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Single genes for fecundity in Icelandic sheep
Chapter 17
Single genes for fecundity in Icelandic sheep Jon V. Jonmundsson THE AGRICULTURAL SOCIETY, 127 REYKJAVIK, ICELAND
and Stefan Adalsteinsson
THE AGRICULTURAL RESEARCH INSTITUTE, KELDNAHOLT, 110 REYKJAVIK, ICELAND
Introduction Fecundity is the most important economic trait in Icelandic sheep breeding. Greater fecundity also increases the realized selection differentials in other traits because the superiority is present in a greater number of progeny than before. It is well known that sheep breeds differ markedly in fecundity (Bradford, 1972). The heritability of number of lambs born per ewe lambing is usually below 0.15 (Turner and Young, 1969; Bradford, 1972; Land, Atkins and Roberts, 1983) but comprehensive Icelandic investigations have consistently resulted in higher values in the range 0.15-0.21 (Hallgrimsson, 1966; Adalsteinsson, 1971; Jonmundsson, 1977; Jonmundsson, Adalsteinsson and Steingrimsson, 1977). It is generally assumed that the genetic effect on sheep fecundity consists of the additive effect of a multitude of genes, each with a small and non-measurable effect. Litter size has a discrete distribution, and the ewe has to reach a certain threshold value in order to respond by an increase of one lamb. The trait as observed is therefore a qualitative trait, while the mode of inheritance of the underlying trait is assumed to be comparable to the inheritance of quantitative traits.
Known effects of single genes on fecundity Many lethal or sublethal genes are known in sheep which result in the death of embryos and lowered fecundity (Rae, 1956; Saperstein, Leipold and Dennis, 1975; Dennis and Leipold, 1976). Embryonic losses in adult ewes during the first weeks of pregnancy are estimated to be 15-30% (Edey, 1969; 1979) and still higher in 1-year-old ewes (Quirke, Adams and Hanrahan, 1983). Lethal genes are, however, not assumed to play a large part in embryonic losses in sheep. Bruere (1974) gave an account of chromosomal aberrations in sheep and suggested that they might be the cause of a large proportion of embryonic losses, although these aberrations need not be inherited. Glahn-Luft and Wassmuth (1980) reported a 1/20 translocation in sheep which resulted in lowered fertility in 159
160
Single genes for fecundity
in Icelandic
sheep
normal ewes when they were mated to affected rams, and a still greater fertility reduction when affected animals were mated inter se. Adalsteinsson and Hallgrimsson (1977) reported on the effect of a few rams which seriously depressed the fertility of their normal mates. This effect was clearly inherited, because it was observed in the sons of affected rams. They estimated the embryonic losses due to this effect to have been 41-53% in comparison with normal rams. Cryptorchidism caused by simple inheritance is known in sheep (Rae, 1956). A combined effect of cryptorchidism in male progeny and infertility in daughters which was reported by Hämori (1964) is probably different from the most common cryptorchidism. The Ke gene which determines the amount of potassium in sheep erythrocytes has been shown to affect lamb mortality (Rasmusen, 1975). The haemoglobin type has been shown to affect ewe fecundity and lamb mortality (Purser and Hall, 1974). In his investigation on colour inheritance in sheep, Adalsteinsson (1970) found an effect of colour genes on ewe fecundity, where white ewes showed a lower fecundity than non-white ewes. Table 17.1 shows a summary of the results from investigations where this effect has been studied. The effect from the various investigations shown in Table 17.1 are marked and remarkably consistent. TABLE 17.1. Observed difference in fecundity of white and non-white ewes Author
Breed
Lambs born per ewe Non-white — white
Davidsson (1966) Adalsteinsson (1970) Adalsteinsson (1975) Dyrmundsson and Adalsteinsson (1980) Kurowska and Danell (1982) Ricordeau έ'ί«/. (1982)
Icelandic Icelandic Icelandic Icelandic Finewool Landrace Berrichon du Cher x Romanov
0.16 0.15 0.15 0.18 0.18 0.11
Adalsteinsson (1984) showed that this effect seems to be a negative effect of the Awh gene on fecundity. He found the effect of the ^^-allele to be strictly additive in 3- and 4-year-old ewes, the heterozygotes showing only half as much fecundity depression as the homozygotes; the depression in homozygous white 3- and 4-year-old ewes was 0.23 lambs born per ewe. The additivity of the effect of the /l^-allele results in a biased comparison when white ewes as a group are compared to non-white ewes, the bias depending on the proportion of heterozygous white ewes entering the comparison. Icelandic investigations have also shown a marked effect of colour genes on the frequency of out of season lambing. Out of season lambing has a much higher frequency among non-white ewes (Dyrmundsson and Adalsteinsson, 1980). This may indicate an effect of colour genes on the level of sex hormones. The single gene effects on fecundity which have been summarized in the foregoing are, without exception, negative. The opposite is the case with the effect of a gene found in Booroola Merinos in Australia. Piper and Bindon (1982) report that the high fecundity in these sheep can be explained by the presence of a single major gene with an effect which seems to be around three standard deviations. Turner (1982) described the origin of these sheep and reported on how an extremely high fecundity was retained for a long time in these sheep by selection on the dam side only.
