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

Fg Silversides, Rd Crawford

To cite this version:

Original

article

Genetic

_aspects

of

a new

mutation

(S

al-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

S

al

obtained from the

University of Massachusetts. The gene symbol

S

al

-"

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 — _{Aspects génétiques} relatifs à une nouvelle mutation

(s

at

’

$

)

_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

s

al

-

s

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

+

.

s

al

-3

_/ albinisme _/ poulet / mutation

*

Present address: _D6partement de _Zootechnie, Universite _{Laval, Quebec, Canada,} G1K

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

s

al

-

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

s

al

-

a

_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

S

al

-’

_(Silversides

and Crawford

1990a,

1990b).

Fertile eggs from the

University

of Massachusetts

produced

the

males that carried the

s

al

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 s}

al

-

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}

_x

₂

_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

determined.

_{Heterogeneity}

_X

₂

_analysis

of the data allowed

_pooling

within

_mating

type.

Males with the genotype

S/sa!’8

were crossed to both

_s

_al

_-

_s

_1-

and

_{s+ /-}

females

to test for

_linkage

of

s

al

-

s

with the s+ locus. The

_hypotheses

of

_linkage

and

independent

assortment were tested with

x2 analyses.

Males

_carrying

s

al

-

s

were

mated to females

_carrying

s

al

’

s

and the

_resulting

_al

_c

_-

_al

_{I s}

_s

_-

_s

males were crossed to

Rhode Island

_Red,

Barred

_Plymouth

Rock and albino

_layer

line hens.

_{Heterogeneity}

x

2

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

s

ad

-

s

.

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%

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

_s

_al

_-

_s

males to albino and

_gold

females are shown

in table III.

_Expected

values take into account that

s

al

-

s

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 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

_(x

₂

=

0.53,

3

df,

P <

_0.90),

but not a 1: 2:1 1 ratio

(x

2

=

9.44,

2

df,

P <

_0.01).

Results of

_mating

males

_heterozygous

for

-

c

al

s

and

s

al

-

s

to females

_hemizygous

for

_{s (Rhode}

Island Reds and females from the albino

_line)

or S

(Barred

Plymouth

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

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

the albino

_{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

DISCUSSION

It is clear from these data that

s

li

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

s

al

-

s

to the s+ locus. Males

heterozygous

for S and

s

al

-

s

were crossed to

sa!-8

and s females. While results differed from those

_expected

with both allelism and

_independant

assortment of the

genes, X

2

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

s

al

-

a

and

sa!-!

confirmed the location of

sal-

s

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

_-

_feathering

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

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

s

al

-

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

s

al

-

s

and

c

s

-

al

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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_LD,

Smith

_EJ,

Crittenden LB

₍₁₉₈₈₎

Association of slow

_{feathering (K)}

and

an

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viral

(ev21)

gene on the Z chromosome of chickens. Poult Sci

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191-197

Bingham

PM,

Judd BH

₍₁₉₈₁₎

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_copia

_transposable

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tightly

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