COLOUI{ INI-IEI~ITANCE IN III. ]PACE AND LEG CO]~OUI~

BY J. A. FI~,ASER ROBERTS. (F~'om the Del)art,mc'nt of Agricult.ure, University College o/' North , Ba,ngor, and, the A,,d,ntal B,reedi,~g Research Dcl)a,rtmcnt , University of Edinburgh.)

I. ~NTRODUCT[ON. I)UPdN(." the past four years the writer has lm.d the opportunity of conducting experiments on the inherit'race of eolour in sheep and a part of the conchlsions that have emerged up to the present time have been published in a series appearing in this ,lou.r,nal (1924, 1926). It is hoped in this way to bring together the results obtained in these experiments as well as the results of other workers and so eventually to add a chapter to the study of coat colour in mammals, a study that h:ts led to fruitful hypotheses, and in particular to more or less physiological conceptions of. genetic action. The writer feels that some such explanation is required to prel!'me this paper, which is mainly n.n attempt to systematise a portion or the field and to analyse further the results obtained by Wood (1905, 1909), and only includes a few casual original observations. Unfortu- nately, there is little prospect at present el the carrying out of any f.urther experiments on the inheritance of [ace colour, so that it may be justifiable to analyse as far "l.s possible the results ah'eady obtained and to fit them into the general scheme.

2. THE RATIONALE OF VARIATIONS IN FACE AND LEG (JoLou~ IN SHEEP. Amongst the mammals about which something is known regarding the inheritance of wn'iations in coat eolour, sheep occupy a. rather special position, this being (:[tie to the peculiarities fit the make-up of the coat,. Primitive sheep, th'l.t are considered to resembh; closely the an('estors of the domesbicai, ed breeds, possess two clearly (leIined coats, a coarse outer protective coat, and it fine immr warmth-rei, a.ining coat. Mosl; modern sheep have l;he illller coat greai;ly developed at, the expense, el" the eli|or eo'~t which, in most cases, has become reduced to a covering of short ffourn, of Gem xlx 17 262 Cdour l'~heritance i'r~ Shee~ stiff hairs on the face and Legs, to a rcnmant of varying but usually snm,ll a,mount in tile body of the fleece known as kemp, and to a birth-coat sometimes present in the new-born lq.mb which is soon lost,. For the sake of simplicity, it; is convenient to visualise a threshold for the formation el pigment. All ordinary white sheep represents ,dmost complete restric- tion, a black one ,~Imost eoml?lete extension. Associated with this and other wlria.tions is the occurrence of dilution which t,ttrns the l)lack into broD.rll or light, red. Between the extremes of self-black and white m~my intermediate conditions arc found. For example, the writer (1924, 1926) has invest,igated what is probably a series of quadruple allclmnorphs; the top of the series is white, then come badger-face pattern, reversed badger-face patt,ern, and black. In this ease the intermediate condition m~ly be visualised as '1. pattern of black "rod white, the threshold for pig- ment [ormation being reached in certain areas but, not in others. Other patterns, such as the piebald pattern described by the writer (1926) or that of tile black-headed Persian sheep, are similar, in t,hat colour is confined to certain areas irrespective el the type el' fibres involved. Another intermediate condition is o1~ an entirely different kind. [11 this second type the threshold for pigment formation is reached in tile case el the derivat,ives of the primitive outer coat but, not at all, or only to a slight extent,, in the case of the derivat,ives of the inner coat. An excellent example el this type of restriction is the , which has been fully described from this point oli view by Nichols (1927). In the Sl.tffolk sheep the face and leg hair, the kemp ill body of the fleece and the portion of the birth-coat, derived [rom the outer coat, are black, while in the case of the wool fibres only the tip is pigmented, the pigment, being present in such small quantity that its contribution to the gross colour of the sheep is negligible. In the adult,, moreover, as tips do not occur except in regenerated fibres, even this slight, pigmentat~ion is almost absent. It is this type el colouring, where pigment is practically confined to deriva- tives of the out~er coat,, that, will be considered in this paper. It shouk[ be not,ed that a consequence of this type of pigment formq.tion is that there is an ahnost perfect, correlation between mnount, distribution, and dihlt,ion of eolour on the fa.ce and on the legs respectively, so t,ha.t when race colour is mentioned it will be understood that leg eolour is also included in the description. It is possible to ext, end the scheme llurt,her and to separal;e t,he va.rial;ions in face colour into three groups. 1. Variations in the. relat,ive proportion of pigmented and unpigment,ed a.re~s and their distribution. J. A. IFll,ASEI-r I~,OBEI~.TS 263 2. Variations in dilution. 3. Variations ill grades of completeness o17 restriction of pigment in the white sheep. A few words of explanation are required with reference to group 3. This group covers variations in the nature and amount of the small quantities of pigment found on the bare skin of the nose, on the hoofs, as well as spots on several regions chiefly round the nose, about the eyes and ears, and on the scrotum. This pigment is mainly confined to the sldn, the h~irs being white, but occasionally the pignlent spreads into the h'firs too. There are several lines of evidence to show that variations of group 1 type and of group 3 type are rightly sep~mtted. It will be shown that variations in the characteristics determined by l'aei~ors of group 1 are inherited in a definite way and that white-faced sheep are homozygous l:or that character. Their genetic constitution is the same in respect go group 1, although they may v'~ry considerably as regards the precise degree of restriction of pigment on the extremities. For example, sheep with pink noses and white hoofs and ahnost complete absence of pigment are in respect of factors of group 1 identical with sheep with black noses and hoofs which also show little spots of black round the muzzle and on the ears. Another line of evidence pointing to the same conclusion is that where there is considerable dilution of the colour on the face as determined by factors of group 2, the pigment on the nose and the scattered colom'ed spots are not necessarily dihtted correspondingly. For example, the has a broken-eoloured face, the patches being light red, but the nose and small spots round the nose and in the ears q.re dark. The wtrious breeds of sheep can be grouped as regards their face eolour in accordance with the scheme. The following breeds '~re dis- tinguished by whole colour on the face subject to increasing degrees of dilution: Suffolk--black. Hampshire Down--l)lack, but not quite as dark as the Suffolk. Shropshire brown. ])orset Down Southdown--mouse eolour. The following breeds are examples of white times with varying degrees of completeness of restriction of colour as determined by factors of group 3 : 264 Uolou~" Inheritance in Sheep

