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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. 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