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Of Sexual Dichromatism and Bright Plumage Coloration Has Been The Vol. 148,No. 3 The AmericanNaturalist September1996 CAROTENOIDS AND SEXUAL DICHROMATISM IN NORTH AMERICAN PASSERINE BIRDS DAVID A. GRAY* Departmentof Biology,167 Castetter Hall, Universityof New Mexico,Albuquerque, New Mexico87131 SubmittedFebruary 3, 1995; Revised November 9, 1995; Accepted November 17, 1995 Abstract.-Sexualdichromatism and the extent of male carotenoid-derived plumage coloration in breedingseason NorthAmerican passerine birds was analyzedby phylogeneticstatistical methods.Passerines as a wholeand five passerine subclades were analyzed by both independent contrastsand simulationmethods. In passerinesas a whole,carotenoids and sexualdichroma- tismare positivelycorrelated irrespective of analysismethod. In threeof the subclades,the correlationsare significant by a clearmajority of analysis methods. Neither melanin nor structur- allyderived colors show similar significant increases with dichromatism. Carotenoids are ob- tainedby animals solely through the diet, whereas both melanins and structurally derived colors can be synthesized.The relationshipbetween sexual dichromatism and theuse of carotenoids in plumagesuggests that sexual selection may have promotedthe expression of a condition- dependenthonest indicator of phenotypic quality. In birdswith nuptial display feathers, carotenoids undoubtedly play a positive r6lewhich is possiblya truesexual function. (GOODWIN 1952, p. 267) The function(s)of sexual dichromatism and bright plumage coloration has been thefocus of much research and debate (Darwin 1871; Sibley 1957; Selander 1972; Bakerand Parker 1979; Hamilton and Zuk 1982).Largely missing from this debate has been a considerationof the biochemicalbasis of plumagecoloration. The majorityof avian plumagecoloration is producedby one, or a combinationof several,of fourmajor types of colordeterminants. Three of thesefour are pig- ments,namely carotenoids, melanins, and porphyrins;the fourth is due to the physicalscattering of lightby microscopicairspaces within the keratinof the featheritself and by reflectionfrom the featherbarbules-so-called structural coloration(Fox 1976;Brush 1978). In general,white, blue, and iridescent plumage colorationis producedstructurally (Fox 1976;Brush 1978); bright red, orange, and yellowplumage coloration is due to carotenoidpigments (Fox and Vevers 1960;Fox 1976;Brush 1978; Hudon and Brush1992); brown, black, gray, buff, and dullbrownish red, dull orange, and dullyellowish plumage coloration is due to melaninpigments (Fox 1976;Brush 1978). Porphyrins produce colors ranging frombrown to blue, green,and red. Althoughwidely distributed among avian taxa,porphyrins tend to be restrictedto feathersor partsof feathers not exposed * E-mail:[email protected]. Am. Nat. 1996. Vol. 148, pp. 453-480. ? 1996 by The Universityof Chicago. 0003-0147/96/4803-0002$02.00.All rightsreserved. This content downloaded from 130.166.34.126 on Thu, 10 Sep 2015 17:16:07 UTC All use subject to JSTOR Terms and Conditions 454 THE AMERICANNATURALIST to directsunlight (Brush 1978),for example, feather shafts of youngpigeons (Fox 1976). Exceptionsare owls (Strigidae),bustards (Otididae), and turacos (Musophagidae).As thepresent analysis is restrictedto passerines,and porphy- rinstend to be restrictedto unexposedfeather areas, porphyrins are notconsid- eredfurther here. Carotenoidsare synthesizedonly in plants, algae, and somebacteria and fungi. Althoughmany animals can modifythe structureof ingestedcarotenoids, no animalshave been shownto synthesizethem (Fox and Vevers 1960;Fox 1976, 1979; Brush 1978); therefore,all carotenoidsfound within animals must have been obtainedthrough the diet. Because ofthis, a condition-dependentsignaling role forcarotenoids has been suggestedby severalauthors (Kodric-Brown and Brown1984; Andersson 1986; Hill 1990;Zuk 1992).Melanins are producedin animalsby the catabolism of the amino acids tyrosine, tryptophan, and phenylala- nine(Fox 1976;Brush 1978). Anabolic and catabolicpathways can interconvert proteinsand theseamino acids (Fox 1976).For thisreason, melanins are less likelythan carotenoids to be limited,honest indicators of phenotypicquality. Structuralcolors are producedby propertiesof thefeather, as previouslynoted. Featherstructure abnormalities are infrequentand usuallylethal in wild birds (Harrison1985). For thisreason, structural colors, in and ofthemselves, are less likely than carotenoid-derivedcolors to honestlyindicate phenotypic qual- ity,except perhaps extreme (i.e., usuallyfatal) nutritional, disease, or genetic stress. The basis ofavian plumage coloration suggests that carotenoid-derived colors, in and of themselves,have thepotential to honestlyreflect phenotypic quality, whereasmelanin and structurallyderived coloration