Single-gene criterion and segregation tests
161
The sheep in Borgarhoefn County in Iceland In light of the recent findings on the inheritance of litter size in the Booroola Merinos, we concentrated our efforts on searching for a similar phenomenon in Icelandic sheep, particularly at the Sheep Breeding Association of the Borgarhoefn County, where the ratio of ewes with three and four lambs has been appreciably higher than in other sheep breeding associations in Iceland. It was soon discovered that the pedigree of almost all ewes with multiple births could be traced to the ewe Thoka, at the farm Smyrlabjoerg. Thoka was born in 1950. According to oral information, Thoka's granddam gave birth to triplets around 1940. This was at that time unheard of there; ewes with twins were a rarity in this area at that time. Production records of Thoka are unfortunately not available, but it is known that she had triplets at least twice. One son of Thoka, Tossi 58165, was kept for breeding; (the first two digits in the number are the birth year). Tossi was used on the farm Borgarhoefn, a neighbour ing farm to Smyrlabjoerg. In the present investigation, information was collected on the number of lambs born from all ewes on record in the Borgarhoefn flock in the period 1961-1983. Until 1973, only part of the ewe flock at Borgarhoefn was recorded, but since 1974 all the ewes in the flock have been recorded. TABLE 17.2. Distribution of ewes in the Borgarhoefn flock on number of lambs at birth during the period 1974-1983. The sheep breeding associations are shown for comparison Source of ewes
Borgarhoefn Sheepbreeding associations
Number of lambs
Number
% %
/
2
3
4
506 27.0 32.3
1193 63.6 66.3
163 8.7 1.4
14 0.7 0.0
The period under study covers 537 recorded ewes. Table 17.2 shows the distribution of litter size of the ewes in Borgarhoefn during the period 1974-1983 and of all other ewes in the sheep breeding associations in the country during the same period. The distribution of the Borgarhoefn ewes differs significantly from the rest of the country. It is noticeable that a much larger proportion of ewes with triplets and quadruplets occur in the Borgarhoefn flock than in the rest of the country.
Single-gene criterion and segregation tests In a further analysis of the data from the Borgarhoefn flock, a comparable method to that used in the Booroola studies was employed (Piper and Bindon, 1982; Davis et al., 1982). Ewes that have given birth to triplets at least once are assumed to carry a high fecundity gene (^4 - ewes). Ewes that have never had more than two lambs are referred to as B - ewes. During the period under study five rams which seem to have carried the high fecundity gene, occurred in the Borgarhoefn flock. All could be traced back to Thoka at Smyrlabjoerg, the first known carrier of the high fecundity gene.
162
Single genes for fecundity
in Icelandic
sheep
TABLE 17.3. Average litter size of daughters of A-rams in the Borgarhoefn flock, classified by status of dam and whether they have had at least one set of triplets Sire
A-dams A -daughters
58165 66285 69281 71325 72367 No. and average
B -daughters
Litter size
No. 0 1 1 2 2 6
B-dams
Litter size
No. 0 0 1 0 0 1
2.22 2.00 2.21 2.24 2.17
A -daughters
1.67 1.67
B-daughters
No.
