Download An Autosomal Dwarfism in the Domestic Fowl

BREEDING AND GENETICS
An Autosomal Dwarfism in the Domestic Fowl
R. K. Cole1
Department of Microbiology and Immunology, College of Veterinary Medicine, Cornell University,
Ithaca, New York 14853-6401
ABSTRACT A mutation in the Cornell K-strain of
White Leghorns, first recognized when two adult males
in a pedigreed family were definitely smaller than their
two other brothers, proved to be an autosomal recessive
mutation and gave rise to the autosomal dwarf stock.
The effect of this gene (adw) can be recognized during
embryonic development and leads to a normal adult,
except for a 30% reduction in body weight. Selection for
small size, egg production, and egg weight over a period
of 15 yr yielded an efficient layer. Production for 11 mo
from first egg was at a rate of 70%, with egg weight at
56 g and body weight at 1,160 g at 10 to 11 mo of age,
based on data for the last four generations. Viability of
the caged hens averaged over 95% for the 13 generations
involved. Sexual maturity was delayed by about 2 wk,
and good incubation (85+%) required 18± more hours
than normal.
When an autosomal dwarf male is used as a sire and
mated to sex-linked dwarf (dw) females, all progeny are
of normal size. Compared with problems of mating normal size males with dwarf females, the use of the two
types of dwarfism can yield good fertility.
(Key words: autosomal dwarfism, body size, economic traits, genetic selection, reproduction))
2000 Poultry Science 79:1507–1516
INTRODUCTION
Almost since the beginning of Mendelian genetics,
there has been interest in the inheritance of body size.
The effect of heredity on body size was used by breeders
long before the science of genetics came into existence.
Various breeds of chickens and other domesticated animals, which varied greatly in size, had already been developed by selection. With the early genetic experiments
with chickens, it became clear that in crosses of breeds that
varied considerably in body size, the offspring exhibited a
blended inheritance for size, although for a time it was
popular to try to fit the data to a limited number of genetic
factors. One now accepts the concept that body size, better
estimated by measurements of the skeleton than of
weight, is essentially a quantitative trait due to the effects
and interaction of many genes.
In crosses between breeds that differ considerably in
size, the F1 population is usually intermediate in size
between the two parental breeds. In some cases, the average for the crosses is above, and in others, below the
mean of the parents. A variety of interpretations can be
used to account for these differences. It is known that the
size of the egg from which a chick is hatched can influence
its size over a relatively long period of time (Goodwin,
1961), although eventually this effect on size is overcome
Received for publication January 9, 2000.
Accepted for publication April 24, 2000.
1
To whom correspondence should be addressed: [email protected].
by the genes of the chick. When the two parental stocks
are relatively similar in size, the progeny may have a
larger body size than either parent, and this is normally
attributed to hybrid vigor. One would expect such a phenomenon to be expressed in crosses between two breeds
that are quite divergent in size, and to be evoked to explain those cases in which the F1 birds exceed the mean
of the two parents. For other cases, some different explanation must be provided. Specific genes known to affect
body size are few in number. Some genetic traits that
affect developmental or physiological processes are associated with a generalized reduction in body size, whereas
for others the reduction may be more pronounced in
the long bones, especially the distal ones of the limbs
(Hutt, 1929).
The sex-linked gene for dwarfism, dw, recovered from
a stock of New Hampshires and described by Hutt (1949,
1959), was the only gene that substantially reduced body
size without adversely affecting viability or efficiency of
reproduction. Hutt (1959) acknowledged receiving some
dwarf White Leghorn pullets from a local farm and cited
their egg production for 110 d and egg weights. He believed they were similar to other dwarf White Leghorns
being studied by Bernier and Arscott (1960), and thus
their dwarfism was due to the dw gene.
The dwarf females from the local farm were subsequently mated to a male that was heterozygous for the
Abbreviation Key: adw = autosomal dwarf gene; dw = sex-linked
dwarf gene.
1507
1508
COLE
dw gene that Hutt had obtained from New Hampshires.
Half of the progeny, both female and male, were subsequently identified as dwarfs (Cole and Austic, 1980). This
proved that the same mutation had occurred in two
breeds of chickens.
These White Leghorn dwarf females came from a cross
of two selected strains and were used by the Kimber
Farms in California as the female parent of the famous
K-137 commercial laying stock. Such breeding stock was
available in Oregon and sold around the world, it is likely
to have been the source of dwarfism observed by other
poultry breeders. Bernier (personal communication; 2000)
fully agrees: “The Leghorn dw gene we worked with
definitely came from two local hatcheries that had purchased Kimber stock.”
Two reports (Rajaratnam et al., 1971; van Tienhoven et
al., 1966) showed that feeding iodinated casein did not
alleviate the effects of the dw gene on body size or egg
production. This finding indicated that hypofunction of
the thyroid gland was probably not a factor in this type
of dwarfism. However, Summers (1972) found that such
dwarfs responded to a dietary supplement of iodinated
casein in a number of ways, including better egg production and larger eggs.
In a cross between Rose Comb Black Bantams and
Barred Plymouth Rock females, in which there must be
many genes related to differences in size, Godfrey (1953)
estimated the number to be 15 pairs, and showed in a
backcross to New Hampshire females in an F2 line that
smallness was associated with s and k, but not b, from
the bantam. Hutt (1959) showed that the gene dw was
closely linked with the loci for s and k, with 7.0 and 6.6%
crossing over, respectively. In the Godfrey cross, in which
the F1 females should, according to his hypothesis of a
single recessive gene, carry that gene for small size and
the males should be heterozygous, at 30 wk of age the
females were only 69% as heavy as the F1 males. This
difference is somewhat greater than the 78% expected for
normal sex-dimorphism (see Hutt, 1959), for calculation
of data from Waters). However, it would appear that the
proposed gene operating in the crosses of Godfrey is
probably not the same as dw, although it may be an allele.
