Autosomal Colour Mosaics in the Budgerigar

AUTOSOMAL COLOUP~ MOSAICS IN TI-IE BUDGEP~IGAI%.

BY F. A. E. CI~EW ~D I¢0WENA LAMY. (I~stitute of Aq~i,ma~ Genetics, Unive~'sity of E(~inbuq:qh.)

(With Plate X and One Text-figure.)

BUDeE~IGA~ liLerature cmltains many references to "bieolours." The term "bicoloured," strictly used, is applied only to what the fanciers call a "half-sider" : a bird. with the plumage of one half of the body (one side from head to tail inclusive) of a colour appropriate to one variety, whilst the other ]lalf (side) is of a colour characteristic of another variety. But it is often used more loosely to describe any bird with two different varietal colours in its plumage, the actual regional distribution of these not being taken into account. The following list, which cannot be accepted as exhaustive, includes seven cases recorded in the Bu@e'ripa~" BulZetin, two eases described in De~" Wdle~zsil,tid~, and eight concerning which we have had correspondence with their owners. Two specimens have been lent to us ~or examination, but in no case has a eytologicM study been made : the bird is too valuable when alive, and useless for cytological purposes when dead. In all the popular books on the budgerigar to which we have had access it is stated that the bicoloured bird has its origin in an egg with two germs. This, presumably, is a reference to the explanations of gynandromorphism in the insect suggested by Boveri (1888), Morgan (1905), and Doncaster (1914). It will be remembered that Boveri ac- counted for this phenomenon by suggesting that the sperm enters au egg which has already begun its first division, and fuses with one of the resulting daughter nucl'ei. Morgan suggested that two sperms were involved, one of which united with the egg nucleus, whilst the other developed independently; and ])oncaster drew attention to a third possibility, namely the fertilisation by two sperms of two egg nuclei. It would seem that the alternative explanation offered by Morgan and Bridges (1919) has not yet become sufficiently demoeratised; yet the chromosome elimination hypothesis is especially useful in th.is connec- tion, for it can accommodate not only the "half-sider" but also the mosaic in which the distribution of the two colom's is not equal and symmetrical. The plumage colour characters involved in this bicolourism 234 Autosoma~ Uolour Mosaics ig~ the Budgerigar in the budgerigar are not, as in. the on,so of Wober's gnoh and Poll's bulffinch, sex-controlled, and they are not sex-linked; they are auto- somals and arc not affected, as is the colour of the core, by the sex horraones. The X-chromosome and the reactions of tissues to the hor- mones of ovary and testis are not concerned, a,nd bicolourism of this kind has nothing whatsoever to do with gynandromorphism or with hermaphroditism. The most probable explanation of this bieolourism is the dimination of an autosome : if the autosome carrying the dominant gone relating to body colour is lost at the first segmentation division in a hotorozygote, then the half-sider results; if it is lost later, then the recessive eolour will be expressed on an area less than one side, and t-,he later it is lost the smaller will be this area, and the extent of this area will be an indication of the time in development when this loss occurred. Thus genetics has a contribution to make to the embryologist, for, theoretically at least, it should help in the making of a timetable. It is not our purpose here to deal with the popular interpretations of budgerigar genetics. A brief statement of the genetic relations of the characters involved will be sufficient to explain the table of mosaics given. The symbols of other interpreters being ill-adapted to the cyto- gonotieal argument offered here, we have used throughout symbols of our own which conform to the type used by modern Drosophila geneticists and others; a mutant gone is represented by a letter, and its normal allele by a + sign, followed by the same letter when this is necessary for clarity. For alMomorphic genes the same basic letter is used, namely, that referring to the tirst established mutant form; those found later have an added symbol to indicate their difference. What may be regarded as the wild-type form of the budgerigar is the "light green" of the fancy, with its light green general body colour and black undulating markings of the wings. All the established mutant characters affect either the body colour or the wing markings, but here we are concerned only with four of these: yellow (y), grey wing (y'"), am allolomorph of yellow, blue (b), and Dark (D), a dominant colour modi~er fairly closely linked with blue. The action of Dark is to affect the distribution of the pigment in the feather so as to cause the plumage eolour, be this green, blue or yellow, to be dark or dull when compared with ~he wild-type light green or with the light blue or light yellow. In the simplex state it yields an effect intermediate between the nulliplox and the duplex. There are thus three shades or varieties each of green, blue and yellow, known to the fancier as light green, dark green, and olive; ]~'. A. E. C~mv ~I) 1%OWENA L~Y 235 sky bhe, cobalt and mauve; light yellow, dark yellow and yellow-olive respectively. Light green, sky blue and light yellow are without this dominant modifier; dark green, cobalt and dark yellow possess it in the heterozygous condition and so do not breed true; whilst olive, mauve and yellow-olive possess it in the homozygous condition. The bhe varieties have a body colour in which yellow is completely absent, and wing markings as in the wild type. The yellow body colour is clear yellow tinged with green; l;he wing markings being almost obliterated. Grey wing, an allele of yellow, yields an effect intermediate between yellow and wild type, the wing markings being grey and the general body colour a subdued green. Blue and yellow straw independent assortment in F2, the double recessive being the "white" of the fancy. This is not a pure white bird but one with a white ground tinged with blue which may be of the sky blue, cobalt or mauve type, the particular shade of blue suffusion being an indication of the presence or otherwise of the dominant modifier. Popularly, tlfis is indicated by the addition of the words blue, cobaIt, or mauve to white. Thus a white bird is either white-blue, white-cobalt, or white-mauve. It is worthy of note that every case of hicolourism in the list involves the "blue" atttosome. Whether this particular eliromosome exhibits a greater tendency to lag than do the rest may perhaps in the future be determined by combined genetical and cytological study. It is of interest to note that yellow is a much older mutant than blue, and that there is no record of the elimination of the yellow chromosome, unless it be that this is the cause of the "pied" character, for all the recorded instances of this condition are explicable on the assumption that the yellow chromosome is eliminated late in development. In twelve out of the sixteen half-aiders, it is on the right that chromosome loss has occurred. Since it is clear that the patchy bird, No. 17, is to be explained, as is also the half-sider, by chromosome elimination, it seems desirable to class them together as autosomal (colour) mosaics, if only for the reason that they are to be distinguished from the mosaics in which the X-chromosome is involved. Of the seventeen autosomal colour mosaics in this paper there are three cases (~1-, 8, 11) in which it is necessary to postulate the presence of a single Dark gene on the side where the elimination, has occurred. Two of these, ~i- and[ 11, give a consistent effect, the single quantity of D Journ. of Genetics xxx 16 "~ ¢o ~o~