Litter size
No.
Litter size
13 4 11 3 9 40
2.34 2.65 2.35 2.35 2.31 2.36
19 5 11 2 9 46
1.65 1.83 1.82 2.00 1.65 1.72
Table 17.3 shows the litter size of the daughters of the five A - sires. The daughters have been separated into two groups, i.e. those having A - dams and those having B - dams. In each of the two groups the daughters have been further classified with respect to their own fertility status as either A - or B - daughters. The classification of the daughters in Table 17.3 is in excellent agreement with the hypothesis that all the sires in question carried a high fecundity gene in the heterozygous state. Only seven of the daughters have dams of type A. Among these daughters, some should be homozygous, but none of them show an excessively high fecundity. The difference in fecundity between A - and B - daughters is on the average 0.64 lambs born (Table 17.3). This difference indicates that the effect of the gene behind this trait is at least two standard deviations. The ^4-ewes in the investigation have had on average 6.8 years on record compared with 6.1 years for the B - ewes. These records do not include the number of lambs at 1 year of age. These results do not indicate that the high fecundity gene adversely affects the A - ewes. Of the 241 records of multiple births in the flock at Borgarhoefn, all except one could be traced back to the five rams descended from Thoka. When the descendants of the oldest ram, Tossi 58165, were traced for three generations, the results shown in Figure 17.1 were obtained. That the high fecundity under study is due to a single major gene is further borne out by the segregation results where a 1:1 ratio of A:B ewes is observed in accordance with expectation, as well as by the fact that the effect of the postulated high fecundity gene remains unchanged for three generations of outcrossing. TABLE 17.4. Number of times a ewe gives multiple birth classified according to her age at the first multiple birth Age at first multiple birth
Number of times with ^ 3 lambs 1
2 3 4 5 6 7 8 Total
1 2 3 4 3 2 1 16
2
3 2 4 6 1 1
3 3 1
4
5
6
7
8
Total
4 2
3 1
3
1
1
5
1
1
18 14 10 6 7 3 1 59
2
1 3 1
14
11
7
4
163
^£TL J νάΓΝ
B 9?
J A£^ 2-2.26
1-1.67
A
/ f \J
Ϋ
? 9
13-2.34
B£^ 2-1.25
10-2.49 | \
ACTCT K l\1 B££ 1-1.57
J A 9 9 5-2.25 B
3<&
Ί Β99 10-1.81
B?? 10- 1.62
χι
Acf x A ?9
&6ό y J
A99 2-2.44
BrfJJ-J
B99 6-1.53
BC#L J B99 2-1.65
4-2.65
Α(&
B?9
B??
19-1.65
2-1.67 A 99
Bdcf
1-2.00
Α ^ φ 1-2.43
A
B99l·· 11-1.68 \\ 3C&
N B99 1-1.57 BJ9 3-1.10
Unexpected
Figure J 7.1 The high fecundity condition in the Borgarhoefn flock traced for three generations. The /i-male on the left is Tossi 58165. He was only mated to ß-females. His daughters, granddaughters and greatgranddaughters are shown classified into A and B females and also classified according to whether their sire was of type A or B. The number of daughters of each type and their average litter size in each generation is shown in each female box
164
Single genes for fecundity
in Icelandic
sheep
Only one ewe in Figure 17.1 was classified as an A - ewe while having both parents of type B. This ewe gave birth to one set of triplets as an adult. Table 17.4 summarizes the results of the A - daughters of the five rams in Table 17.3, together with the appropriate descendants of ram 58165 in Figure 77.i.The ewes are classified with respect to the number of times they have had three or more lambs according to the age at which they first had a multiple birth. The ewes are on average 3.7 years old when they first give birth to three or more lambs, and on average they give birth to three or more lambs 2.9 times. It should be borne in mind that some of these ewes are still alive, and a few of them started in the recording scheme at an adult age.
