Abstract
Evolution of diet-derived sexual ornaments—some of the most spectacular and diverse traits in the living world—highlights the gap between modern evolutionary theory and empirical data on the origin and inheritance of complex environment-dependent traits. Specifically, current theory offers little insight into how strong environmental contingency of diet-dependent color biosynthesis and environmental variability in precursor supply can be reconciled with extensive evolutionary elaboration, diversification, and convergence of diet-dependent displays among animal taxa. Moreover, biosynthetic pathways of diet-derived displays combine seemingly irreconcilable robustness, lability, and modularity to facilitate elaboration under variable environmental conditions. Here I show that an ontogenetic decrease in the predictability of an association between organismal and environmental components of color biosynthesis and the corresponding evolutionary transition from short-term epigenetic inheritance of peripheral biosynthetic components to genetic inheritance of the most reliable upstream components link the causes of developmental variation with the causes of inheritance in diet-derived displays. Using carotenoid-based colors as an empirical model, I outline general principles of a testable evolutionary framework of diversification and functional robustness of diet-derived displays, and suggest that such a framework provides insight into the foundational question of evolutionary biology—how to connect causes of within-generation developmental variation with causes of among-generation and among-taxa variation and thus with causes of evolution?
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Aharoni, A., Gaidukov, L., Khersonsky, O., McQ Gould, S., Roodveldt, C., & Tawfik, D. S. (2005). The ‘evolvability’ of promiscuous protein functions. Nature Genetics, 37, 73–76.
Alberch, P. (1991). From genes to phenotype: Dynamical systems and evolvability. Genetica, 84, 5–11.
Arnold, F. H., Wintrode, P. C., Miaazaki, K., & Gershenson, A. (2001). How enzymes adapt: Lessons from directed evolution. Trends in Biochemical Sciences, 26, 100–106.
Baatz, M., & Wagner, G. P. (1997). Adaptive inertia caused by hidden pleiotropic effects. Theoretical Population Biology, 51, 49–66.
Badyaev, A. V. (2004a). Developmental perspective on the evolution of sexual displays. Evolutionary Ecology Research, 6, 975–991.
Badyaev, A. V. (2004b). Integration and modularity in the evolution of sexual ornaments: An overlooked perspective. In M. Pigliucci, & K. Preston (Eds.), Phenotypic integration: The evolutionary biology of complex phenotypes (pp. 50–79). Oxford: Oxford University Press.
Badyaev, A. V. (2005a). Colorful phenotypes of colorless genotypes: Towards a new evolutionary synthesis of animal color displays. In G. E. Hill, & K. J. McGraw (Eds.), Bird coloration: Function and evolution (pp. 349–379). Cambridge: Harvard Univ. Press.
Badyaev, A. V. (2005b). Stress-induced variation in evolution: from behavioral plasticity to genetic assimilation. Proceedings of Royal Society London: Biological Sciences, 272, 877–886.
Badyaev, A. V., & Duckworth, R. A. (2003). Context-dependent sexual advertisement: Plasticity in development of sexual ornamentation throughout the lifetime of a passerine bird. Journal of Evolutionary Biology, 16, 1065–1076.
Badyaev, A. V., & Foresman, K. R. (2004). Evolution of morphological integration: I. Functional units channel stress-induced variation in shrew mandibles. American Naturalist, 163, 868–879.
Badyaev, A. V., & Hill, G. E. (2003). Avian sexual dichromatism in relation to ecology and phylogeny. Annual Review of Ecology and Systematics, 34, 27–49.
Badyaev, A. V., & Landeen, E. A. (2007). Developmental evolution of sexual ornamentation: Model and a test of feather growth and pigmentation. Integrative and Comparative Biology (in press).
Badyaev, A. V., & Qvarnström, A. (2002). Putting sexual traits into the context of an organism: A life-history perspective in studies of sexual selection. Auk, 119, 301–310.
Badyaev, A. V., & Vleck, C. M. (2007). Context-dependent ontogeny of sexual ornamentation: Implications for a trade-off between current and future breeding efforts. Journal of Evolutionary Biology (in press).
Badyaev, A. V., & Young, R. L. (2004). Complexity and integration in sexual ornamentation: An example with carotenoid and melanin plumage pigmentation. Journal of Evolutionary Biology 17, 1317–1327.
Baker, M. C., & Baker, E. M. (1990). Reproductive behavior of female buntings: Isolating mechanisms in a hybridizing pair of species. Evolution, 44, 332–338.