Merino ] Doli~et Horn~ very white. R,ydand J Longwoo] breeds, e.g. Border Leioester--whit;e with dark or motl:led nose and varying amounts of small dark spots. The following breeds have broken co]our on the face: Kerryhill---eoloured areas on face not as dark as black of SuiIolk. Scotch Blackface--whole Mack or broken black. Welsh Mountain--coloured areas light red or tan. A special complication exists in the ease of Wenslcyd'fles and Lei- testers, which are ('haraeterised by blue faces, the blue appearance being due to the growth of white fibres on a dark skin. This complication is not considered further in this paper. llt is a most remarkable fact, and one that apl)arently has escaped comment, that sheep with whole-colonred faces or white faces breed entirely true for these features, whereas breeds with 1)roken colour on the time most emphatically do not breed true for t~he grade of speckling desired, or even sometimes for broken cofour at all. Similarly, constant; selection is required to maintain the desired degree of dilution of colom' and the desired grade of restriction of colour on the nose. These facts suggest that inheritance of w~.riations of group 1 type is not complicated and suggests, furthcr, that whole-coloured faces and white faces depend upon a homozygous condition. It is a point of some interest that "white pattern," a white spot on the top of the head and a white tip to the tail, as described by Adametz (1917) and the writer (1924, 1926), among others, is not expressed in sheep with colottred faces, although it seems to be established that the factors responsible occur generally amongst colom'ed breeds and also in white ones. In the latter case, however, they cannot be expressed.

