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Pigmentation and Feather Structure in Genetic Variants of the Gouldian Finch, Poephila Gouldiae

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Pigmentation and Feather Structure in Genetic Variants of the Gouldian Finch, Poephila Gouldiae PIGMENTATION AND FEATHER STRUCTURE IN GENETIC VARIANTS OF THE GOULDIAN FINCH, POEPHILA GOULDIAE ALAN H. BRUSI•I AND HAROLD SEIFRIED THE GouldJanFinch, Poephilagouldiae, is amongthe most colorfulof estrildinefinches. The speciesis distributedthrough tropical northern Australia,where it inhabitsgrassy plains. It is nomadicover at leastpart of its range,is an extremelysociable species, and occursin largeflocks even during the breedingseason. Because of its colorfulplumage and simple diet of seeds,it enjoysconsiderable favor as a cagebird. One of the most interestingaspects of the plumage in this speciesis the occurrencein nature of a polymorphismin facial color. Three facial or head colorsare knownin wild birds: black, which is the most common; red, which occursin approximatelyone out of four birds; and yellow or orange, which occursin only one in every three to five thousandbirds. As the color phasesare known from all areas of the species'range and occur in all flocks, they are not consideredseparate geographicraces. In addition to the three face colors, there are several mutants that involve both melanisticpigmentation (Butler, 1902) and feather structure (Im- melmann, 1965, pers. comm.) but theseare only poorly known. Becausethe Gouldian Finch is popular as a cage bird, a considerable amount of information has been obtained on the genetics of the facial colors. Southern(1946) has shownthat althoughthe black type is more commonthan the red, the red is dominantover black. Furthermore,the red and black allelesare sex linked. Murray (1963) showedthat the gene for the rarer orangeface is autosomaland recessiveto both red and black. Birds that are homozygousfor yellow and also for the recessiveblack head are black faced but have a yellow tipped beak rather than the usual red tip (Southern's"type C" black genotype). We undertookthe investigationson the pigmentationand feather struc- ture reportedhere for severalreasons. The GouldianFinch representsan opportunityto studycarotenoid metabolism in a nondomesticspecies about whosegenetics some information is available. Relatively little is known aboutthe metabolismof thesepigments in vertebratesgenerally and, in spiteof thewide use of plumagecoloration in aviansystematics, practically no information is available on the pathways of carotenoidmetabolism in birds. P. gouldiaeis of potentialgeneral interest in an attempt to under- stand the control and evolutionof these metabolicpathways. This finch alsoprovides ideal materialfor studieson the metabolismof pigmentsin 416 The Auk, 85: 416-430. July, 1968 July, 1968] GouldJan Finch Feather Structure 417 birds with complexplumage patterns. Much of the previouswork on the biochemistryof pigmentshas beenwith speciesthat are essentiallymono- chromaticin their carotenoidpatterns (Fox and Hopkins, 1966a; V/51ker, 1962). Finally, this material allowed us to extend considerablysome earlier work on the relationshipbetween pigment metabolism, deposition, and feather structure. MATEP.•AI,S A•D METI•ODS Skins of the three color phasesof the brightly colored, highly patterned GouldJan Finch were generously provided by H. B. Totdoff of the University of Michigan Museum of Zoology. Adults of both sexesare similarly colored,with the femalessome- what dulleL The back and upper surfacesof the wings are green, the rump and upper tail coverts cobalt-blue, the rectricesblack, the foreneck and breast lilac with a caudal margin of yellow-orange. The abdomen and sidesare yellow, the lower central abdominal area and under tail coverts white, the bill is greyish-white tipped with red, and the legs and feet are yellow. There is a black throat patch and a band of cobalt-blue encirclesthe head completely. Separate extracts of the head and various body contour feathers were made in 95 per cent alkaline methanol and in pyridine. Extraction was carried out in small batches over steam. Initial partition of alkaline-ethanol extracts with n-hexane or petrol ether partially resolved with crude ethanolic extracts into hypophasic and epiphasic layers. Each phase was washed three times with the opposite solvent, and the washingswere pooled and added to the original extract. Becauseno interfacial salts were produced during partitioning, we assumed no pigments with carboxylic functional groupswere present. Pyridine extracts were either used directly for some spectral analysis or the pig- ments were transferred to a more polar solvent by dilution. There were no differences in the pigmentsproduced by the two extraction proceduresas measuredby spectral tests or by co-chromatography.In many casespyridine is more desirableas an ex- traction medium than