Heritability estimate, and records of one-year-old ewes The available data are somewhat limited for heritability estimation. The heritability of litter size was estimated in the Borgarhoefn material, on 1072 records from 417 ewes, in the age classes 2-4 years, out of 58 sires. The heritability was found to be 0.16±0.07, and the repeatability 0.32±0.03. These results agree well with previous heritability estimates on Icelandic data, but the repeatability estimate in the present study is appreciably higher, as one would expect (Jonmundsson, Adalsteinsson and Steingrfmsson, 1977). Only a certain proportion of the ewe lambs in the Borgarhoefn flock is mated during their first winter. Furthermore, lambing records for ewe lambs in the flock are only available for the last few years. TABLE 17.5. Number of lambs born at 1 year of age to ewes classed A- or Bin later records Ewe type
Number of lambs at one year of age 1 2
,4-ewe ß-ewe
9 98
9 11
Table 17.5 shows the fecundity at 1 year of age of the A - and B - ewes which have lambing records at that age. These limited data show a significantly higher twinning rate at 1 year of age in the A - ewes. Studies on the fecundity records in the sheep breeding associations have shown a clear connection between twinning at 1 year of age and occurrence of multiple births in adult life (Jonmundsson, 1982).
Miscellaneous information on the high fecundity condition The high fecundity has, if anything, been selected against in the Borgarhoefn flock. For that reason there are fewer A - ewes in the younger age classes than in the older ones. A few rams have been sold from the flock to neighbouring flocks and, in many cases, high fecundity has occurred in these flocks when the daughters of the bought-in rams matured. Almost all examples of quintuplets and sextuplets in Icelandic ewes can be traced to this high fecundity strain of sheep. In the Smyrlabjoerg flock where Thoka, the ewe of origin, was born, a strain of highly fecund ewes has been maintained by consecutive breeding for daughters of high fecundity ewes.
The high fecundity sheep at Skriduklaustur
165
Lambing record at age 2 - 1 0 years
O Thoka
1
Q
Rispa
3 - 2 - 3 - 1 - 3 - 3 - 3 - 3
Q
Brenna
2 - 3 - 3 - 2 - 2 - 2 - 3
1 1 I
Q Katla 70302
3 _ 3 _ 2 - 4 - 3 - 4 - 4 - 4 - 3
0
2 - 4 - 3 - 4 - 4 - 4 - 3 - 1
Prila 73034
>1
_J O
Angi 79608
Age of daughters
\
Number of lambs 2 3
4
x
1
16
16
3
2
2
23
11
3
2.38
4
4
2
2.80
3
1.63
Figure 17.2 The line of female ancestry between the ewe Thoka at Smyrlabjoerg and the ram Angi 79608, with their lambing records. The lower part of the figure shows the litter size of the daughters of Angi 79608 at 1, 2 and 3 years of age
The pedigree of one ram, no. 79608, is shown in Figure 17.2, together with the available information on the fecundity of his daughters up to the age of 3 years. As the figure shows the daughters of this ram show an outstanding fecundity. Ram 79608 was mated to A - ewes. In the spring of 1983, seven of his daughters were barren because they have never shown heat. All these ewe are out of large litters of A - dams. This phenomenon needs further investigation because these ewes could possibly be the first ewes which are homozygous for the high fecundity gene. Owen (1982) reported a similar phenomenon in the high fecundity Cambridge sheep and suggested that it was due to a prenatal effect.