If the reduction in weight of approximately 30% associated with the dw gene in hemizygous females is related
to the normal sex difference of 78%, Hutt’s F1 females
from a cross of dwarf males with normal females should
weigh approximately 55% as much as the normal-appearing, but heterozygous, F1 males. Hutt’s (1959) data
shows 57% for this relationship. In a cross using the same
one as Godfrey (1953), Jull and Quinn (1931) found from
very limited data that the F1 females were only 72% as
heavy as the F1 males at 30 wk of age, a figure very
close to Godfrey’s 69%. In the reciprocal cross, the sex
difference was 85%. Thus, in the crosses between Rose
Comb Black Bantam and the Barred Plymouth Rock, there
is evidence from two sources that the net effect of the sex
chromosome from the bantam is to depress body size.
Whether a specific gene is responsible was not established. Kaufman (1948) also had some limited data that
indicated that “Partridge-coloured bantams” were small
because of a sex-linked recessive gene.
Maw (1935) provided better evidence that a specific
sex-linked gene influenced body size, but in this case
small size was inherited as a dominant trait. The cross
was between the Golden Sebright Bantam and the much
larger Light Brahma. Furthermore, in the F2 generation,
in which the number of females was relatively large (83),
the distribution (based on length of femur, which varied
from 57 to more than 81 mm) showed a reasonably good
bimodal array, as would be expected if a single sex-linked
gene for size was segregating in the female progeny of
heterozygous sires. There are a variety of bantam breeds,
and there is no reason to believe that smallness is necessarily inherited in the same way or even that sex-linked
genes may be involved in all cases. Jaap (1971) found
similar evidence for a dominant sex-linked effect that
reduced body size by about 10% in Sebright Bantams.
A dwarfism, inherited as a simple autosomal recessive
trait, is described in this paper.
ORIGIN OF THE AUTOSOMAL DWARF
Among a family of four brothers hatched in 1964 from
a mating within the Cornell K-strain of White Leghorns
(Cole and Hutt, 1973), there were two recorded as dwarfs
when housed at 7 mo of age. The record further indicated
that they were “proportionally reduced in size and in
good fleshing.” At 1 yr of age, one weighed 1,740 g and
was marked as “thin,” whereas the other (N 991) weighed
2,100 g and was marked as “solid fleshing.” Weights for
10 males of the same age used as sires in K-strain matings
in 1965 averaged 2,670 g.
Inheritance
A mating was made using dwarf male N 991 and three
full or half-sisters, and two unrelated K-strain females.
Two of the three sibs produced more than two chicks,
and for these there was a ratio of 18 dwarfs to 26 nondwarfs. The two unrelated dams produced 30 normal
progeny and no dwarfs. These and other data are given
in Table 1.
In matings of dwarfs inter se, including those involving
segregates from the K-strain, the dwarfism bred true to
type with only one recorded exception among several
hundred progeny classified. The one exception, hatched
in 1967, had a body weight at 6, 8, and 10 wk of age
slightly below the average for other dwarf females and
subsequently bred as a dwarf when mated to a dwarf
male (all of her nine progeny were dwarfs). In Table 1, this
female is considered to be a dwarf. Because the matings in
1968 among dwarf breeders had produced only dwarf
progeny, some of the cockerels from matings in 1969
through 1971 were discarded as early as 7 wk of age. For
these, a definite classification for dwarfism was therefore
not possible. All cockerels that were retained, even
though a majority were discarded at 5 mo of age, were
classified as dwarfs.
1509
AUTOSOMAL DWARFISM IN DOMESTIC FOWL
TABLE 1. Results of mating dwarf males to various types of dams
Dams
Expected1
Observed
Source
No.
Phenotype
Dwarf
Normal
Dwarf
Normal
Sibs of original male
K-strain
K-strain segregates
1967 breeders
2
2
4
5
3
2
14
4
62
Normal
Normal
Dwarf
Dwarf
Normal2
Normal
Dwarf
Normal2
Dwarf
18
0
27
19
6
23
147
28
26
30
0
0
9
21
0
30
22
0
27
19
7.5
0
147
29
22
30
0
0
7.5
23
0
29
235
192
0
0
C-strain
1968 breeders
1969 to 1971 breeders
Females
Males
235
192
0
0
1
Expected if dwarfism is a simple recessive trait.
Heterozygous: from a mating of dwarf male × normal female.
3
At variance with expectation; see text.
2
In backcross matings, using dwarf sires and seven normal daughters of dwarf sires, the ratio of 34 dwarfs to
39 normals was in agreement with the expected 1:1 ratio.
In an outcross to females of a different strain 2 of 23
progeny were recorded as dwarfs. Even though presumably the product of an outcross, their body weights at 6, 8,
and 10 wk of age were within the range for contemporary
dwarf females and outside the range for nondwarf females. One was discarded at 3 mo of age and for her the
classification could have been incorrect. The other one,
however, when mated to a dwarf male produced 13 progeny, all dwarf. Dwarf birds had not been seen previously
nor subsequently in this other strain (Cornell C). It must
be admitted, although reluctantly, that an error in the
pedigree of some chicks assigned to the C-strain dams
had been made. The data, however, support the conclusion that the dwarfism is caused by a single recessive
gene, for which the symbol adw was suggested.
DESCRIPTION OF THE DWARFISM
At the early age of 10 wk, the dwarfs can usually be
recognized by a combination of three criteria. These include low body weight, a somewhat shortened shank,
and a compact conformation of the body.
Body Weight
The effect of the dwarfing gene on growth is clearly
expressed by 6 wk of age, when the dwarfs are reduced
in weight compared with their normal but heterozygous
sibs. Among a small number (23 of each phenotype, as
subsequently determined) there were no overlaps of
weights at 6 wk of age. At 8 wk of age, for which more
data are available, the dwarfs’ average weight was only
69% as much as that of their normal sibs. As will be
shown later, the effect of the adw gene commences during
embryonic growth.
With few exceptions, the normal segregates were not
retained to maturity, and hence there are no data from
which to calculate the effects of the dwarfism on adult
body weight. Because selection within the dwarf line has
been for smallness in addition to reproduction traits, the
size of these birds in later years probably results from
the combined effect of the adw gene and the many others
that affect growth and body size. We can, however, make
some estimations by comparing the dwarfs with K-strain
birds of a similar age. For at least 10 yr, the K-strain had
also been selected for a smaller size than the 2,000 g that
was characteristic of the strain in the previous decade.