Bitgood, J. J., & Somes, R. G. J. (2003). Linkage relationships and gene mapping. In: R. D. Crawford (Ed.), Poultry breeding and genetics (pp. 469–496). Amsterdam: Elsevier.
Blanco, G., Frias, O., Garrido-Fernandez, J., & Hornero-Mendez, D. (2005). Environmental-induced acquisition of nuptial plumage expression: A role of denaturation of feather carotenoproteins? Proceedings of the Royal Society B, 272, 1893–1900.
Bleiweiss, R. (2004). Novel chromatic and structural biomarkers of diet in carotenoid-bearing plumage. Proceedings of the Royal Society B, 271, 2327–2335.
Blount, J. D., Metcalfe, N. B., Birkhead, T. R., & Surai, P. F. (2003). Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science, 300, 125–128.
Britton, G. (1998). Overview of carotenoid biosynthesis. In G. Britton, H. Pfander, & S. Liaaen-Jensen (Eds.), Carotenoids: Biosynthesis and metabolism (pp. 13–147). Basel: Birkhäuser.
Brockmann, H., Völker, O. (1934). Der Gelbe Federfarbstoff des Kanarievogels (Serius canaria) und das Volkommen von Carotinoided bei Vögeln. Hoppe-Zeyler’s Zeitschrift für, 224, V.
Brush, A. H. (1967). Pigmentation in the scarlet tanager, Piranga olivacea. Condor, 69, 549–559.
Brush, A. H. (1978). Avian pigmentation. In A. H. Brush (Ed.), Chemical zoology (pp. 141–161). New York: Academic Press.
Brush, A. H. (1990). Metabolism of carotenoid pigments in birds. FASEB, 4, 2969–2977.
Caropale, L. H. (1999). Chance favors the prepared genome. Annals New York Academy of Sciences, 870, 1–21.
Carroll, S. B. (2005). Evolution at two levels: On genes and form. PLoS Biology, 3, e245.
Carroll, S. B., Grenier, J. K., & Weatherbee, S. D. (2001). From DNA to diversity molecular genetics and the evolution of animal design. Blackwell Science, p. 162.
Cate, C. T., & Bateson, P. (1988). Sexual selection: The evolution of conspicuous characteristics in birds by means of imprinting. Evolution, 42, 1355–1358.
Chetverikov, S. S. (1926). On certain aspects of the evolutionary process from the standpoint of modern genetics. Journal of Experimental Biology Series A, 2, 1–40.
Craig, J. K., & Foote, C. J. (2001). Countergradient variation and secondary sexual color: Phenotypic convergence promotes genetic divergence in carotenoid use between sympatric anadromous and nonanadromus morphs of sockeye salmon. Evolution, 55, 380–391.
Cushing, J. E. Jr. (1941). Non-genetic mating preferences as a factor in evolution. Condor, 43, 233–236.
Davidson, E. H. (2006). The regulatory genome: Gene regulatory networks in development and evolution. Academic Press, p. 304.
Desselberger, H. (1930). Ueber das Lipochrom der Vogelfeder. Journal fur Ornithologie, 78, 328–376.
Firn, R. D., & Jones, C. G. (1996). An explanation of secondary product “redundancy”. In J. T. Romeo, J. A. Saunders, & P. Barbosa (Eds.), Phytochemical diversity and redundancy in ecological interactions (pp. 295–312). New York: Plenum Press.
Fitze, P. S., Tschirren, B., & Richner, H. (2003). Carotenoid-based colour expression is determined early in nestling life. Oecologia, 137, 148–152.
Fox, D. L., Smith, V. E., & Wolfson, A. A. (1969). Carotenoid selectivity in blood and feathers of lesser (Africa) Chilean and Greater (European) flamingos. Comparative Biochemistry and Physiology, 23, 225–232.
Fraser, P. D., Shimada, H., & Misawa, N. (1998). Enzymic confirmation of reactions involved in routes to astaxanthin formation, elucidated using a direct in vitro assay. European Journal of Biochemistry, 252, 229–236.
Gilbert, S. F. (2001). Ecological developmental biology: Developmental biology meets the real world. Developmental Biology, 233, 1–12.
Gilbert, S. F. (2005). Mechanisms for the environmental regulation of gene expression: Ecological aspects of animal development. Journal of Bioscience, 30, 64–74.
Gluckman, P. D., Hanson, M. A., & Beedle, A. S. (2007). Early life events and their consequences for later disease: A life history and evolutionary perspective. American Journal of Physical Anthropology, 19, 1–19.
Goodwin, T. W. (1952). Comparative biochemistry of carotenoids. London: Chapman and Hall.