may do so if coupledwith an additionalhonesty-enforcing mechanism. This is notto arguethat traits that are synthesizedendogenously are necessarilypoor indicators of phenotypic qual- ity.What is beingargued, however, is thatcarotenoid pigments by theirnature havegreater potential to be honestindicators of phenotypic quality than do either melaninsor structuralcolors in the absence of additional honesty-enforcing mech- anisms.Clearly many synthesized traits do reflectphenotypic quality, for exam- ple, the tail of the male peafowl,Pavo cristatus(Petrie 1994), the size of the combof redjungle fowl, Gallus gallus (Ligon et al. 1990;Zuk et al. 1990a),and the size and symmetryof severalfeather ornaments (M0ller and Pomiankowski 1993). Synthesizedtraits that do honestlyreflect phenotypic quality, however, mostlikely will require an additionalmechanism to enforcehonesty, for example, strongopposing natural selection, that is, handicaptraits (Zahavi 1975,1991), or testosterone-mediatedexpression (Folstad and Karter1992). For example,the badgeof the male house sparrow, Passer domesticus,is producedby melanin.It acts as a signalof social dominanceand status(M0ller 1987a). However,so far as anyoneknows, the honestyof thebadge as a signalis unrelatedto thefact thatit is producedby melanin.Instead, honesty is maintainedthrough social interaction(M0ller 1987b). Testosterone-mediated trait expression seems an un- likelyhonesty-enforcing mechanism for avian plumage, as male-typeplumage in most species of birdsdevelops from the absence of estrogenrather than the presenceof testosterone(see Owensand Short1995). This content downloaded from 130.166.34.126 on Thu, 10 Sep 2015 17:16:07 UTC All use subject to JSTOR Terms and Conditions CAROTENOIDSAND SEXUALDICHROMATISM 455 If sexualselection, either by male-male competition or byfemale choice, oper- ates on the basis of condition-dependenthonest indicators of quality(Zahavi 1975,1991; Andersson 1982, 1986; Kodric-Brown and Brown1984; Grafen 1990), thencarotenoid, but notnecessarily melanin or structural,coloration would be expectedto increasein lineageswith increased sexual selection.To test this hypothesis,I lookedfor interspecific correlations between sexual dichromatism and theproportion of carotenoid, melanin, and structurallyderived plumage col- oration.Specifically, the hypothesis predicts positive correlations between carot- enoid-derivedplumage coloration and sexualdichromatism. This argumentassumes that sexual dichromatism reflects the accumulated ef- fectsof sexualselection rather than other selective pressures (Darwin 1871; Sel- ander1972; Baker and Parker 1979; M0ller and Birkhead 1994). It is also assumed thatthe biochemical origin of plumagecolors can reliablybe inferredfrom the color itselfwithout requiring direct biochemical evidence for all species. This assumptionmay seem tenuous at best;however, Hudon and Brush(1992, p. 319) state,"Carotenoids produce the majority of bright yellow, orange, and redhues foundin birds . plumage color is a good indicatorof the kinds of carotenoids deposited."That is, notonly can thepresence of carotenoids reliably be inferred fromplumage color, but the specifictypes of carotenoidsmay also be inferred. Known exceptionsinclude hummingbird (Trochilidae) gorgets, which are pro- duced structurally,parrot (Psittaciiformes) red and yellowfeathers, which have an unknown,but probably noncarotenoid, color origin (Hudon and Brush1992), and the greenand red pigmentsof turacos(Musophagidae), which derive from theporphyrins turacoverdin and turacin(Fox 1976). An importantdifference between this study and previousstudies of theevolu- tionarysignificance of avian colorationis the analysisof dichromatismand the underlyingbiochemical nature of coloration. This approach has at leasttwo major advantages.First the conceptsof "conspicuousness"and "brightness"are avoided.This is a significantimprovement over previous analyses because con- spicuousnessand brightnessare subjectiveand dependenton ecologicallyrele- vantenvironmental conditions. In addition,as humansalmost universally per- ceive carotenoidcoloration as bright,correlating carotenoid coloration with "brightness"would be tautological.Second, the resultsare morelikely to be independentof differences between human and avian sensory systems, which are greaterthan previously appreciated (Bennett et al. 1994). METHODS Data Collection NorthAmerican passerines for which information was availablein a standard fieldguide (National Geographic Society 1987) and in a technicalbird-banding guide(Pyle et al. 1987)and forwhich phylogenetic information was availablein Sibleyand Ahlquist(1990) were used. Each of 12 plumageregions was scored forsexual dichromatism (i.e., dichromaticor notdichromatic) and probable color origin(i.e., carotenoid,melanin,
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