As adults, the dwarfs were maintained in cages, a management procedure that results in an increase in body
weight, whereas the K-strain birds were maintained on
the floor. The body weight recorded immediately after
oviposition at 1 yr of age for 78 dwarf hens hatched in
1971, was 1,345 g (a range of 1,130 to 1,670 g, with only
two above 1,550 g). The average weight for K-strain hens
for a 4-yr period (1966 to 1969) was 1,800 g. Thus, these
caged dwarf hens were approximately 75% as heavy as
the nondwarf K-strain hens housed in floor pens.
Relatively few dwarf males were retained to full maturity. Fifteen males (hatched in 1969) averaged 1,929 g (a
range of 1,640 to 2,210 g) at 9 mo of age. Eight 2-yr old
cocks (hatched in 1971), retained because of good sibtests for egg production and egg size, averaged 1,870 g
(range 1,710 to 2,090). They were, therefore, approximately 70% as heavy as K-strain males. In general, the
effect of the adw gene on body weight is similar in males
and females, and results in a reduction by approximately 30%.
With renewed interest in the stock and the availability
of support funds, expansion of the stock was permitted
in 1979. In the intervening years—1972 to 1979—one nonpedigreed generation involved the surviving and limited
number of dwarfs (six males and 11 females, then 5 yr
old). In 1979, the surviving three males and six females,
then 3 yr old, were used in nonpedigreed matings that
included unselected K-strain females, from which the heterozygous daughters were retained. These daughters
were mated to dwarf males in 1980 to yield some dwarf
progeny used to supplement those few obtained from
the dwarf × dwarf matings. Resumption of full-pedigree
1510
COLE
matings in 1981 involved six males (hatched in 1979 or
1980) and 30 pullets selected from among 60 on the basis
of body weight, egg production for 3¹⁄₂ mo, and egg
weight. These breeders averaged 1,661 and 1,208 g in
body weight, respectively. Their progeny at 7¹⁄₂ mo of
age weighed, on average, 1,416 g (a range of 1,250 to 1,640
g) for 32 males, and 1,133 g (a range of 980 to 1,310 g)
for 118 females, 71 of which had an egg in the shell gland
at time of weighing.
TABLE 2. Production to 500 d of age by four
K-strain dwarf segregates
Weight at 1 yr of age
Hen
1
N 2792
P 1877
P 2255
Q 772
Egg no.
Eggs, g
Body, g
149
231
234
242
56.5
52.7
57.0
59.3
1,300
1,230
1,380
1,590
1
The capital letter indicates year of hatch: N = 1964, P = 1965, and Q
= 1966.
Length of Shank
By inspection and comparison with normal White Leghorns of a corresponding age, the dwarfs have shortened
shanks. For 71 dwarfs and 18 normal segregates at 5 mo
of age, mean shank lengths in live cockerels were 10.08
cm for dwarfs and 11.75 for normals, and the ranges were
9.4 to 11.3 cm for dwarfs and 11.3 to 12.1 cm for normals.
Conformation
When the dwarfs are held properly in one’s hand, with
keel resting on the palm and legs clasped between the
fingers, the compactness of the body is quite evident. The
shortness of the leg, from hip to foot, and the increased
relative size of muscles of the tibiotarsal region are similar
in birds that are dwarfed due to the dw gene.
Relative Shortening of the Leg Bones
The adw gene does not appear to have disproportionate
effect on the distal skeletal elements of the hind limb.
Based on measurements taken on two females and three
males, the ratios (× 100) for the length of the femur to
that of the tibiotarsus or to the tarsometatarsus in dwarfs
(142.5 and 105.0 for males, and 144.7 and 100.5 for females,
respectively) are similar to those for normal White Leghorns [144.3 and 99.2 for males, and 141.7 and 95.5 for
females, respectively, as reported by Hutt (1929)].
These data show that the autosomal dwarfs are proportionately reduced in size, as determined by the relative
length of the skeletal elements of the hind limb; therefore
they are quite different from some other dwarfs, such as
those resulting from the dw or Cp genes, in which the
more distal elements are affected to a greater degree
(Hutt, 1959). Based on these very limited data, the effect
of sex on the total length of the three major bones of the
hind limb causes those of the females to be 19% shorter
than those of the males, which is similar to the sex-dimorphism in normal birds (12 to 17%) as reported by Hutt
(1929).
EFFECT ON EGG PRODUCTION
AND EGG SIZE
The performance records for the four dwarfs subsequently recognized in the K-strain are given in Table 2.
Those for P 2255 demonstrate that the dwarfs could lay
rather well and have a combination of large eggs and
small body weight. The N 2792 female was not recognized
as a dwarf until late in the summer of 1965. When mated
to the original dwarf sire (N 991) in mid-October, this
hen laid 12 eggs that averaged 59.2 g in weight.
Once it was established that the dwarfism was a simple
genetic trait and more could be produced, a selection
program was started in an attempt to combine small body
size with good production of relatively large-sized eggs.
Selection was based on the records for the sibship and
for the individual female, usually for a period of 4.5± mo.
The data for the four selected generations are given in
Table 3.
There was some improvement in egg production, but
this resulted primarily from lowering the age at which
production commenced. There was no improvement in
rate of production after 1968, but the birds laid larger eggs
and did so even though body size had been decreased,
especially in 1971. The overall performance of the dwarfs
appears to have been improved as a consequence of selection.
As indicated previously, it is not proper to compare
production by the dwarfs with that by nondwarf stocks
because of differences in housing them as layers and in
the length of the test period. The dwarfs, also hatched
later in the spring, were therefore not exposed to the same
environmental conditions, especially length of day at the
time of approaching maturity. However, some data on
the performance of the K-strain compared with that of
dwarfs, are given in Table 4.
The rate of production by the dwarfs was not quite as
high as that of the normal-sized K-strain hens. The test
period (maximum days available for production) was 2
mo less for the dwarfs. Because rate of production normally declines with age, the rate for a period comparable
in length with that used for the K-strain would be less
than indicated in Table 4 for the dwarfs. Of the 292 dwarf
females that survived, only 20 were not laying in the last
10-d period of the test. Also, for a 28-d period in August,
1972, and beyond the 450-d test period, 79 living dwarf
hens laid at a rate of 54%.