8 d d 6 d d 6

~ © %-t © d3 ~oO~ ~.~ Q+,~ ~..~ ~o~ 0 .~o ~b.o~ ~ ~ o~ ~ bD ~'~ ~;e~ ~o~~.~o ~,o ~ ~ ~. ..~-~ ~.o o~ o .~ .~ .~og

o o .~,~ bD03 ~ ~'~ ~'~ o~ •~ .H ~ ~ ~7~ Zl "~ o H o'~, bO~ :1~r i o~ o~ 0 o,.~ 0~ bO ~ "'~ 0 ~O, ~N s ~ oo ~.~ ~ ~-~ ~ o 0 0~ .o~ o~ o~ o~-~ ~ 0 0 0 c~ 03 ~ g ~g~ 8 -~ ~ ~o o '~ .~'~ "~

N N;~ No -

"to o~- <-o o~- <-o C~-

4~ 0 I

b,O + J,.-..~ ~0~I~ ~0 ~ I~ 00~' + ~ +'~ ~o~ ~o p~ bo

C.) c~ ~q m

o ~ !~ 6~ +

~° ql% i +~ ~ I,-~ ~ 0 ~-~I ~

O0 d 8.0 d d d d d • ~ ~o

~o~ ~ ~ ~ o~ ~°*~ 0 ~ ~ bO ~'~ ® ~0 ~'~ 'r:.~0

~-~ ~ °~ N~s~ ~~ ~ ~ ~~0 ~

~ ~: ~.~ o ~ ~o

o~ ° ~ o~ ~ ~o

• , o-~ ~o ~ ~o ~ • ~o o~ o o o~ o~ .~ 0-~ 'T. o~ o-~ o~~° ~o~ .~=~ .°~ d

• ~

m N~ N n~°

~" OF '¢'0 "¢'0 OF "C-O 04- ~:0 OF

• ~ ~ ~ ..~0o ,

~I ~ ~ ~ co o -

o " + o

16-2 238 A utosomal Colour Mosaics i~z the Budgerigar producing the same degree of modification as when present with its normal allelomorph. But in No. 8, where the constitution of the side where elimination has ocm~rred is the same with regard to that gene, the effect produced is described as being equal to the homozygous condition of Dark, i.e. giving the "mauve" (instead of cobalt) suffusion of white. Since there is no reason to doubt that the observation is in each case correct, the explanation given for the last-named case is possibly in- sufficient. It might be necessary to postulate that not the wh.ole chromosome but only that portion carrying the normal allele of blue had been eliminated on the white-mauv4 side, leaving two Dark genes as on the normal side. But perhaps a simpler explanation is suggested by the fact that this bird was homozygous for yellow, while the other two were not. Since yellow obliterates in great part the oxydase that is normally present in blue, the material providing the sphere of action for the single Dark gene would be in this case considerably reduced, in consequence of which the effect produced by it would possibly be exaggerated. It is to be expected that the bicoloured bird will breed either as a heterozygous dominant, or else as a homozygous recessive, for the reason that the gonad of one side of the body is not necessarily derived from cells belonging to the same side. Thus in the case of a lighf green/blue "half-sider," the cells of the gonad can include either (1) two blue chromosomes, one carrying the blue gene, the other carrying the wildtype allele of blue; or (2) but one blue chromosome, this carrying the blue gene. Both of the testes of a male may be of the first type or of the second, or one can be of the first type and the other of the second, and thus a cock can breed as an unexceptional heterozygous blue, as a homozygous blue, or as a heterozygous blue peculiar in that he elaborates a great excess of gametes carrying the blue gene. The single ovary of a hen must either be of the first type or else of the second, and she will breed, therefore, either as an unexceptional heterozygous blue or else as a homozygous blue. But in the case of that gonad, either ovary or testis, with only one blue chromosome, half of the gametes elaborated thereby will be without this chromosome, and it would not be surprising, therefore, to learn that a bicoloured bird breeding as a homozygous blue was markedly infertile. F. A. E. CREw AND P~0WENA LA~¥ 239

