorzata A. Gazda, Sandra Afonso, Paulo G. Mota, Rebecca E. Koch, Geoffrey E. Hill, Joseph C. Corbo, and Miguel Carneiro
High-density lipoprotein receptor SCARB1 is required for carotenoid coloration in birds
PNAS 2017 : 1700751114v1-201700751.
Weaver, R. J., Hill G E., Kuan P L, and Tseng,Y-C. 2016. Copper exposure reduces production of red carotenoids in a marine copepod. Environmental Indicators 70:393-400.
Lopes, R. L., J. D. Johnson, M. B. B Toomey, S. M. Ferreira, J. Melo-Ferreira, L. Andersson, G. E. Hill*, J. C. Corbo*, and M. C. Carneiro*. 2016. The redness gene in birds. Current Biology *co-corresponding authors.
Koch, R.E., G.E. Hill, and K.J. McGraw. 2016. Precursor and product carotenoid pigments in yellow and red factor canaries (Serinus canaria) The Wilson Journal of Ornithology.
Koch, R. E., Wilson, A. and G. E. Hill. 2016. The importance of carotenoid dose in supplementation studies with songbirds. Physiological and Biochemical Zoology 89(1):61–71.
Koch R. and Hill, G. E. 2015. Rapid evolution of bright monochromatism in the domestic Atlantic Canary (Serinus canaria). Wilson Journal of Ornithology 127(4):615-621.
Ge, R., Johnson, J.D., P. A. Cobine, K. J. McGraw, R. Garcia, G. E. Hill. 2015. High concentrations of keto-carotenoids found in the Hepatic Mitochondrial fraction of a molting red songbird. Physiological and Biochemical Zoology 88.4 (2015): 444-450.
Balenger S. L. Bonneaud, C., Sefick, S., Edwards, S. V., Hill, G. E. 2015. Plumage color and pathogen-induced gene expression in a wild songbird. Behavioral Ecology 26(4), 1100–1110. doi:10.1093/beheco/arv055
Mateos-Gonzalez, F., Hill, G. E., & Hood, W. R. (2014). Carotenoid coloration predicts escape performance in the House Finch (Haemorhous mexicanus). Auk 131(3): 275-281.
Hill, G. E. 2014. Cellular Respiration: The Nexus of Stress, Condition, and Ornamentation. Integrative and Comparative Biology 54:645-657.
McGraw, K. J., Giraudeau, M., Hill, G. E., Toomey, M. B., & Staley, M. (2013). Ketocarotenoid circulation, but not retinal carotenoid accumulation, is linked to eye disease status in a wild songbird. Archives of Biochemistry and Biophysics. 539(2): 156-162.
Johnson J.D. and G.E. Hill. 2013. Is carotenoid ornamentation linked to the inner mitochondria membrane potential? A hypothesis for the maintenance of signal honesty. Biochimie 95:436–444.
Hill, G. E. and J. D. Johnson. 2012. The Vitamin A-Redox Hypothesis: A Biochemical Basis for Honest Signaling via Carotenoid Pigmentation. American Naturalist. 2012. Vol. 180, pp. E127–E150
Hill, G. E. 2011. Condition-dependent traits as signals of the functionality of vital cellular processes. Ecology Letters 14: 625-634.
Huggins, K., K.J. Navara, G.E. Hill, and M.T. Mendonça. 2010. Detrimental effects of carotenoid pigments: the dark side of bright coloration. Naturwissenschaften 97:637644.
Hill, G. E., W.R. Hood, and K. Huggins. 2009. A multifactorial test of the effects of carotenoid access, food intake, and parasite load on production of ornamental feather and bill coloration in American Goldfinches. J. Experimental Biology 212:1225-1233.
Shawkey, M. D., G. E. Hill, K.J. McGraw, W. R. Hood, and K. Huggins. 2006. An experimental test of the contributions and condition dependence of microstructure and carotenoids in yellow plumage colouration. Proceedings of Royal Society, Lond. Series B 273:2985-2991.
Navara, K.J., G.E. Hill, and M.T. Mendonça. 2006. Yolk androgen deposition as a compensatory strategy. Behavioral Ecology and Sociobiology 60: 392-398.
Shawkey, M. D., and G. E. Hill. 2005. Carotenoids need nanostructures to shine. Biology Letters 1:121-124. PDF
Hill, G. E., and K.L. Farmer. 2005. Carotenoid-based plumage coloration predicts resistance to a novel parasite in the house finch. Naturwissenschaften 92: 30-34.