From the available data, the author can, therefore, estimate that compared with the K-strain females, the dwarfs
would lay at a comparative rate of 90% and produce 87%
as many eggs in a test period to 500 d of age.
EFFECT ON REPRODUCTION
All matings were made by artificial insemination (AI).
The level of fertility was below that normally following AI
1511
AUTOSOMAL DWARFISM IN DOMESTIC FOWL
TABLE 3. Performance records for four generations of dwarfs
Year of hatch
Item
1968
1969
1970
1971
Females tested, no.
Length of test period, d
Females, completing test, no.
Mean age at first egg, d
Egg production, no.
Rate, from first egg, %
Egg weight at 10 to 11 mo, g
Body weight at 10 to 11 mo, g
72
436
70
175.7
167.9
63.8
54.6
1,481
70
444
68
182.2
165.3
67.21
55.3
1,404
75
450
75
180.7
174.7
66.01
57.5
1,419
80
450
79
174.8
183.5
67.1
56.6
1,345
1
One non-layer not included.
(1968, 90%; 1969, 90%; 1970, 82%; 1971, 78%). Hatchability
progressively declined over the four generations (1968,
79%; 1969, 72%; 1970, 58%; 1971, 52%).
A majority of the embryos that did not hatch had
pipped and were still alive on Day 22 of incubation. Inspection of such embryos and of chicks that did hatch
showed that the abdomen was distended beyond the degree normally seen in other stocks. Although the chicks
appeared to be normal in size, it was apparent that the
yolk sac was too large to be accommodated within the
body cavity. A measure of the relative size of the yolk
from unincubated eggs was calculated for 24 eggs sampled when the hens were about 13 mo of age. The eggs
averaged 58.45 g in weight, with a range from 52 to 79
g, and the yolk represented 29.7% of the egg weight, with
a range of 26.0 to 32.2%. The proportion of the egg that
was yolk is similar to that reported by Olsson (1936) for
hens (29.8%) and that reported for 58-g eggs (31.9%) by
Romanoff (1949). In general, the relative size of the yolk
declines slightly as the total weight of the egg increases.
Eggs for incubation were obtained from 22-mo-old
dwarf hens and paired for weight with eggs from the
Cornell K-strain as a control [the 103 available dwarfstrain eggs weighed an average of 59.93 g (a range of 51.0
to 69.6 g). For 11 of the very heavy eggs, it was not
possible to obtain K-strain eggs of comparable size]. The
control eggs, with a few exceptions, were of identical
weight, and did not deviate by more than 0.2 g. The
average weight for the 92 paired eggs was 59 g. Of these,
both eggs for 79 pairs contained live embryos on Day 19
of incubation. At that time, the eggs were transferred
to a refrigerator to kill the embryos, and subsequently
weights of the egg, embryo, and yolk sac were determined
to the nearest 0.05 g. These data are given in Table 5.
The findings confirmed the earlier observations. The
autosomal dwarf embryos (complete with yolk sac) were
an average of only 1.1 g (2.8%) smaller than K-strain
embryos from eggs of identical weights. However, the
embryos without the yolk sac were 2.4 g (or 8.5%) smaller
and had larger yolk sacs (1.3 g or 11.8%). These data
account for the distended abdomens of those chicks that
did hatch and for the abnormal number of embryos alive
on Day 22 of incubation, which, other than for a distended
abdomen, appeared to be normal. A smaller embryo is
thus required to accommodate a larger yolk sac within
its body cavity at hatching time. The dwarfism associated
with the adw gene is therefore expressed during the incubation period.
EFFECT ON VIABILITY
The autosomal dwarfs have excellent viability, which
is due to their origin from the K- and C-strains that had
been selected for viability (Cole and Hutt, 1973). Three
of the dwarf female breeders used in 1969 were derived
from a backcross of normal F1 females, produced by crossing C-strain dams with K-strain dwarf sires. When reared
with other birds of similar size, the mortality among females was negligible, as shown in Table 6.
Of the 37 discarded in 1968, 12 were not dwarfs, 15
had crooked toes or crossed beaks, and six came from a
dam whose definitive egg weight was considered to be
too low. In 1971, eight of the 10 pullets discarded had
either crooked toes or crossed beaks. Thirteen of the 15
TABLE 4. Egg production by dwarf and K-strain females that survived the test period
K-strain1
Dwarfs
Year
Age at
first egg,
d
Maximum
no.2
Actual
no.
Rate,
%
Age at
first egg,
d
Maximum
no.2
Actual
no.
Rate,
%
1967
1968
1969
1970
1971
167
162
170
...
...
333
338
330
...
...
237
232
219
...
...
71
69
66
...
...
...
176
182
181
175
...
260
262
269
275
...
168
165
175
184
...
65
63
65
67
1
Approximately 1,000 females per generation.
Length of the test period minus mean age of first egg.
2
1512
COLE
TABLE 5. Effect of autosomal dwarfism on embryonic development
Egg weight, g
Weight loss, g1
Embryo weight, g
Yolk sac weight, g
Yolk sac/embryo, weight, %
Difference
Dwarfs
K-strain
(control)
Actual
Percentage
59.00
7.50
25.99
12.43
47.8
59.00
8.53
28.39
11.12
39.2
0
−1.03
−2.40
+1.31
+8.6
0
−12.1
−8.5
+11.8
+21.9
1
During 19 d of incubation.
deaths during the period from 15 to 160 d of age were
caused by either cannibalism, perosis, or defects.