The high fecundity sheep at Skriduklaustur In autumn 1976 an experiment on breeding a strain of high fecundity sheep was initiated at the Experimental Station, Skriduklaustur by collecting lambs out of
166
Single genes for fecundity in Icelandic sheep
high fecundity ewes. The procedure was similar to that adopted in several other countries in the preceding years, as described by Land, Atkins and Roberts (1983). Some of the experimental lambs were bought in from the flocks at Smyrlabjoerg and Borgarhoefn. At that time we were not aware of the mode of inheritance of this high fecundity, and the selection was not based on that principle. Up to now only limited selection has been carried out within the high fecundity strain, the main objective having been performance recording of individuals. Few records are available, but the daughters of classed ewes show a separation into two groups which agrees well with the hypothesis that their dams are heterozygous for a major fecundity gene. One of the bought-in ewes in the experiment has shown an exceptional fecundity. She had triplets at 1 year of age and from three to five lambs per lambing since then, the average being 3.83 lambs per year in 6 years of adult life. In autumn 1982 the testis weight of ram lambs from the Skriduklaustur flock was recorded at around 120 days. Sires from the high fecundity strain sired ram lambs with significantly heavier testicles, 257 g (84 lambs) compared with 226 g (163 lambs) for the progeny of other sires. It is not known whether the rams in the high fecundity strain carry the major gene under study. We propose to refer to the gene described as the Thoka gene in reference to the ewe Thoka, the first known carrier.
The utilization of the high fecundity gene It is obvious that through proper utilization of a gene with as large effect as that described here, a marked increase in ewe fecundity can be achieved in a relatively short time. Much research on the condition is needed, however, and some of the items needing further investigation will be pointed out in the following. In the material described here it has not been possible to find individuals which can be classified as homozygous. The breeding carried out so far has not been aimed at producing such individuals. However, until such individuals are identified nothing can be deduced about the dominance or additive effects of the gene. At present the only way to establish whether a ram carries the gene is to test his daughters. There, it is of importance to find out how early in the life of the daughter the condition manifests itself. The daughters of ram no. 79608 shown in Figure 17.2 indicate that the condition is partly visible at 1 year of age. The possibility of finding methods to select rams for breeding on their own phenotype should be investigated, such as selection on testis size, hormonal level, etc. The measure of fecundity in the present investigation has been number of lambs born. Lamb mortality in this strain should be investigated further. The owners of the sheep under study indicate, however, that this is not a serious problem. It is of interest to study the effect of the high fecundity gene in ewes of different colours. The foundation ewe, Thoka (means Fog), was of grey colour, and grey as well as other non-white colours are frequent in this strain. Hanrahan's hypothesis about the relationship between number of ova shed and number of lambs born is of particular interest in this connection (Hanrahan, 1980; Hanrahan and Piper, 1982). From this hypothesis it must be assumed that separation of homozygous and heterozygous ewes is very difficult on the basis of number of lambs born. It therefore seems of great importance to initiate studies on
The utilization
of the high fecundity
gene
167
ovulation rate in ewes of this strain in order to be able to assess the behaviour of the trait more accurately. At present very few rams seem to be carriers of the high fecundity gene, ram no. 79608 being the only one which is known with certainty to be a carrier. It seems highly relevant to take such rams into insemination stations in order to distribute the condition more widely. In the Borgarhoefn county there are now between 100 and 200 ewes which are assumed to carry the gene. In order to ensure the best possible utilization of the gene these ewes should be mated extensively to elite rams at the artificial insemination stations. Their sons should then be retained for breeding and taken through a planned progeny testing scheme. It is of great importance to widen the breeding base before pure-breeding within the strain is started. It is clear that several traits in addition to the high fecundity condition have to be included in the breeding stock in order to secure general utilization of this important gene in practical sheep breeding in Iceland. Acknowledgement We want to