FG Silversides

RD Crawford

English

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Original article
Genetic aspects of a new mutation
(Sal-s) to sex-linked
imperfect albinism in chickens
FG Silversides * RD Crawford
Department of Animal and Poultry Science,
University of Saskatchewan,
Saskatoon, Saskatchewan S7N OWO, Canada
(Received 8 January 1990; accepted 22 August 1990)
Summary - A mutation to imperfect albinism occurred in a line of chickens that had been
closed for 15 generations. This is the sixth such mutation to be described in chickens, and
similar mutations have occurred in a variety of other avian species. The mutation is sex-
linked, recessive, and linked to the s+ locus, as well as to the Sal obtained from the
University of Massachusetts. The gene symbol Sal-" is. proposed for this new mutation to
distinguish it from other s°’1 genes in chikens. The occurrence of a number of individuals
mosaic for ocular pigmentation in matings involving s’l-a supports the hypothesis that
the mutation is the result of integration of a genetic element in or near the s+ locus.
,a’-5 / albino / chicken / mutation
Résume &mdash; Aspects génétiques relatifs à une nouvelle mutation (sat’$) pour l’albinisme
imparfait lié au sexe chez la poule. Une mutation pour un albinisme imparfait est apparue
dans une lignée de poulets qui était restée fermée depuis 15 générations. Il s’agit de la
sixième mutation de ce genre à avoir été décrite chez la poule; des mutations ont été
observées dans diverses autres espèces aviaires. Le gène mutant est lié au sexe, il est
récessif et lié au locus s+ de même qu’un gène sa! obtenu de l’Université de Massachussets.
Le symbole sa!’s est proposé pour ce nouveau gène pour le distinguer d’autres gènes s°l chez
le poulet. L’apparition d’un certain nombre d’individus mosaique3 pour la pigmentation
oculaire dans des croisements incluant sal- plaide pour l’hypothèse selon laquelle la
mutation est le résultat de l’intégration d’un élément génétique à l’intérieur ou à proximité
du locus s+.
sal-3 / albinisme / poulet / mutation
* Present address: D6partement de Zootechnie, Universite Laval, Quebec, Canada, G1K
7P4
INTRODUCTION
A sex-linked locus with three alleles is primarily responsible for control of pigment
production on the non-black areas of the fowl. The wild-type (s+) allele allows full
expression of phaeomelanin, the silver (S) allele prevents its deposition and the
allele for imperfect albinism allows only limited production of all types of melanin.
The literature describes at least 5 mutations to sex-linked imperfect albinism in
the chicken (Mueller and Hutt, 1941; Hutt and Mueller, 1943; Champion, 1958;
Werret et al, 1959). In 1983, 15 albino individuals, all female, were found among 700
progeny of a flock mating involving 12 sires and 30 dams, suggesting the presence
of a sex-linked gene. In pedigreed matings, one of these sires yielded 15 albino and
42 colored individuals when mated to Brown Leghorn females. Again, all albinos
were females and further studies of the new mutation are based on descendents of
this sire. The albino phenotype is similar to that of other imperfect albinos. Briefly,
melanin pigmentation in the down and feathers is reduced to leave a ghost pattern,
and the eyes are red at hatching but darken with age. The gene symbol sal-S (s =
Saskatchewan) is proposed for this gene to differentiate it from the others.
Similar mutations have occurred in other avian species: Japanese quail (Lauber,
1964; Sittman et al, 1966), ring-neck pheasants (Bruckner, 1969), turkeys (Hutt and
Mueller, 1942) and budgerigars (Kokemuller, 1936 as cited by Hutt and Mueller,
1942). A cinnamon mutation known to canary fanciers (Dodwell, 1976) would also
appear to be sex-linked imperfect albinism. This report summarizes segregation
data from crosses involving the sal- gene and describes the occurrence of mosaic
individuals among the offspring of crosses involving this gene.
MATERIALS AND METHODS
During the course of investigations of the new gene for imperfect albinism, a number
of lines of chickens were used. The line in which the gene mutation occurred
is a single gene marker stock segregating for 0 and P, formed from Aracauna,
Brown Leghorn and Rhode Island Red breeds in 1967 and 1968 and maintained
as a closed flock since then. The albino meat and layer lines were developed at
the University of Saskatchewan and segregate for Sal-’ (Silversides and Crawford
1990a, 1990b). Fertile eggs from the University of Massachusetts produced the
males that carried the sal gene maintained there. This gene was probably one
of the mutations first described by researchers at Cornell University (Smyth, 1987,
personal communication), hence the gene symbol sal-c (c = Cornell) will be used to
indicate this origin. The pure breeds used (Brown Leghorn, White Leghorn, Light
Sussex, White Wyandotte, Barred Plymouth Rock and Rhode Island Red) were
from the collection of antique stocks kept at the University of Saskatchewan. Most
have been maintened as unselected closed flocks for 20 or more generations.
In the course of these studies, 47 sets of matings were made, involving all
6 possible albino and non-albino genotypes (table I). Heterogeneity x2 analyses
(Strickberger, 1976) were performed on data sets making up the three mating
combinations expected to produce both genotypes with expected values based on
the hypothesis of a single sex-linked gene. The three other mating combinations were
expected to produce progeny of only one phenotype. The sex of 5421 individuals was
determined. Heterogeneity X2 analysis of the data allowed pooling within mating
type.
Males with the genotype S/sa!’8 were crossed to both sal- 1- and s+ /- females