Another recessive dwarfism, considered a facultative
lethal, first described by Landauer (1929) and subsequently found in two other Rhode Island Red flocks, was
described by Hutt (1949). The genetic data from Upp, as
cited by Hutt (1949), indicated that the dwarfism was due
to homozygosity for a recessive gene (id). Obviously, it
was not the same mutation as adw. It might have been at
the same locus, because Landauer (1929) indicated that
they had enlarged heads. Both Leenstra and Pitt (1984)
and Ruyter-Spira et al. (1998a) cited this abnormality in
the adw autosomal dwarf broiler-sire line developed in the
Netherlands. Landauer (1929) also reported that Warren,
who had found a dwarfism similar to the one he found,
mentioned that curled toes were the only indication of
the dwarfism in the very young chicks. In the early generations of the dwarfism in the White Leghorns at Cornell,
a number of chicks showed curled toes at hatching, and
so they were not kept. If curled toes were observed at any
time during the growing period, the bird was discarded.
by Bernier and Arscott (1972), egg size can be increased,
but at the expense of an increase in body size.
The autosomal dwarfs perform similarly to the sexlinked dwarfs when compared with normal-sized controls. They may lay at a better rate with eggs of a larger
relative size, but again, this is at the expense of a larger
body. As indicated previously, the adw dwarfs were tested
in individual laying cages. This management practice normally results in a heavier body weight and larger eggs,
but at the expense of number of eggs. Even so, the adw
dwarfs, when compared with the K-strain for a 2-yr period when K-strain performance was at its peak, laid at
a rate similar to, or better than, that for sex-linked dwarfs
over a longer test period.
Both types of dwarfs require a few extra days to reach
maturity as measured by age at first egg. Consequently,
body weight taken at a common age just prior to commencement of production would tend to decrease the
estimated relative size of the dwarf, because the ovary
and oviduct need further development.
DISCUSSION
COMPARISON OF AUTOSOMAL AND
SEX-LINKED DWARFS
The sex-linked dw gene has been used by commercial
breeders to produce what was known as the “minifowl.”
It has also been used in female parents for the production
of normal broiler chicks, because they need less feed for
growth and hatching-egg production. The smaller size
allows more breeders to be used in a given area.
In general, based on limited reports, egg production is
reduced close to the level of 84.9% reported by Hutt
(1959). Reductions in egg and body weights are also similar to Hutt’s (1959) 90 and 70%, respectively. As shown
Unlike sex-linked dwarfism, the autosomal counterpart
causes a proportional reduction in body size that is first
expressed during embryonic development. Its detrimental effects on egg production and egg size are probably
related to the reduction in body size rather than to a
direct effect of the adw gene on these traits.
Whereas commercial chickens result from the crossing
of two or more unrelated strains, terminal mating is usually between normal-size females and dwarf males for
the production of the “minifowl,” and the reciprocal cross
could be used for the production of broiler chicks. In
both cases, the marked sex differences in body size may
TABLE 6. Mortality among female progeny from four generations
Year of hatch
Hatched, no.
Discarded, no.
Mortality, %
1 to 14 d
15 to 160 d
Tested, no.
Mortality to end of test, no.
1968
1969
1970
1971
Total
113
37
77
0
81
0
93
10
364
47
2
2
72
2
0
7
70
2
3
3
75
0
0
3
80
1
1.4
4.2
297
1.7
AUTOSOMAL DWARFISM IN DOMESTIC FOWL
handicap normal mating efficiency. Bernier and Arscott
(1972) were able to improve fertility by increasing the
number of males used in the breeding pens, but such a
practice is not in the best interests of efficient chick production.
The use of homozygous sex-linked dwarf males and
autosomal dwarf females should minimize the problem
of low fertility associated with marked sex differences in
body size. The effects of the adw gene would not be seen
in the progeny, but the effects of dw would be expressed
in the female offspring. However, intriguing as this may
be, the fact remains that such parental stocks would have
to excel in production traits and transmit that excellence
to their progeny. At the present stage in the development
of the autosomal-dwarf strain, its low level of hatchability
would make it unsuitable for use as a female parent strain.
However, the effect of the adw gene on the size of the
embryo in relation to the size of the yolk sac should not
be a problem in crosses with sex-linked dwarf males,
because the embryo would be Adw/adw. On the other
hand, a transfer of the adw gene to the strain used as the
sire of the broiler chick could be done. There, its effects on
strain reproduction would not be so serious economically,
because many fewer males than females are required for
commercial chick production.
The establishment of homozygosity for both adw and
dw in the same individual might result in an interesting,
bantam-type bird. The autosomal gene adw causes a proportional reduction in body size by approximately 30%.
Its effects on size are evident during the late incubation
period, when an 8% reduction in size, associated with a
larger-than-normal yolk sac, prevents many chicks from
hatching. The gene has no effect on viability after
hatching.
Compared with the K-strain of White Leghorns from
which it was derived, the dwarf stock requires 1 or 2 wk
more to reach age at first egg. Thereafter, the dwarf stock
lays at a rate of approximately 90% of that attained by
normal-size K-strain hens, and the eggs are 95% as large.
Actual production rate by survivors from first egg to an
age of 450 d was 65.5%, with adult egg and body weights
of 57.0 and 1,385 g, respectively.
SUBSEQUENT INFORMATION
The major portion of this report was prepared in 1973.
Following the opportunity to expand the stock in 1979,
the last paragraph of the Subsection “Body Weight” was
added in 1981. To make subsequent information available, additional data are now discussed.
According to Somes (1990), only six specific genes have
been identified that cause viable dwarfism. Five are sexlinked, and three of these are at the dw locus identified
by Hutt (1949). There have been many (200+) reports
covering studies of dwarfism in chickens, as per Cavney
(personal communication), but most of them involved the
sex-linked dwarfism.
Prior to 1973, many studies of the sex-linked dwarfs
dealt with the effects of the dw gene on the basic biology
1513
of the bird, including its use in meat-type stock. Several
reports were given at an International Symposium in
France (Calet, 1971).
Guillaume (1976) provided a very detailed report and
cited 142 references, some of which did not involve the
dw gene. Emphasis was placed on the effects of the dw
gene on body structure, growth, and performance as influenced by basic physiological and biochemical factors.
With development of new technologies, emphasis has
been placed on studies of specific DNA. Recognition of
sex-linked dwarfism that appears to be very similar to
the dw reported by Hutt (1949), has occurred at other
locations and has involved different breeds of chickens.