express our thanks to the farmers in the Borgarhoefn County who provided information on the high fecundity condition. Particular thanks are due to the farmers Ragnar Sigurdsson, Borgarhoefn and Karl Bjarnason, Smyrlabjoerg. References ADALSTEINSSON, S. (1970). Journal of Agricultural Research in Iceland, 2, 3-135 ADALSTEINSSON, S. (1971). Journal of Agricultural Research in Iceland, 3, 28-38 ADALSTEINSSON, S. (1975). Annales de Genetique et de Selection animale, 7, 445-447 ADALSTEINSSON, S. (1984). First World Congress on Coloured Sheep and Their Products, New Zealand, edited by H.T. Blair, pp. 237-241 ADALSTEINSSON, S. and HALLGRf MSSON, S. (1977). Journal of Agricultural Research in Iceland, 9, 77-82 BRADFORD, G.E. (1972). Journal of Reproduction and Fertility, Suppl. 15, 23-41 BRUERE, A.N. (1974). Proceedings of the First World Congress on Genetics Applied to Livestock Production, 1, 151-175 DAVIDSSON, J. (1966). Freyr, 62, 15-17 DAVIS, G.H., MONTGOMERY, G.W., ALLISON, A.J., KELLY, R.W. and BRAY, A.R. (1982). New Zealand Journal of Agricultural Research, 25, 525-529 DENNIS, S.M. and LEIPOLD, H.W. (1976). Zughthygiene, 11, 105-112 DYRMUNDSSON, O.R. and ADALSTEINSSON, S. (1980). Journal of Heredity, 71, 363-364 EDEY, T.N. (1969). Animal Breeding Abstracts, 37, 173-190 EDEY, T.N. (1979). In Sheep Breeding, 2nd edn, edited by G.J. Tomes, D.E. Robertson, R.J. Lightfoot and W. Haresign, pp. 315-325. London: Butterworths GLAHN-LUFT, B. and WASSMUTH, R. (1980). Proceedings EAAP, Sheep and Goat Commission, München HALLGRf MSSON, S. (1966). Thesis for Licentiate in Agriculture, Agricultural University of Norway HÄMORI, D. (1964). Allatenyesztes, 13, 133-140 HANRAHAN, J.P. (1980). Proceedings of the Australian Society of Animal Production, 13, 405-408 HANRAHAN, J.P. and PIPER, L.R. (1982). Proceedings EAAP, Sheep and Goat Commission, Leningrad JONMUNDSSON, J.V. (1977). Journal of Agricultural Research in Iceland, 9, 31-42 JONMUNDSSON, J.V. (1982). Freyr, 78, 578-579 JONMUNDSSON, J.V., ADALSTEINSSON, S. and STEINGRIMSSON, J.T. (1977). Journal of Agricultural Research in Iceland, 9, 50-62 KUROWSKA, Z. and DANELL, Ö. (1982). Färskötsel, 62, 14-15 LAND, R.B., ATKINS, K.D. and ROBERTS, R.C. (1983). In Sheep Production, edited by W. Haresign, pp. 515-535. London: Butterworths OWEN, J.B. (1982). Proceedings EAAP, Sheep and Goat Commission, Leningrad
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PIPER, L.R. and BINDON, B.M. (1982). Proceedings of the World Congress on Sheep and Beef Cattle Breeding, 1, 395-400 PURSER, A.F. and HALL, J.G. (1974). Proceedings of the British Society of Animal Production, 3, 95 QUIRKE, J.F., ADAMS, T.E. and HANRAHAN, J.P. (1983). In Sheep Production, edited by W. Haresign, pp. 409-429. London: Butterworths R A E , A.L. (1956). Advances in Genetics, 8, 189-265 RASMUSEN, B.A. (1975). In Handbook of Genetics, 4, edited by R.C. King, pp. 447-457. New York: Plenum Press RICORDEAU, G., TCHAMITICHIAN, L., RAZUNGLES, J., LEFEVRE, C. and BRUNEL, J.C. (1982). 2nd World Congress on Genetics Applied to Livestock Production. Madrid, VII, 596-598 SAPERSTEIN, G., LEIPOLD, H.W. and DENNIS, S.M. (1975). Journal of American Veterinary Medical Association, 167, 314-322 TURNER, H.N. (1982). In The Booroola Merino, edited by L.R. Piper, B.M. Bindon and R.D. Nethery, pp. 1-7. Melbourne: CSIRO TURNER, H.N. and YOUNG, S.S.Y. (1969). Quantitative Genetics in Sheep Breeding. Ithaca, New York: Cornell University Press
Single genes for fecundity in Icelandic sheep Jon V. Jonmundsson THE AGRICULTURAL SOCIETY, 127 REYKJAVIK, ICELAND
and Stefan Adalsteinsson
THE AGRICULTURAL RESEARCH INSTITUTE, KELDNAHOLT, 110 REYKJAVIK, ICELAND
Introduction Fecundity is the most important economic trait in Icelandic sheep breeding. Greater fecundity also increases the realized selection differentials in other traits because the superiority is present in a greater number of progeny than before. It is well known that sheep breeds differ markedly in fecundity (Bradford, 1972). The heritability of number of lambs born per ewe lambing is usually below 0.15 (Turner and Young, 1969; Bradford, 1972; Land, Atkins and Roberts, 1983) but comprehensive Icelandic investigations have consistently resulted in higher values in the range 0.15-0.21 (Hallgrimsson, 1966; Adalsteinsson, 1971; Jonmundsson, 1977; Jonmundsson, Adalsteinsson and Steingrimsson, 1977). It is generally assumed that the genetic effect on sheep fecundity consists of the additive effect of a multitude of genes, each with a small and non-measurable effect. Litter size has a discrete distribution, and the ewe has to reach a certain threshold value in order to respond by an increase of one lamb. The trait as observed is therefore a qualitative trait, while the mode of inheritance of the underlying trait is assumed to be comparable to the inheritance of quantitative traits.