3. A FURTI~EIt ANALYSIS OF TIIE RESULTS OF WOOD. The only thorough piece of genetieal research on this subject was carried onl~ by Wood (1905, 1909), who made reciprocal crosses between Suffolks and Dorset Horns, raising an F., generation of 73. The Suffolk, as already mentioned, has an intensely black face, while the represents almost the extreme in reduction of pigment. The F~ animals had speckled faces of a more or less uniform kind, with some tendency to the formation of a pattern round the nose and eyes. An F 2 generation of 33 individuafs was raised and their characterisation was described as follows : J. A. Fm~sErr I)~OBEI~TS 265 3 pure black faces. 3 pure white faces. 3 white faces with black noses. 3 white faces with black round eyes. 3 white faces wii;h 1)lack round eyes and black noses. I with large irregular patches of black on the face. 17 with more or lass uniformly speeldcd faces. 33

A speckle-f'med F e ram was mated fie speckle-faced F t ewes, the result being given as lollows: No pure black faces. 2 pure white facts. 26 speclded facts or faces showing pattern. 28 A white-faced ram from this mating w,ts crossed to ])orset Horn ewes and gave nine lambs with pure white faces. Wood suggested Chat the evidence for segregation is clear and that three characters are probably involved representing white, black, the patterns and speclding, some eha.raeterisations depending upon the heterozygous condition. He did not attempt any further analysis, but after the lapse of eighteen years it is perhaps possible to do this. Questions of dilution do not enter appreciably into this cross. Suffolks have been selected for an extreme of darkness for generations, though it would appear that some diluting factors were introduced by the Dorset Horn because Wood mentions the fact that some of the hybrids exhibited a distinctly tan colour. ])ilution can therefore be ignored and attention concentrated on the action of factors of group 1. The true breeding character of the parents suggests that they repre- sent a homozygous condition. The extracted white from the F, x/~'2 mating was also a true breeding parental type. The ]}roportions of blacks and of whites in F, are strongly suggestiw; of a dihybrid ratio, the whites and the blacks being the homozygous parental forms. If it, is assumed that sheep with two dominants, one or both heterozygous, are speclde- faced, and that sheep with one dominant, either homo- or heterozygous, show the patterns, the constitutions and characterisation of the F2 are as follows : 266 Colour Inherita, nce in Sheep

1 AABB--black ft~ee. l AAbb. 2 AABb" 2 Aabb 2 AaBB speckle fa,ce. 1 aaBB pal;terns.

4. ~OMI,] I[<~IJIVIJI-[EtlOBSf,~I~VA'I?ION8, About three years ago the writer had the opportunity of exa.mining some 1~'1 and F. sheep of a Suffolk-Cheviot cross, bred by the late Dr ])ougb~s, of Auchloehan, Lesmah~Lgow. These sheep had been bred with ~ commercial lmrpose ~md the t,'1 was ~ selected one. The observations that i~ was possible to make were in perfect accordance with those of Wood. There were some differences that were to be expected when the distinction between the Cheviot and ~he Dorset l-[orn is borne in mind. New,fly all a.re white-faced at the present time, but in commercial flocks sheel) with broken tan on tile face are sometimes J. A. I?I'~ASj,~I~ ;l~o.Bl~l~T8 267 seen. This was responsible 1:o1' a cert~ain variability in the i,'l which the wrif,er did not have the opl?ortunity of examining fully because tllei<', sheep ha(l been selected I'or the uniform speckling. In the F.a the parental types, willie and whole eolour, appeared. There was much more dilution, however, some of the whole-eoloured sheep as well as t;he bi'oken-eoloured ones having f'mes of 'L peculiar sickly ldd-glove shade. The writer also had the oplmrlmnit,y of exanlining it I(erryhilI-Merino crossbred lamb which is a cross of considerable interest in colnieetion with thc general hypothesis. On this hypothesis the speekle-fa(:ed Kerry- hill slleep shmlhl possess both doniinanl;s, at least; one in the llet, erozygous condition. The Merino is whil;e-faee(I. The land) had a (lark lial~tern Oil the ilO8O exa.el~ly simila.r to the three F,, sheep (leseril)ed by Weed. It is not an unreasonable "l.ssumption to make that the lamb was i)robal)ly a homozygous recessive as regards one factor and heterozygous i~s regards the other. In any ease, this piece of evidence is entirely in l;avour of the position assigned to tflle speckle-faced Kerryhill breed. Blackface ewes, which have broken-eoloured or whole-black faces, are often mated to Border Leieestcr rams, which h~ve white faces. The face colour of the lambs from this cross is in entire agreement with the two-factor hypothesis. Some lambs l/.re speckle-faced, a large number have lighter faces with a pattern involving mainly the nose, and ooonsion- ~dly a white face is seen.