Dunnington and Siegel (1998) used a dwarf gene from
two different sources (USA and France), and showed that
the two genes were “not expressed in a discernible different way in terms of physiological measures.” It is possible
that these were from the same mutation [the one found
by Hutt (1949)]. The dwarf broiler stock listed as coming
from the USA population came from the Arbor Acres
Breeding Farm. This famous breeding organization could
have obtained the dw gene from Hutt, and might have
included it in a broiler parent line they sent to breeders
in Europe, as was common practice in the 1950s.
Burnside et al. (1991) found in a broiler line obtained
from Arbor Acres Farms that the dw gene involved a
mutation in the growth hormone receptor gene.
A study by Duriez et al. (1993) on a dwarf gene that
came from a commercial sex-linked dwarf Leghorn strain
in 1975 found that it involved the “last invariant amino
acid of the WS-like motif (amino acid sequence WS×WS)
common to all members of the cytokine receptor superfamily.“ Again, this mutation could have been the one
studied by Bernier that came from Kimber Farms. Kimber
Farms sold stock used to produce the K 137 commercial
Leghorn layers to breeders in Europe.
As indicated earlier, the dw gene found by Hutt appeared to be identical to the one found in the Kimber
stock. A male that had one sex chromosome carrying the
gene from one source (New Hampshire) and the other sex
chromosome carrying the gene from the second source
(Leghorn) was a typical dwarf.
Subsequent studies that involved the autosomal dwarf
are as follows: Because of Bernier’s interest in dwarfism,
hatching eggs from the autosomal dwarf stock were sent
to him in the early 1970s. Subsequently, he produced a
few hens that were both sex-linked and autosomal dwarf
(P. E. Bernier, 635 N. W. 34th Street, Corvallis, OR 97330,
personal communication, 1982). The combination of the
two types of dwarfism, compared with those dwarfed or
normal due to dw or adw, gave rise to a smaller mature
body weight (1,000 vs. 1,317 and 1,862 g, respectively),
and good egg production (189 vs. 175 and 193, respectively) and good egg weight (56.2 vs. 54.4 and 65.4 g, respectively).
Subsequently, he provided hatching eggs to Dr. Leenstra at the Spelderholt Centre in the Netherlands. She
transferred the adw gene to a line used as the sire of
broilers. When mated to sex-linked (dw) dwarf females
1514
COLE
(Leenstra and Pit, 1984), the progeny were essentially
normal in size. The dwarf line was discarded because of
high mortality, in both males and females, due to a leg
problem that was cited as “slipped tendon syndrome.”
This leg problem, also known as perosis, is related
to dietary level of manganese and is also influenced by
heredity. Leghorns normally need only 30 ppm of manganese, whereas New Hampshires need at least 50 ppm
but, in some cases, will develop perosis if given a diet
containing 100 ppm. Thus, the dwarf broiler parent line
developed by Leenstra, which resembled the Cornish line,
a heavy meat-type breed, may have been affected because
of a higher requirement for manganese.
Some of the autosomal dwarf Leghorn chicks showed
swollen hocks at hatching, and in the early years, a few
developed perosis during the growing period. A possible
biological problem related to manganese requirement
may have existed. Any such affected individual was discarded. In recent years, such problems have not been seen
in any of the chickens at Cornell.
Leenstra and Pit (1984) and Ruyter-Spira et al. (1998a)
indicated that these dwarfs, at least in the stock used in
the Netherlands, had enlarged heads. Abnormalities in
head shape or size have never been recognized in our
Leghorn strain of such dwarfs at Cornell.
Once the stock became available for basic biological
studies, it was used by J. A. Marsh, who reported:
The profile of those hormones known to be important
in the regulation of growth have been examined in the
autosomal dwarf strain and compared with the normalgrowing control K-strain. Growth hormone levels in the
autosomal dwarf strain and K-strains were monitored
from 2 to 18 wk and were found to be essentially the
same, except for slightly elevated levels found in the
autosomal dwarf strain after the peak growth period
(i.e., after 12 wk). Serum thyroxine (tetra-iodothyronine, or T4) levels were slightly depressed in the autosomal dwarf strain over the entire growth period,
whereas tri-iodothyronine (or T3) levels were depressed during the same time periods that GH levels
were elevated (Scanes et al., 1983). Insulin-like growth
factor-I (IGF-I) was examined by Huybrechts et al.
(1985) and was found to differ from the K-strain only
at the oldest age included (i.e., 18 wk of age).
There have been several examinations of immune activity within the autosomal dwarf strain. No differential
peripheral blood lymphocyte counts were found between K and autosomal dwarf strains at several different ages (Erf et al., 1987). There was an increased ability
of the autosomal dwarf strain, compared with the K
strain, to mount a graft-vs.-host response after 15 wk
of age. No difference was observed between the Kstrain and autosomal dwarf strain in either their primary or secondary antibody responses (Marsh, 1983;
Marsh et al., 1984).
The autosomal dwarfs developed and maintained at
Cornell were homozygous for the B15 haplotype. Their
source, the Cornell K strain, is also homozygous for B15.
The status of the K-strain, involving up to 15 sires and
140 dams used as breeders each year over a period of 30
yr, with respect to haplotype was never known. A major
question exists: why did the K-strain become homozygous for B15?
The locus for the adw gene on chromosome 1 is very
close to that for high-mobility group protein I-C and the
insulin-like growth factor 1, as determined by RuyterSpira et al. (1998a). In mice and humans, these two genes
are closely linked, and mutations in these genes are responsible for dwarfism in mice. No such mutations were
found in the genes in the autosomal dwarf chickens, as
was later determined by Ruyter-Spira (1998b).
The mature pullets (120) from the 1993 hatch were
evaluated by Austic (personal communication) for feed
conversion, in terms of the amount consumed vs. the
amount of egg material produced, over a period of 44
wk that commenced at an age of 23± wk. The results
indicated an efficient use of feed. The diet contained protein at 16.9% (Met, 0.36%; Lys, 0.76%) and had metabolizable energy at a level of 2,932 kcal/kg. The hen-day feed
consumption was 79 g vs. 110 g as currently recorded for
Babcock B-300. Feed conversion (kg feed/kg egg mass)
was 1.96 vs. 2.17 and 2.19 as cited by Heil and Hartmann
(1997) for the European Random Sample Tests in 1995
and 1996. In a subsequent test, for a short period, it was
found that increasing the level of dietary protein was
not effective.