Known effects of single genes on fecundity Many lethal or sublethal genes are known in sheep which result in the death of embryos and lowered fecundity (Rae, 1956; Saperstein, Leipold and Dennis, 1975; Dennis and Leipold, 1976). Embryonic losses in adult ewes during the first weeks of pregnancy are estimated to be 15-30% (Edey, 1969; 1979) and still higher in 1-year-old ewes (Quirke, Adams and Hanrahan, 1983). Lethal genes are, however, not assumed to play a large part in embryonic losses in sheep. Bruere (1974) gave an account of chromosomal aberrations in sheep and suggested that they might be the cause of a large proportion of embryonic losses, although these aberrations need not be inherited. Glahn-Luft and Wassmuth (1980) reported a 1/20 translocation in sheep which resulted in lowered fertility in 159
160
Single genes for fecundity
in Icelandic
sheep
normal ewes when they were mated to affected rams, and a still greater fertility reduction when affected animals were mated inter se. Adalsteinsson and Hallgrimsson (1977) reported on the effect of a few rams which seriously depressed the fertility of their normal mates. This effect was clearly inherited, because it was observed in the sons of affected rams. They estimated the embryonic losses due to this effect to have been 41-53% in comparison with normal rams. Cryptorchidism caused by simple inheritance is known in sheep (Rae, 1956). A combined effect of cryptorchidism in male progeny and infertility in daughters which was reported by Hämori (1964) is probably different from the most common cryptorchidism. The Ke gene which determines the amount of potassium in sheep erythrocytes has been shown to affect lamb mortality (Rasmusen, 1975). The haemoglobin type has been shown to affect ewe fecundity and lamb mortality (Purser and Hall, 1974). In his investigation on colour inheritance in sheep, Adalsteinsson (1970) found an effect of colour genes on ewe fecundity, where white ewes showed a lower fecundity than non-white ewes. Table 17.1 shows a summary of the results from investigations where this effect has been studied. The effect from the various investigations shown in Table 17.1 are marked and remarkably consistent. TABLE 17.1. Observed difference in fecundity of white and non-white ewes Author
Breed
Lambs born per ewe Non-white — white
Davidsson (1966) Adalsteinsson (1970) Adalsteinsson (1975) Dyrmundsson and Adalsteinsson (1980) Kurowska and Danell (1982) Ricordeau έ'ί«/. (1982)
Icelandic Icelandic Icelandic Icelandic Finewool Landrace Berrichon du Cher x Romanov
0.16 0.15 0.15 0.18 0.18 0.11
Adalsteinsson (1984) showed that this effect seems to be a negative effect of the Awh gene on fecundity. He found the effect of the ^^-allele to be strictly additive in 3- and 4-year-old ewes, the heterozygotes showing only half as much fecundity depression as the homozygotes; the depression in homozygous white 3- and 4-year-old ewes was 0.23 lambs born per ewe. The additivity of the effect of the /l^-allele results in a biased comparison when white ewes as a group are compared to non-white ewes, the bias depending on the proportion of heterozygous white ewes entering the comparison. Icelandic investigations have also shown a marked effect of colour genes on the frequency of out of season lambing. Out of season lambing has a much higher frequency among non-white ewes (Dyrmundsson and Adalsteinsson, 1980). This may indicate an effect of colour genes on the level of sex hormones. The single gene effects on fecundity which have been summarized in the foregoing are, without exception, negative. The opposite is the case with the effect of a gene found in Booroola Merinos in Australia. Piper and Bindon (1982) report that the high fecundity in these sheep can be explained by the presence of a single major gene with an effect which seems to be around three standard deviations. Turner (1982) described the origin of these sheep and reported on how an extremely high fecundity was retained for a long time in these sheep by selection on the dam side only.
