536 BRUCKN•R,Inheritance o! WhitePlumage in Phasianus L[Auk Oct.

INHERITANCE OF WHITE PLUMAGE IN PHASIANUS

BY J. H. BRUigKNER

Plate •r8 TH• data herewithpresented deal with the inheritanceof white plumagein the Ring-neckedPheasant, Phasianus colchicus torquatus. in a previouspublication (1939) the author has pointed out the scarcityof knowledgeconcerning the geneticsof this speciesand re- ported on the inheritanceof an incompletelydominant, autosomal genefor melanin. A generalreview of the literature on the genetics of the pheasantis given in that paper and accordinglywill not be repeatedhere. The pheasantfancier has long had blue-eyedwhite pheasantsin his aviary, but the origin of this variety is apparently unknown. Occasionallyreports are publicizedof pure-white pheasantsbeing shot in the wild. Whether such birds result from mutations occur- ring in the wild populationor haveescaped from aviariescannot be proven,but the latter alternativeseems unlikely. White plumageamong wild specieswhich are normally colored is not uncommonand albinos have been reported in many birds as well as in mammals,reptiles, amphibians, etc. In very few birds, however,is the exact nature of the white determinedand in many casesthe specimendescribed is not a true albino at all but merely a bird with more or lessdepigmentation of the plumage. In the bird with completealbinism melanin is absentin all parts of the body. The eye appearspink in color becauseof the blood in the capillariesof the iris and retina. In most white birds the eye is black, brown, orange, or bluish, and all of these colorsindicate the presenceof melanin. True albinism is rare but birds in which a coloredeye is associatedwith white plumageare common. During the pastnine years,approximately a million pheasantchicks havebeen hatched at the New York Stategame farms and amongthese but one true albino has been found. It is not uncommon to find white chicks,but usually thesehave somepigmented down on the wings. Almost without exceptionsuch chicksdevelop some pig- mentedfeathers as they assumethe juvenal and adult plumagesand 'pied' birds, not white ones,are the final result. Inheritanceof color in the DomesticFowl, a speciesin the same subfamilyas P. colchicus,may give someindication of what might Vol.•94• •8-• a BRUCI•NER,Inheritance of WhitePlumage in Phasianus 537 be expectedof color in the pheasant. In that specieswhite plumage may be due to any one of three differentgenes. The White Leghorn fowl carriesa unifactorial,incompletely dominant, autosomalgene which inhibits the formation of melanic pigment. Fundamentally the White Leghorn is a coloredbird, but the presenceof the inhibit- ing gene in homozygousform preventsthe expressionof black. In heterozygousindividuals some color is evident. This type of white plumageis found occasionallyin other breeds,but so far as is known is the result of crossingwith White Leghorns. The secondkind of white plumage is that found in Plymouth Rocks, Wyandottes,Dotkings, Langshans,and other breedsof fowl. This white is autosomaland recessiveand is apparentlydue to the absenceof a genenecessary for the formation of melanin. Sincethe eyes are pigmented in both the dominant and the recessivewhites, neither is a true albinism and both should be considered as a kind of white in which the manifestationof melanin is usually restricted to the eye. Batesonand Punnett (1908) describedanother 'com- plementary' white in Silkie fowls, but no other workers have been able to detect it in that breed. True albinism is so rare in the fowl that in the thirty-nine years since the rediscoveryof Mendel's laws only one casehas thus far been reported. The conditionwas found by Warren (1933) to be a simpleautosomal recessive character. The white pheasantshows no signsof pigmentationin the plum- age, but beak and shanksare a pearl white and the eyesare blue. It can be seenthat the white plumageof the pheasantmight pos- siblybe any one of the geneticallydifferent types of white reported above, or possiblystill another, since in thesewhite pheasantsthe eyeis blue, a conditionnot found in any of the white fowlsmentioned above. Moreover,the shank color is affectedin white pheasants but not in mostwhite fowls. It is possible,of course,that in these white pheasantsthe shank-and eye-colordilution are due to other genesclosely linked with that for white plumage. In the absenceof definite information of the genetic basis for white plumagein the pheasantan investigationwas begun in 1938. While it was under way anotherreport of 'hereditaryalbinism' was found. Taibell (1928)concluded that white is a monohybridreces- sive character. He called his white specimens'albinos', but the description furnished indicated that they were blue-eyed whites. Since his studies were somewhat limited, it seems advisable to re- port the presentexperiments. 538 BRVCKN•rt,Inheritance of WhitePlumage in Phasianus L[Auk Oct.