SUBSEQUENT IMPROVEMENTS
The performance of the pedigreed populations produced through 1995 are given in Table 7. The evidence
indicates that these dwarfs are able to reproduce very
well and to lay a good number of relatively large eggs.
Genetic selection played a role in the improvement obtained, although there had been some inbreeding. The
breeding program also included attempts to limit the level
of inbreeding. Because only three males were involved in
matings made in 1979 to re-establish the stock, subsequent
matings involved closely related individuals. The same
phenomenon occurred in the 14 subsequent generations,
because only six sires could be used each year. In a few
cases, two of the six sires were half-brothers. Obviously,
more progress could have been attained if more breeders
could have been used, and with more progeny tested
for performance. Breeder selection, based on family and
individual performance, would have increased progress.
Selection for hatchability did include performance of
the family, because male chicks were retained from only
the two best families from the six dams mated to each
of the six sires. Some of the improvement shown in Table
7 resulted from changes in management. A delay in hatching due to the problem of the embryo getting the large
yolk sac into its body cavity led to some delay in pipping
the shell. The hatcher had to be used at a given time each
week and involved several different stocks under the
control of other people. The hatched and dried chicks
gave rise to dust blown about the hatcher, which created
problems for the dwarf embryos that were in the process
1515
AUTOSOMAL DWARFISM IN DOMESTIC FOWL
TABLE 7. Data on the Cornell autosomal dwarf line (adw)
Female progeny caged at 5¹⁄₂± mo
At 10+ mo
Year
of
hatch
Fertility,
%
Hatch,
%
1980
1981
1982
1983
1984
1985
1986
1987
1988
1989
1990
1991
1993
1995
...
78.0
83.0
76.4
89.6
83.2
81.4
75.7
82.8
73.3
78.8
85.5
94.9
93.6
...
68.6
58.9
62.7
49.4
66.1
70.3
65.1
83.22
86.5
87.8
86.8
87.0
80.9
Used as parents for the next generation
At 16± mo
At 10± mo
No.
Age at
first
egg
Production,
%
Egg
wt
g
Body
wt
g
Age,
d
Eggs,
no.
Mortality,
no.
60±
97
103
126
110
138
147
123
120
120
120
120
120
120
...
...
209
191
182
182
182
184
179
185
182
175
175
180
...
...
70.3
71.4
62.8
70.3
74.8
75.0
81.2
79.6
82.1
78.8
82.4
74.9
...
...
54.6
55.6
53.6
52.5
51.7
54.0
55.2
52.4
55.9
58.4
58.6
52.4
...
...
1,222
1,226
1,260
1,280
1,245
1,332
1,283
1,247
1,242
1,165
1,124
1,114
...
...
483
507
492
452
477
484
488
490
500
500
500
496
...
...
157.4
175.2
190.5
166.5
198.6
198.2
218.3
214.6
222.9
222.6
235.0
223.0
...
8
3
6
8
8
6
0
2
5
3
1
6
193
No.
Production,
%
Egg
weight,
g
Body
weight
g
Eggs at
16+ mo1
30
36
36
36
36
36
36
42
36
36
36
36
36
36
73.4
75.7
73.4
76.7
76.2
75.3
79.1
78.8
84.2
85.1
85.6
83.7
85.7
82.6
54.5
58.3
54.5
56.3
52.8
53.0
52.4
54.2
54.5
52.7
55.9
57.7
56.8
53.8
1,208
1,245
1,248
1,296
1,240
1,256
1,238
1,317
1,283
1,248
1,235
1,173
1,149
1,177
245.4
253.7
242.6
1
A major criterion for hens used as 2-yr-old breeders.
See note in text concerning management problems encountered in hatcher.
3
See note in text concerning unexpectedly high mortality in early 1996.
2
of getting out of the pipped egg. Using a hatcher that
was limited to the autosomal dwarfs gave better results
(1988). Because it takes longer for the dwarf chicks to
hatch, the problem can be helped by starting the incubation period 18 to 24 h earlier for eggs from the dwarf line,
especially if they are to be hatched in a hatcher used at
the same time for other stocks.
The exact cause of the poorer performance by the 1995
population is not known. The author had to give up
control of the stock on January 1, 1996, when the 1995
population was 37± wk old. At that time it was doing
well. Egg production for December was at a level of 82
vs. 83.5% for the previous generation. There had been no
mortality. The cause of the subsequent high mortality
was not determined. The existing records indicated that
the birds that died had laid reasonably well just before
death. The six that died by the 4th of the month had laid
an average of 21.7 eggs during the previous month. For
the 12 that died later in the month (the ninth to the 26th),
the production rate for that month, including day of
death, averaged over 52%.
ACKNOWLEDGMENTS
The author appreciates the efforts and interests of D.
D. Caveny in preserving special strains of chickens and
his desire that the history of the autosomal dwarf also be
retained. Credit is also given to H. S. Siegel for his detailed
help in making the current report meet the specifications
for publication.
REFERENCES
Bernier, P. E., and G. H. Arscott, 1960. Relative efficiency of sexlinked dwarf layers and their normal sisters. Poultry Sci.
39:1234–1235.
Bernier, P. E., and G. H. Arscott, 1972. Fifteen years of observations on the dwarf gene in the domestic fowl. Ann. Genet.
Sel. Anim. 4:183–215.
Burnside, J., S. S. Liou, and L. A. Cogburn, 1991. Molecular
cloning of the chicken growth hormone receptor and complementary deoxyribonucleic acid: Mutation of the gene in sexlinked dwarf chickens. Endocrinology 128:3183–3192.
Calet, C., 1971. Symposium on the dwarf (dw) gene in chickens.
World’s Poult. Sci. J. 27:276–292.
Cole, R. K., and R. E. Austic, 1980. Hereditary uricemia and
articular gout in chickens. Poultry Sci. 59:951–960.