Griswold, C. K. (2006). Pleiotropic mutation, modularity and evolvability. Evolution and Development, 8, 81–93.
Hadfield, J. D., & Owens, I. P. F. (2006). Strong environmental determination of a carotenoid-based plumage trait is not mediated by carotenoid availability. Journal of Evolutionary Biology, 19, 1104–1114.
Hill, G. E. (2003). A red bird in a brown bag: The function and evolution of colorful plumage in the house finch. Oxford Ornithology Series.
Hill, G. E., & Benkman, C. W. (1995). Exceptional response to dietary carotenoid supplementation by female Red Crossbills. Wilson Bulletin, 107, 620–621.
Hoekstra, H. E. (2006). Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity, 97, 222–234.
Hudon, J. (1991). Unusual carotenoid use by western tanager (Piranga ludoviviana) and its evolutionary implications. Canadian Journal of Zoology, 69, 2311–2320.
Hudon, J., & Brush, A. H. (1989). Probably dietary basis of a color variant of the cedar waxwing. Journal of Field Ornithology, 60, 361–368.
Huxley, J. S. (1942). Evolution: The modern synthesis. Allen and Unwin.
Inouye, C. Y., Hill, G. E., Stradi, R. D., & Montgomerie, R. (2001). Carotenoid pigments in male house finch plumage in relation to age, subspecies, and ornamental coloration. Auk, 118, 900–915.
Jablonka, E. (2001). The systems of inheritance. In S. Oyama, P. E. Griffiths, & R. D. Gray (Eds.), Cycles of contingency: Developmental systems and evolution (pp. 99–116). Cambridge: MIT Press.
Karadas, F., Pappas, A. C., Surai, P. F., Speake, B. K. (2005). Embryonic development with carotenoid-enriched eggs influences the post-hatch carotenoid status of the chicken. Comparative Biochemistry and Physiology B, 141, 244–251.
Kimball, R. T., Ligon, J. D. (1999). Evolution of avian plumage dichromatism from a proximate perspective. American Naturalist, 154, 182–193.
Koutsos, E. A., Clifford, A. J., Calvert, C. C., & Klasing, K. C. (2003). Maternal carotenoid status modifies the incorporation of dietary carotenoids into immune tissues of growing chickens (Gallus gallus domesticus). Journal of Nutrition, 133, 1132–1138.
Kritzler, H. (1943). Carotenoids in the display and eclipse plumage of bishop birds. Physiological Zoology, 16, 241–245.
Lee, P. C., & Schmidt-Dannert, C. (2002). Metabolic engineering towards biotechnological production of carotenoids in microorganisms. Applied Microbiology and Biotechnology, 60, 1–11.
Lewontin, R. C. (1974). The genetic basis of evolutionary change. New York: Columbia University Press.
Lewontin, R. C. (1983). Gene, organism and environment. In D. S. Bendall (Ed.), Evolution: From molecules to men (pp. 273–285). Cambridge: Cambridge University Press.
Linville, S. U., & Breitwisch, R. (1997). Carotenoid availability and plumage coloration in a wild population of Northern Cardinals. Auk, 114, 796–800.
Lucas, A. M., & Stettenheim, P. R. (1972). Avian anatomy: Integument. USDA.
Mayr, E. (1963). Animal species and evolution. Cambridge: Harvard University Press.
Majerus, M. N., & Mundy, N. (2003). Mammalian melanism: Natural selection in black and white. Trends in Ecology and Evolution, 19, 585–588.
McGraw, K. J. (2004). Colourful songbirds metabolize carotenoids at the integument. Journal of Avian Biology, 35, 471–476.
McGraw, K. J. (2006). The mechanics of carotenoid coloration in birds. In: G. E. Hill, & K. J. McGraw (Eds.), Bird coloration. I. Mechanisms and measurements (pp. 177–242). Cambridge, MA: Harvard University Press.
McGraw, K. J., & Hardy, L. (2006). Astaxanthin is responsible for the pink plumage flush of Franklins and Ring-billed gulls. Journal of Field Ornithology, 77, 29–33.
McGraw, K. J., & Parker, R. S. (2006). A novel lipoprotein-mediated mechanism controlling sexual attractiveness in a colorful songbird. Physiology and Behavior, 87, 103–108.
Mijts, B. N., Lee, P. C., & Schmidt-Dannert, C. (2004). Engineering carotenoid biosynthetic pathways. Methods in Enzymology, 388, 315–329.