GENETIC ANALYSIS

The first crosses were made in 1958. A male and two female white pheasantswere purchasedfrom a fancier with the assurancethat they had bred true for many generations. These birds had white plumage, blue eyes,and pearl-white beak and legs. There were no coloredfeathers anywhere in the birds nor did they showany after the adult molt. The male was mated with four Ring-neck females and the two white femaleswere mated to a Ring-neckmale with the following results:

Progeny

Parents Number Color

White cP X Ring-neck 9 9 89 Ring-neck Ring-neck cP X white 9 9 14 Ringmeek

This is what would be expectedin the Fx generationif the white plumagewere due to a recessive,unifactorial, autosomalgene. If the character were sex-linked and recessive,that would be shown by differencesin the progenyfrom reciprocalmatings. The mating of normal, colored,Ring-neck males to white femaleswould then produceF• progenywith normalplumage, but in the reciprocalmat- ing of whitemales to Ring-neckfemales, the femaleprogeny would be white, while the male progenywould be Ring-neck color. Since such'criss-cross' inheritance was not found, thesefirst matings demon- stratedthe autosomalnature of the gene. At maturitymost of the F• birdswere identical in appearancewith the Ring-neckstock, but an occasionalbird exhibiteda completely white primaryor tail-feather. Othershad a patchof white feathers on the throat but in the majority white was not in evidence. All progenyhad dark-pigmentedeyes, beak and shanks. F 2 GENERATION In 1959, the F• progenyof the white • X Ring-neck 9 9 were matedinter se to producethe F2 generation(pen 1-$9). This was also done [or the progenyof the Ring-neck• X white 9 9 (pen 2-$9). In theseF2 generationsthe expectationwas $ colored:1 white, if the white were a simple,recessive character. Classificationsat hatching,including embryosdying late in which color could be determined, were as follows: Vol.•94t •8] -• BRUCKNr•,Inheritance of White Plumage in Phasianus 539

Hatched Late dead embryos Combined

Ring-neck White Ring-neck White Ring-neck White

Pen 1-39 70 25 25 6 95 31 Pen 2-39 44 13 10 4 54 17

Combined total 149 48 Expected (3: 1 ratio) 147.75 49.25

Taken either separatelyor togetherthese matings yield an unusually closefit to the 3: 1 ratio expected. About onehundred oœ these birds were reared to maturity and in none oœthem did any oœthe white segregatesassume the Ring-neckplumage or showthe pied condition. It wasnoted that a numberoœ these (adult) birdshad an occasional dark feather,particularly on the head. Conversely,some oœ the F2 Ring-neckshad an occasionalwhite feather in the wing or a small white patch of featherson the throat. Doubtlessthese were indi- vidualsheterozygous for white. Birds oœthat genotypemust have comprisedtwo-thirds of the F2 population,but sinceonly a few oœ the Ring-necksshowed any white feathers,it is clearthat the white plumageis usuallycompletely recessive in the heterozygote. The symbolc, which is usedto denotethe genefor recessivewhite in the fowl, is assignedto this gene responsiblefor the absenceoœ color in the pheasant. The normal wild Ring-necked Pheasant would thus be CC, while the pure-whitebirds would be cc.

BACKCROSSES The expectationhere, as in any backcrossto the recessiveform, was a ratio of 1 colored: 1 white. Backcrossmatings oœ Fx progeny were made to the white male and females. One oœthe original white hens died during the breedingseason and, accordingly,two additional white hens were obtained from the original source oœ the stockused in the experiment. The resultswere as follows:

Hatched Late deadembryos Combined

Ring-neck White Ring-neck White Ring-neck White

Pen 3-39 33 21 21 15 54 36 Pen 4-39 61 66 30 15 91 81

Combined total 145 117 Expected (1: 1 ratio) 131 131 540 Inheritanceof WhitePlumage in Phasianus LI'Auk Oct.

There is a deficiencyof white chicks in both these backcrosses. Applicationof theX 5 testfor goodnessof fit of observedand expected ratios (in combinedtotals) yields a valuefor X• of 2.992and, with n = 1, the value for p is .083. This meansthat the deviation from expectationis not significant,and, therefore,the hypothesisthat a single gene causesthe recessivewhite is not invalidated. Dunn (1923) reported a lethal gene linked with recessivewhite in White Wyandottefowl. The deficiencyof whitesin thesepheasant back- crossesdoes suggest that embryonicmortality is higher in cc em- bryosthan in Cc ones. However,there was no deficiencyof the homozygousrecessives in the F• generationand the discrepanciesin the backcrossesshould therefore be ascribed to chance. Since the deficiencyof whiteswas evident in theembryos dying late, any lethal effectof the white in the homozygouscondition must have been exertedin embryosdying at somestage before the plumagecolor couldbe determined.It is noticeablethat the majordeviation from the expected1: 1 ratiowas in pen3-39, which yielded a ratioof 54 Ring-neckto 36 white chicks,whereas pen 4-39gave a ratio of 91 Ring-neckto 81 whitechicks. The latteris a reasonablygood fit to the normal ratio. Some of the white birds from the backcrossesshowed an occasional darkfeather and a few of the Ring-necksshowed a whitefeather or two aswas the casein the F• matings.