Cole, R. K., and F. B. Hutt, 1973. Selection and heterosis in
Cornell White Leghorns: A review, with special consideration of interstrain hybrids. Anim. Breed. Abstr. 41:103–118.
Dunnington, E. A., and P. B. Siegel, 1998. Comparison of sexlinked dwarf genes in chickens from two sources when introgressed into unrelated backgrounds. Br. Poult. Sci. 39:216–
220.
Duriez, B., M. L. Sobrier, P. Duquesnoy, M. Tixier-Boichard, E.
Decuypere, G. Coquerelle, M. Zeman, M. Goossen, and S.
Amselem, 1993. A naturally occurring growth hormone receptor mutation: In vivo and in vitro evidence for the functional importance of the WS motif common to all members
of the cytokine receptor superfamily. Mol. Endocrinol.
7:806–814.
Erf, G. E., W. E. Briles, and J. A. Marsh, 1987. Graft-versus-host
response in sex-linked dwarf, autosomal dwarf, and control
K strain chickens. Dev. Comp. Immunol. 11:769–779.
Godfrey, E. F., 1953. The genetic control of growth and adult
body weight in the domestic fowl. Poultry Sci. 32:248–249.
Goodwin, K., 1961. Effect of hatching egg size and chick size
upon subsequent growth rate in chickens. Poultry Sci.
40:1408–1409.
Guillaume, J., 1976. The dwarfing gene dw: Its effects on anatomy, physiology, nutrition, management. Its application in
poultry industry. World’s Poult. Sci. J. 32:285–304.
Heil, G., and W. Hartmann, 1997. Combined summaries of European Random Sample Egg Production Tests completed in
1995 and 1996. World’s Poult. Sci. J. 53:291–296.
Hutt, F. B., 1929. Sex dimorphism and variability in the appendicular skeleton of the Leghorn fowl. Poultry Sci. 8:202–218.
Hutt, F. B., 1949. Genetics of the Fowl. McGraw-Hill Book Co.,
Inc., New York, NY.
1516
COLE
Hutt, F. B., 1959. Sex-linked dwarfism in the fowl. J. Hered.
50:209–221.
Huybrechts, L. M., D. B. King, T. J. Lauterio, J. A. Marsh, and
C. G. Scanes, 1985. Plasma concentrations of somatomedin
C in hypophysectomized dwarf and intact growing domestic
fowl as detected in heterologous radioimmunoassay. J. Endocrinol. 104:233–239.
Jaap, R. G., 1971. Effect of sex-linked genes on body size and
reproduction. World’s Poult. Sci. J. 27:281–282.
Jull, M. A., and J. P. Quinn, 1931. The inheritance of body weight
in the domestic fowl. J. Hered. 22:283–294.
Kaufman, L., 1948. Sex-linked inheritance of body weight in
fowls. Pages 291–296 in: Proceedings of the 8th World’s Poultry Congress (E). Nielsen & Lydiche, Copenhagen, Denmark.
Landauer, W., 1929. Thyrogenous dwarfism (myxoedema infantilis) in the domestic fowl. Am. J. Anat. 43:1–43.
Leenstra, F. R., and R. Pit, 1984. The autosomal dwarf as broiler
sire mated to normal and sex-linked dwarf dams: Performance of progeny. Pages 140–142 in: The XVII World’s Poultry Congress Proceedings. WPSA, Helsinki, Finland.
Marsh, J. A., 1983. Assessment of antibody production in sexlinked and autosomal dwarf chickens. Dev. Comp. Immunol.
7:535–544.
Marsh, J. A., W. C. Gause, S. Sandhu, and C. G. Scanes, 1984.
Enhanced growth and immune development in dwarf chickens treated with growth hormone and thyroxin. Proc. Soc.
Exp. Biol. Med. 175:351–360.
Maw, A.J.G., 1935. The inheritance of skeletal dimensions in the
domestic fowl. Sci. Agric. 16:85–112.
Olsson, N., 1936. Studies on some physical and physiological
characters of hen’s eggs. Pages 310–320 in: Proceedings of
the 6th World’s Poultry Congress (Leipzig). WPSA, Berlin,
Germany.
Rajaratnam, G., J. D. Summers, E. T. Moran, and A. S. Wood,
1971. Effect of thyroprotein on performance of dwarf layers.
Can. J. Anim. Sci. 51:217–223.
Romanoff, A. L., and A. J. Romanoff, 1949. The Avian Egg. John
Wiley & Sons, New York, NY.
Ruyter-Spira, C. P., A.J.C. deGroof, J. J. van der Poel, J. Herbergs,
J. Masabanda, R. Fries, and M.A.M. Groenen, 1998a. The
HMGI-C gene is a likely candidate for the autosomal dwarf
locus in the chicken. J. Hered. 89:295–300.
Ruyter-Spira, C. P., J. Herbergs, E. Limpens, J. A. Marsh, J. J.
van der Poel, T.A.Y. Ayoubi, and M.A.M. Groenen, 1998b.
Nucleotide sequence of the chicken HMGI-C cDNA and expression of the HMGI-C and IGF1 genes in autosomal dwarf
chicken embryos. Biochim. Biophys. Acta 1339:83–87.
Scanes, C. G., J. Marsh, E. Decuypere, and P. Rudas, 1983. Abnormalities in the plasma concentration of thyroxine, tri-iodothyronine and growth hormone in sex-linked dwarf and autosomal dwarf White Leghorn domestic fowl (Gallus domesticus). J. Endocrinol. 97:127–135.
Somes, R. G., Jr., 1990. Mutations and major variants of muscles
and skeletons in chickens. Pages 230–232 in: Poultry Breeding
and Genetics, R. D. Crawford, ed. Elsevier, Amsterdam,
The Netherlands.
Summers, J. D., 1972. Nutrition of dwarf layers. Ann. Genet.
Sel. Anim. 4:251–258.
van Tienhoven, A., J. H. Williamson, M. C. Tomlinson, and K.
MacInnes, 1966. Possible role of the thyroid and the pituitary
glands in sex-linked dwarfism in the fowl. Endocrinology
78:950–957.