alkaline ethanol as the latter produces artifacts (alkoxide salts) with certain pigments. Pigments that remained hypophasic in the ethanol:n- hexane partitioning system were forced into petrol ether or n-hexane by the method of Rothblat et al (1964). Absorption spectra were recordedon a Cary RecordingSpectrophotometer (Model 11). Partition coefficientswere determined by the method of Petracek and Zechmeis- ter (1956) and M•,, values according to Krinsky (1963). Determination of the nature of various functional groups was by the reduction of keto groups with sodium borohydrate (Krinsky and Goldsmith, 1960) and conversionof epoxideswith acid chloroform (Karrer and Jucker, 1950). Acetylation with acetic •nhydride was used to test for hydroxy groups (Bamji and Krinsky, 1966) on both suspectedfeather pigments (xanthophyll) and on known xanthophyll. The xanthophyll epoxide struc- ture was further identifiedby reactionwith acetyl chlorideand reactionwith strong acid. Crude extracts of pigments were separatedby both column and thin-layer chroma- tography (TLC). Alumina was used exclusively in the chromatographiccolumns. The columnswere poured dry, under slight pressure,on to a pad of glass wool. Columnswere developedwith either benzeneand petrol ether or benzeneand ethyl acetate and the bands removed mechanically (Fox, 1953). The individual pigments were the.neluted with methanol, filtered, and forced into petrol ether by the addition of water. In nearly all casesthis treatment produced completely epiphasicfractions. 418 BausH aND SE•FmED [Auk, Vol. 85 The transfer of strongly hypophasicpigments was aided by the addition of a mixture of equal parts benzene and petrol ether. Columns were also used to prepare known carotenoid pigments:taraxanthin and violaxanthi.n from the dandelion (Taraxacum oJJicinale),lutein from corn (Zea mays), and canthaxanthin from feathers of the male Scarlet Tanager (Piranga olivacea). These pigments were used as reference compounds. Thin-layer chromatography (Stahl, 1965) was carried out on oven-dried preprepared silica gel plates (Eastman Kodak Chromatograms). The plates were developed with benzene-ethyl acetate (2:1). A benzene-acetone(98:2) system produced comparable separation,but the material oxidized more rapidly after separation than in the benzene- ethyl acetate system. For comparative purposes TLC was preferred to columns, as the resolvingpower was greater and the separation quicker. Furthermore, up to ten samplescould be eo-chromatographed simultaneously. Whole mounts of feathers from various parts of the head and body of P. gouldiae were made with Canada balsam. In addition, mounts of carotenoid-containingfeathers from various body areas were made from individuals of the following species: Piranga olivacea Dendrocopos villosus Piranga ludovicianus Colapies auratus Richmondena cardinalis Regulus satrapa Carpodacus purpureus Melittophagus gularis Pheucticus ludovicianus L ybius torquatus Acanthis flammea Pipra aureola Setophagaruticilla Ajaia ajaia Tyrannus tyrannus Phoenicopterusroseus Dendroica ]usca RESULTS Feather structure.--Melanin-containing feathers from the face of the black-headedbirds were characterizedby numerousrelatively long barbs which divergedfrom a short rachis. Each barb was coveredwith short, thick barbuleswhich containedheavy depositsof melanin (Figure 1A). (As in previouscommunications from this laboratorywe prefer a restrictive usageof the term barb. On a feather, the barb is the primary branch of the rachiswhich normally supports the barbules.This usageis synonymous with the term ramus.) The carotenoid-containingfeathers of the face also possessedonly a short rachis. However, unlike the melanin-containingfeathers, the barbs were flattenedand typically lackedbarbules in areasof carotenoiddeposi- tion. A few fine barbuleswere presentin the medial, unpigmentedareas of the barbs (Figure lB, 1C). A similar relationshipbetween structural elementsand pigmentationwas noted in the more complexfeathers of the neck of P. gouldiae. The longer barbs on thesefeathers had three different areasof coloration. The proxi- mal portionof eachbarb had numerousbarbules and the entire area was heavily pigmentedwith melanin granules. The middle portion of the featherconsisted entirely of sectionsof the barbs that lackedbarbules and July, 1968] GouldianFinchFeatker Structure 419 Figure 1. Structure of feathers from the face of the three color phases of P. gouldiae. A, black face, distal end of rachis and barbs with barbules; B and C, barbs of red and orangeface respectively.Note lack of barbuleson barbs in these two color phases. Actual length of feathers was 2 nun. containedcarotenoid pigment; this area was red in reflectedlight. In the mostdistal portionsof the feather the carotenoidpigment was absentfrom the barb and the feather appearedblue in reflected light but was black under transmittedlight. This was
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