5. @ONCJI,UStoN. The analysis of \'Vood's figures, supported by the observations men- tioned in different parts el this paper, justify the adoption, as i~ working hypothesis, of the scheme outlined in the first part of the paper. There is reason to suppose that the variations in face colour of the white- fleeced breeds of sheep can be classified according to the throe el'cups postulated. 17'urt~her, there is good evidence that with regard to variations of the first group--those affecting the distribution of white an(:l coloured areas--the differen,Jes found in the pure breeds and crosses between theni can be explained in terms of two factors. Of course, the possibi]il~y nnist not be excluded that other t'acf,ors also exist thai, modify the action of f,hose main factors. Wifh regard to dilu'0io,l and extreme restriction nothing is known, but the multiplicity of grades f,hat exist suggest the inf,eraef, ion of nlany factors. One llraetical (.:onehision of interest is t;hti,l; in eases where breeders of sheep c]lal'aCJl~el'ised by b.rokell oolollr Oll the face lind il) dillicull; to 268 Colour Inheritance in Sheep

m~tintain l,heir ideal type, they have probably based that ideal tyl)e upon a hetcrozygous condition.

6. SOMMAI~. I. A tyl)e of pigmenta.tion in sheep is found in which t:he derivatives of the l)rimitive outer coat--face and leg hair, kern]), and birth-coat--are colom'cd and the body of the fleece practicMly free from eolom'. 2. Variations in f'me eolour fall into three groups: (1) Those affecting the reb~tiw', proportions and distributions of ('olourcd, and white fibres. (2) Those attecting the dilution of this pigment. (3) Those affecting the precise degree of restriction of pigmentation in the white-faced sheep; this pigment being mainly confined to the skin. 3. A further analysis of the results of T. B. Wood in his crosses of Suffolk and Dorset Horn sheep shows that these results can be explained on the basis of a two-factor difference, the variations in this case being of group 1. 4. As a worldng hypothesis, it is suggested that the a, bove classifica- tion, togct, her with the recognition that variations of group 1 are mainly due to the different states of two factors, affords a reasonable expbmation of the wu'iations in face colour found in the white-fleeced breeds of sheep and in their crosses.

7. ItEFEP~ENCES. ADA~IETZ, L. (1917). "Studien iiber (lie Mendelsche Vcrerbung der wichtigstcn Rassenmerkm~le der KarakulschMc bei Reinzucht und Krcuzung mit Haln- bouillet." Bibl. Gen. I. 1-258. NICHOLS, J. E. (1927). "On the Occurrence of Dark Fibres in the Sultolk Fleece with l?art.icular Reference to the :Birth Co~t of the L~mb?' Jour. Text. Inst. xvili. 395-417. ROBElVrS, J. A. F. (1924). "Colour Inheritance in Sheep. I. Bl~ek Colour a.nd Badger- face Pattern in Welsh Mountain Sheep." Journ. of Gen. XlV. 367-374. .... (1!)26). "Colour Inheritance in Sheep. H. The Piebald Pattern of the PiebMd ]3recd." Journ. of Gen. x~x. 77-83. ]~om~'rs, J. A. F. and J].:Nl~1~, T. J. (I926). "A Prclimina.ry Note on Reversed Badgerfaee Pattern in Sheep." Welsh Journ, ,'lyric. n. 70-73. Wooo, T. B. (1905). "Note on the Inheritance of Horns and Fa.ce Colour in Sheep." Journ. Attic. Sci. I. 364-365...... (1909). "The Inheritance of ]-Iorns and Face Colour in Sheep." Jouvn. Agric. s HL 145-15-1.