In orderto checkfurther the conclusionas to the geneticbasis for whiteplumage, the whitesegregates from the backcrossmatings, pens3-39 and 4-39, were mated inter se in 1940. Two suchmatings were made with the result that 75 chicks were hatched. These chicks wereall purewhite when hatched, and at maturityshowed no signs of coloredplumage. DISGUSSION The sourceof the white pheasantsas bred in captivityis not definitelyknown, but, ashas been mentioned, white individualsin wild birdsof otherspecies are not uncommon. Some of thesewild speci- mensare true albinos,but they are relativelyrare. Gamebreeders differin theiropinions as to theorigin of thisvariety. Somebelieve it to be a true mutationor 'sport'while othersthink that it is the result of selectionfrom 'pied' or 'spotted'stock. This latter aberrantform is relativelycommon. Gorrespondence with observantgame breeders hasindicated that white mutationsfrom Ring-neckand melanistic pheasantshave been known to occur. Vol.1941sS] .• BRUCKNER,Inheritance o[ WhitePlumage in Phasianus 541

It is evident from the data presentedin this paper that white plumagein the pheasant,Phasianus colchicus, is due to the presence in the homozygouscondition of a unifactorial, autosomal gene. Dominanceof the allele, C, for color, is sometimesincomplete since heterozygousindividuals often showoccasional white feathers. Con- versely,homozygous recessive individuals may show a slight ticking or a coloredfeather. Recessivewhite segregatesfrom backcrossmat- ings breed true when mated inter se. It would seemthat white plumage in P. colchicusis similar in characterto the recessivewhite found in White Wyandotte, White Plymouth Rocks and other varieties of fowls. However, in the pheasantthe pigment in the eye, beak and shank is so reducedthat thesestructures appear bluish, whereasthese areas are not affectedin white fowls. This suggeststhat the genes responsiblefor white plumagein the two speciesare not comparableor else,possibly, that the pheasantcarries a gene,or genes,for the dilution of eye, shank and beak color closelylinked with the gene c responsiblefor absence of color in the plumage. However, since in all the white birds raised in this study no exceptionswere observedto the rule that white pheasantshave blue eyes, beak and shanks, it seemsmost probable that the singlegene, c, is responsiblefor the dilution of melanin pigment in theseareas as well as for its elimination from the feathers. SUMMARY White plumagein the genusPhasianus is due to a single,auto- somal,recessive gene, c, presentin the homozygouscondition. This is shown by ratios observedin 103 Fx, 262 backcross,and 197 F2 pheasantsfollowing crosses involving white and Ring-neckPheasants.

LITERATURE CITED BAaW•SON,W., Am) PuremEant,R. C. 1908. Experimental studies on the physiologyof heredity. Reports to the EvolutionCommittee of the Royal Society,4: 18-35. ]•RUCKNER,J. H. 1939. The inheritanceof melanismin pheasants.Journ. Heredity,30: 45-52. DUNN, L. C. 1923. A lethal gene in fowls. Amer. Naturalist, 57: 345-349. TAIBELL, A. 1928. L'eredita meridaliana dell'albinism in Phasianus colchicus L. Rivista di Biologia, Milano, 10: 695-701. WARREN, D, C. 1933. Inheritanceof albinism in the DomesticFowl. Journ. Heredity, 24: 379-383. 5't2 BRVCKN•R,Inheritance of WhitePlumage in Phasianus [AukL Oct.

EXPLANATION OF PLATE 18

UPPERF•CURE: Normal Ring-neckedPheasant, Phasianus colchicus, used in study of the inheritanceof white plumage. Fx hybridsbetween this bird and pure-white pheasantscannot be distinguishedfrom the common Ring-neck except in rare in- stanceswhere one or two main tail- or wing-feathersmay be white. LowER F•CVRE:Pure-white pheasant used in this study. The white segregates in the F• and backcrossmatings are identical in appearanceand breedingbehavior with the original white stock. Departmentof Poultry Industry Cornell University,Ithaca, New York THE AUK, VOL. 58 PLATE 18

NORiMALLY PLUIMAGED RIN½;-NECKI•]D PHEASANT

I}URE-WHITE RING-NECKED PHEASANT USED IN THIS STUDY