Minvielle, F., Gourichon, D., & Moussu, C. (2005). Two new plumage mutations in the Japanese quail: “curly” feather and “rusty” plumage. BMC Genetics, 6, 1–5.
Nanjundiah, V. (2003). Phenotypic plasticity and evolution by genetic assimilation. In G. B. Muller, & S Newman (Eds.), Origination of organismal form: Beyond the gene in developmental and evolutionary biology (pp. 245–263). Cambridge: The MIT Press.
Negro, J. J., Tella, J. L., Hiraldo, F., Bortolotti, G. R., & Prieto, P. (2001). Sex- and age-related variation in plasma carotenoids despite a constant diet in the red-legged partridge (Alectoris rufa). Ardea, 89, 275–279.
Olson, S. L. (1970). Specializations of some carotenoid-bearing feathers. Condor, 72, 424–430.
Omland, K. E., & Hofmann, C. M. (2005). Adding color to the past: Ancestral-state reconsrtuction of coloration. In G. E. Hill, & K. J. McGraw (Eds.), Bird coloration: Function and evolution (pp. 417–454). Cambridge: Harvard University Press.
Oyama, S. (2000). In B. H. Smith & E. R. Weintraub (Eds.), The ontogeny of information: Developmental systems and evolution. Durham: Duke University Press.
Panov, E. N. (1989). Natural hybridization and ethological isolation in birds. Moscow: Nauka.
Parker, R. S. (1996). Absorption, metabolism, and transport of carotenoids. FASEB Journal, 10, 542–551.
Pigliucci, M., Murren, C. J., & Schlichting, C. D. (2006). Phenotypic plasticity and evolution by genetic assimilation. Journal of Experimental Biology, 209, 2362–2367.
Prum, R. O. (2005). Evolution of the morphological innovations of feathers. Journal of Experimental Zoology (Mol Dev Evol), 304B, 570–579.
Reeves, C. D. (2003). The enzymology of combinatorial biosynthesis. Critical Reviews in Biotechnology, 23, 95–147.
Rice, S. H. (2001). The evolution of developmental interactions: Epistasis, canalization, and integration. In J. B. Wolf, D. I. Brodie Edmund, & M. J. Wade (Eds.), Epistasis and the evolutionary process (pp. 82–98). New York: Oxford University Press.
Schlinger, B. A., Fivizzani, A. J., & Callard, G. V. (1989). Aromatase, 5α- and 5β-reductase in brain, pituitary, and skin of the sex-role reversed Wilson’s phalarope. Journal of Endocrinology, 122, 573–581.
Schmalhausen, I. I. (1949). Factors of evolution. Philadelphia, Pennsylvania: Blakiston.
Schmidt-Dannert, C., Umeno, D., & Arnold, F. H. (2000). Molecular breeding of carotenoid biosynthetic pathways. Nature Biotechnology, 18, 750–753.
Schwab, W. (2003). Metabolome diversity: Too few genes, too many metabolites? Phytochemistry, 62, 837–849.
Slagsvold, T., & Lifjeld, J. T. (1985). Variation in plumage colour of the great tit (Parus major) in relation to habitat, season and food. Journal of Zoology London, 206, 321–328.
Somes, R. G. J. (2003). Mutations and major variants of plumage and skin in chickens. In R. D. Crawford (Ed.) Poultry breeding and genetics (pp. 169–208). Amsterdam: Elsevier.
Stern, D. L. (2000). Evolutionary developmental biology and the problem of variation. Evolution, 54, 1079–1091.
Stradi, R. (1998) The colour of flight: Carotenoids in bird plumage. Milan, Italy: University of Milan Press.
Stradi, R., Pini, E., & Celentano, G. (2001). Carotenoids in bird plumage: The complement of red pigments in the plumage of wild and captive bullfinch (Pyrrhula pyrrhula). Comparative Biochemistry and Physiology B, 128, 529–535.
Stradi, R., Rossi, E., & Bellardi, B. (1996). Carotenoids in bird plumage: - II. The pattern in three Loxia species and in Pinicola enucleator. Comparative Biochemistry and Physiology B, 113, 427–437.
Surai, P. F., Ionov, I. A., Kuklenko, T. V., Kostjuk, I. A., MacPherson, A., Speake, B. K., Noble, R. C., & Sparks, N. H. C. (1998). Effect of supplementing the hen’s diet with vitamin A on the accumulation of vitamins A and E, ascorbic acid and carotenoids in the egg yolk and in the embryonic liver. British Poultry Science, 39, 257–263.