THE CIIRO~'IOSOh'I]~S OF TIII~ I~UDO]~I~IOAr¢I. The mitotic metaphase plate, as revealed in 60-hours old embryonic material (Text-fig. 1) exhibits the same general features as are found in other birds (e.g. Crew (1932), White (1932), Sokolow and Trofimow (].933) in the fowl; Werner (1927) in the duck; Werner (1931) in the tin'key). There are three size classes of chromosomes, large, medium and small: ~he larger members of the complemen~ are to be seen at the periphery, and the small ones at the centre. Lightly stained granules were found among the small chromosomes, and it was impossible to decide whether these were chromosomes or not. If they are, then the chromosome number exceeds 60, if not, then the number is about 52. There are six large chromosomes, of which two have a submedian attachment constriction, and consequently are V-shaped with unequal arms. In the figure the largest is unpaired: it is assmned that this is the X-chromo-

Text-fig. 1. The chromosomesof ~he budgerigar (Alien's gentian-vioIeg) x ~200.

some, and that the individual from which the tissue was derived was a female. Three others of the large chromosomes have an attachment constriction which is subterminal, and they have one long and one very short arm. The remaining large chromosome has a median attachment, and is V-shaped with equal arms. At late mitotic anaphase the large chromosomes exhibit lagging. There are three pail's of medium-sized chromosomes, two with subterminal and one with a terminal attachment constriction. The small chromosomes are dot-like. They show a great tendency towards clmnping. Though chromosome elimination and non-disjunction might perhaps be demonstrated cytologically in cases in which the large chromosomes were involved, it would be quite impossible to do so if the small dot-like ones were concerned. However, it may be assumed that in a form such as this with so many chromosomes, irregularities ill their distribution 1 We are indebted to our colleague, Dr P. Ch. Koller, for the following nol}es relabing to the chromosomecomplex. 240 Autosomal Colour M/osaics in the Budgerigar must occur fairly commonly, and that evidence of such might take the form of the regional expression of a recessive plumage colour in a hybrid. [Note added 21. 1. 1935.] Since this paper was written, two other cases have been encountered. The first is in the possession of the Vienna Zoological Institute, and is cobalt on the right side, sky blue on the left. Prestmlably the explanation is that in a bird hefierozygous for the Dark gene, the blue chromosome carrying this gene and the gene for blue has been lost on the left. The second case, having been purchased fl'om a breeder, is now in our possession. Pheno~ype and geno- Phenotype and geno- type of parents l,ype of bicolour A______a d~ ~ right 1eft cobalt sky blue eobalb sky blue yg~'b D yb+D yb D y--- y b +D +y b +/9 +y b +D -VY b +D" Again in this case it is the paternal blue chromosome that is lost on the left. It carried the blue and the Dark genes.

SUMMARY. 1. Seventeen autosomal colour mosaics in the budgerigar (Melopsit- tacus undulatus) are described: sixteen of these being "half-riders." It is suggested that every one of them is the result of the elimination of the "blue" autosome. 2. The chromosome number is 50-60. There are three size classes: the X-chromosome is large : only one X is present in the female. The very considerable number of small dot-like chromosomes makes it impossible to'determine with certainty the actual number, and also to recognise chromosome loss. The large chromosomes show lagging.

REFEI%ENCES. ANoN (1933). "Wieder ~m ~rfolg in der Zuchfl der Ha]fseiter." Der Wellensittich, No. 21, 201-2. Hannover-Linden. ]3ov]~RI, Tm (1888). "Ueber par~ielle ]3efruchttmg." N.B. Ges. 2~ferph. Physiol. .~titnchen, 4, 64-72. Curer, F. A. E. (1932). "A c~sc o~ leg colour asymmet0ry in ~he fowl." J. Genet. 25, 359-65. -- (1933). "A e~se of non-disjunction in the fowl." Prec. roy. See. Edin. 53, 89-100. DONOAS~'~, L. (1914). The determination of sex. C~unbridgo. ])UNOKER, H. (]928). "Die Vererbung der Farben bei Wol]ensi~ichen." Vhgelferner L~gnder, i. FL;, " •

-L ~5 ""

~/..~.