to test for linkage of sal- with the s+ locus. The hypotheses of linkage and
independent assortment were tested with x2 analyses. Males carrying sal- were
mated to females carrying sal’ and the resulting al- I scmales were crossed to
Rhode Island Red, Barred Plymouth Rock and albino layer line hens. Heterogeneity
x2 analysis of the data from these three crosses allowed pooling of the data using
either hypothesis.
Individuals mosaic for ocular pigmentation resulted from a number of matings.
Although nearly all died mid-way through incubation, they were not observed
until unhatched eggs were opened after 22 of incubation. The occurrence and
approximate time of death was recorded for all mosaic embryos, as was the sex.
of 9 and the distribution of pigment in the eyes of 37. Mutation frequency was
determined as the number o,f mosaics divided by the total of albinos plus mosaics.
The frequency per mutation opportunity adjusted this data to account for albino
females having only one Z chromosome, and thus only one opportunity for mutation,
while albino males have two.
RESULTS
Table I presents segregation data from matings involving sad-. In matings between
albinos, 15 non-albino individuals were observed; this is probably too many to
be explained by pedigree errors. In the three matings where both genotypes were
expected among the progeny, a slight deficiency of albinos was observed which was
not explained by consistent differences in fertility or early embryonic mortality. This
difference was significant in only one mating and was largely the result of a difFerence
in one of the 16 data sets pooled to obtain the totals shown. In this mating, 23.3%
of offspring were albino (25% expected), and in the exceptional data set, 22.1%
were albino. Both of these suggest a ratio of 1: 3 albino and non-albino individuals.
The cross between homozygous non-albino males and non-albino females produced
two albino individuals, probably the result or pedigree errors.
The four crosses expected to produce albino offspring all produced a low incidence
of individuals which were mosaic for ocular pigmentation (table I). This was
observed as an area of pigment on an otherwise colorless eye. No mosaic individuals
were observed in over 900 offspring of the crosses not expected to produce albinos,
suggesting that mosaics were the result of albino melanocytes becoming capable of
producing pigment, rather than the reverse.
Sex ratio (table II) produced by these matings were very close to those expected
from a sex-linked recessive gene. Four unexpected individuals (1 albino male and 3
non albino females) may have been the result of pedigree errors or misclassification.
The results of mating S I sal-s males to albino and gold females are shown
in table III. Expected values take into account that sal- came from a stock
homozygous for s+ and the albino parents would be expected to carry s+ in a
cryptomeric form if the genes reside at separate loci. Chi-square analyses showed
that the results differed from both hypotheses. However, the x2 value for the
hypothesis of linkage was much smaller than that for independant assortment. A
similar situation was observed when heterozygous males were mated to gold females.
Mating males heterozygous for sai-! to females hemizygous for s’l-  produced
141 embryos. Allelic genes should produce a 1:1:1:1 1 ratio of albino and non-albino
males and females, and complementation of unlinked genes should result in a 1: 2:1 
ratio of albino females, non-albino males and non-albino females, with no males.
The observed numbers were 38:32:36:35 and x2 analysis showed that these fit a
1: l:1:1 1 ratio (x2 = 0.53, 3 df, P < 0.90), but not a 1: 2:1 1 ratio (x2 = 9.44, 2 df,
P < 0.01).
Results of mating males heterozygous for sal-c and sal- to females hemizygous
for s (Rhode Island Reds and females from the albino line) or S (Barred Plymouth
Rocks) are shown in table IV. Again, hypothesis of both linkage and independent
assortment were tested. The data were found to fit a 1:1 1 ratio, expected with
alleleism of the genes, but not a 3:4:1 1 ratio.
Table IV shows the occurrence of embryos mosaic for ocular pigmentation
observed among the offspring of 15 matings. Mosaics appeared to be albino except
that one or both eyes contained a variable amount of pigment. The 15 embryos
classified as non-albino produced from matings of albino males to albino females
were thought to be mosaics with extensive areas of pigmentation. No attempt was
made to record mosaicism of feather pigmentation since mosaic embryos died soon
after feather growth began, the embryos were not observed until after 22 days
of incubation (8-12 days after death) and the genes c and I segregated of these
populations producing white down on non-albino individuals. The frequency of
observed mosaics per mutation opportunity ranged from 0.52 to 4.87%. The data
sets were classified into those involving the albino meat line, those involving thealbino layer line, and those involving sa -1. There were no clear differences between
the 3 groups and the frequency of mosaics observed per mutation opportunity was
1.93% in combined matings.
The distribution of the pigment on 37 of the mosaics was observed. More pigment
was seen on the right side of 31 embryos, on the left side of 4 and the pigment
on 2 others was deposited approximately equally on both sides. Sixty-four of the
embryos died between 9 and 15 days of incubation, 7 died before this time and only
3 survived longer; none hatched. The sex of 9 mosaic individuals was determined
surgically. Three were male and the rest were female. One female was from a cross