Surai, P. F., & Speake, B. K. (1998). Distribution of carotenoids form the yolk to the tissues of the chick embryo. Journal of Nutritional Biochemistry, 9:645–651.
Tella, J. L., Figuerola, J., Negro, J. J., Blanco, G., Rodríguez-Estrella, R., Forero, M. G., Blázquez, M. C., Green, A. J., & Hiraldo, F. (2004). Ecological, morpholigical and phylogenetic correlates of interspecific variation in plasma carotenoid concentration in birds. Journal of Evolutionary Biology, 17, 156–164.
Test, F. H. (1969). Relation of wing and tail color of the woodpeckers Colaptes auratus and C. cafer to their food. Condor, 71, 206–211.
Tobias, A. V., & Arnold, F. H. (2006). Biosynthesis of novel carotenoid families based on unnatural carbon backbones: A model for diversification of natural product pathways. Biochimica et Biophysica Acta, 1761, 235–246.
Trams, E. G. (1969). Carotenoid transport in the plasma of the scarlet ibis (Eudocimus ruber). Comparative Biochemistry and Physiology, 28, 117–118.
Troy, D. M., & Brush, A. H. (1983). Pigments and feather structure of the redpolls, Carduelis flammea and C. hornemanni. Condor, 85, 443–446.
Tyczkowski, J. K., & Hamilton, P. B. (1986). Evidence for differential absorption of zeacarotene, cryptoxanthuin, and lutein in young broiler chickens. Poultry Science, 65, 1137–1140.
Umeno, D., Tobias, A. V., & Arnold, F. H. (2005). Diversifying carotenoid byosynthetic pathways by directed evolution. Microbiology and Molecular Biology Reviews, 69, 51–78.
Vitkup, D., Kharchenko, P., & Wagner, A. (2006). Influence of metabolic network structure and function on enzyme evolution. Genome Biology, 7, R39.
Wagner, A. (2003). Risk management in biological evolution. Journal of Theoretical Biology, 225, 45–57.
Wagner, A. (2005). Robustness and evolvability in living systems. Princeton, NJ: Princeton University Press.
Wagner, G. P., & Altenberg, L. (1996). Complex adaptation and the evolution of evolvability. Evolution, 50, 967–976.
Wagner, G. P., & Schwenk, K. (2000). Evolutionary stable configurations: Functional integration and the evolution of phenotypic stability. Evolutionary Biology, 31, 155–217.
West-Eberhard, M. J. (2003). Developmental plasticity and evolution. Oxford: Oxford Univ. Press, p. 795.
West -Eberhard, M. J. (2005). Phenotypic accommodation: adaptive innovation due to developmental plasticity. Journal of Experimental Zoology (Mol Dev Evol), 304B, 610–618.
Wilkins, A. S. (2001). The evolution of developmental pathways. Sinauer Associates, p. 603.
Witmer, M. (1996). Consequences of an alien shrub on the plumage coloration and ecology of cedar waxwings. Auk, 113, 735–743.
Young, R. L., & Badyaev, A. V. (2007). Evolution of ontogeny: linking epigenetic remodeling and genetic adaptation in skeletal structures. Integrative and Comparative Biology (in press).
Young, R. L., Haselkorn, T. S., & Badyaev, A. V. (2007). Functional equivalence of morphologies enables morphological and ecological versatility. Evolution.
Yu, M. K., Yue, Z. C., Wu, P., Wu, D. Y., & Mayer, J. A., et al. (2004). The developmental biology of feather follicles. International Journal of Developmental Biology, 48, 181–191.
Yu, M., Wu, P., Widelitz, R. B., & Chuong, C.-M. (2002). The morphogenesis of feathers. Nature, 420, 308–312.
Yue, Z., Jiang, T. -X., Widelitz, R. B., & Chuong, C. -M. (2005). Mapping stem cell activities in the feather follicle. Nature, 438, 1026–1029.
Acknowledgments
I thank B. Hallgrímsson, K. Oh, D. Seaman, R. Young, L. Landeen, and three anonymous reviewers for exceptionally useful comments on previous versions of this manuscript, and C. Schmidt-Dannert, R. Duckworth, and E. Bradley for extensive discussions and many suggestions. This work was funded, in part, by the National Science Foundation grants and the David and Lucille Packard Fellowship.
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Badyaev, A.V. Evolvability and Robustness in Color Displays: Bridging the Gap between Theory and Data. Evol. Biol. 34, 61–71 (2007). https://doi.org/10.1007/s11692-007-9004-5
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DOI: https://doi.org/10.1007/s11692-007-9004-5