expected to produce only albino females and the other mosaics were from crosses
expected to produce albinos of both sexes.
DISCUSSION
It is clear from these data that sli is sex-linked and recessive. Six mating combi-
nations, comprised of 47 crosses made over a period of several years and involving
different populations, resulted in the genotype of 9637 individuals and the sex of
5421 of these being determined. The results were very close to those expected.
Crosses were made to determine the relationship of sal- to the s+ locus. Males
heterozygous for S and sal- were crossed to sa!-8 and s females. While results
differed from those expected with both allelism and independant assortment of the
genes, X2 values for the hypothesis of allelism were small. Linkage does not explain
the observed difference from expectations using either hypothesis, since the observed
results did not fall between the expectations, and were closer to those expected with
allelism of the genes. In addition, linkage would be expected to produce deviations
from expected in the same phenotypic classes and in the same direction for both
crosses, a result which was not observed. The deviation from the ratio expected
with allelic genes is probably due to chance, although misclassification cannot be
ruled out. Allelism of sal- and sa!-! confirmed the location of sal- to the s+ locus.
One consistent observation among the crosses expected to produce albinos was a
slight deficiency of the mutants. This deficiency, the occurrence of mosaic embryos,
and the large number of mutations to sex-linked imperfect albinism in various
avian species could all be explained if the mutation was the result of integration of
a movable genetic element into or near the s+ locus.
McClintock described such elements in maize (Fincham and Sastry, 1974) and
they have since been well documented in maize, bacteria, yeast and drosophila
(Calos and Miller, 1980; Whitney and Lamoreux, 1982). Bingham and Judd (1981)
proposed that the wa mutation in Drosophila resulted from the insertion of the copia
element into the fly’s genome but not into the peptide coding region, producing a
mutant phenotype which is near-white with eyes containing a substantial amount of
pigment. Such polar effects have also been described for bacterial insertion elements
(Nevers and Saedler, 1977). Jenkins et al (1981) suggested that the dilute (d)
coat color mutation of mice may be the result of viral DNA integration. Bacon
et al (1988) suggested that the K mutation in chickens could also be the result of
viral integration since K and ev21 are tightly linked and because females in slow-
feathering strains of White Leghorns infrequently revert to the rapid-fe thering
phenotype. Unstable genetic elements have been implicated or proposed to explain
pigment mosaics in plants (Groose et al, 1988; Smith et al, 1988), mice (Witney
and Lamoreux, 1982) and dogs (Sponenberg, 1984). The mutations alter the
pigmentation and random somatic reversions to wild-type produce areas of normal
color. Somatic reversions to wild-type affected 5.3 to 46.5% of mice with various
mutant phenotypes (Whitney and Lamoreux, 1982) and 1.8 to 4.8% of merle dogs
(Sponenberg, 1984).
Somatic reversion in a small percentage of imperfect albino embryos could explain
the slight deficiency of albinos, since all mosaics were presumably albino. The rate
of reversion is comparable to that found in mice and dogs, keeping in mind that
classification of mosaics here was only on the basis of ocular pigmentation, some
mosaics were classified as non-albino (3.9 and 2.0% in 2 sets of matings involving
only albino parents), and that albino females had only 1 sex chromosome. The
phenotype of mosaics is similar to that of a number of organisms carrying unstable
elements and the production of some pigment by mutant birds suggests that a
sequence is inserted near the locus rather than into it.
Mutations to sex-linked imperfect albinism are common in avian species. The
gene is sex-linked and the phenotype is dramatic in a colored population, so that
new mutations are easily seen. Nevertheless, random integration of a sequence
providing this number of apparently identical mutations would be at a level that
would cause havoc with the remainder of the genome and would appear to be
unlikely. Most insertion elements are at least moderately specific in their site of
integration (Calos and Miller, 1980). Tereba (1983) reported that 6 of 10 ev loci
localized in the genome of the chicken have been found on chromosome I and
suggested preferred integration sites of the ev DNA as one possible explanation.
An insertion sequence may have a preferred site of integration in the avian genome
at or near the s+ locus, or an insertion element may reside at a suitable distance
from the the locus to transpose easily into or near to it. Somes (1984) shows many
mutant genes, including K, in this region of the sex chromosome of the chicken,
supporting the latter hypothesis. Rates of reversion in crosses involving the albino
layer line, the albino meat line and sal-c were very similar, suggesting that this is
independent of the genetic background of the birds, and that if insertion elements
are involved, they are similar for sal- and sal-c and are inserted in similar places.
ACKNOWLEDGMENT
The authors with to express gratitude to P M6rat for providing the French
translations.
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Genetic aspects of a new mutation  (Sal-s) to sex-linked  imperfect albinism in chickens

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Genetic aspects of a new mutation (Sal-s) to sex-linked imperfect albinism in chickens

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