Single-gene criterion and segregation tests
161
The sheep in Borgarhoefn County in Iceland In light of the recent findings on the inheritance of litter size in the Booroola Merinos, we concentrated our efforts on searching for a similar phenomenon in Icelandic sheep, particularly at the Sheep Breeding Association of the Borgarhoefn County, where the ratio of ewes with three and four lambs has been appreciably higher than in other sheep breeding associations in Iceland. It was soon discovered that the pedigree of almost all ewes with multiple births could be traced to the ewe Thoka, at the farm Smyrlabjoerg. Thoka was born in 1950. According to oral information, Thoka's granddam gave birth to triplets around 1940. This was at that time unheard of there; ewes with twins were a rarity in this area at that time. Production records of Thoka are unfortunately not available, but it is known that she had triplets at least twice. One son of Thoka, Tossi 58165, was kept for breeding; (the first two digits in the number are the birth year). Tossi was used on the farm Borgarhoefn, a neighbour ing farm to Smyrlabjoerg. In the present investigation, information was collected on the number of lambs born from all ewes on record in the Borgarhoefn flock in the period 1961-1983. Until 1973, only part of the ewe flock at Borgarhoefn was recorded, but since 1974 all the ewes in the flock have been recorded. TABLE 17.2. Distribution of ewes in the Borgarhoefn flock on number of lambs at birth during the period 1974-1983. The sheep breeding associations are shown for comparison Source of ewes
Borgarhoefn Sheepbreeding associations
Number of lambs
Number
% %
/
2
3
4
506 27.0 32.3
1193 63.6 66.3
163 8.7 1.4
14 0.7 0.0
The period under study covers 537 recorded ewes. Table 17.2 shows the distribution of litter size of the ewes in Borgarhoefn during the period 1974-1983 and of all other ewes in the sheep breeding associations in the country during the same period. The distribution of the Borgarhoefn ewes differs significantly from the rest of the country. It is noticeable that a much larger proportion of ewes with triplets and quadruplets occur in the Borgarhoefn flock than in the rest of the country.
Single-gene criterion and segregation tests In a further analysis of the data from the Borgarhoefn flock, a comparable method to that used in the Booroola studies was employed (Piper and Bindon, 1982; Davis et al., 1982). Ewes that have given birth to triplets at least once are assumed to carry a high fecundity gene (^4 - ewes). Ewes that have never had more than two lambs are referred to as B - ewes. During the period under study five rams which seem to have carried the high fecundity gene, occurred in the Borgarhoefn flock. All could be traced back to Thoka at Smyrlabjoerg, the first known carrier of the high fecundity gene.
162
Single genes for fecundity
in Icelandic
sheep
TABLE 17.3. Average litter size of daughters of A-rams in the Borgarhoefn flock, classified by status of dam and whether they have had at least one set of triplets Sire
A-dams A -daughters
58165 66285 69281 71325 72367 No. and average
B -daughters
Litter size
No. 0 1 1 2 2 6
B-dams
Litter size
No. 0 0 1 0 0 1
2.22 2.00 2.21 2.24 2.17
A -daughters
1.67 1.67
B-daughters
No.
Litter size
No.
Litter size
13 4 11 3 9 40
2.34 2.65 2.35 2.35 2.31 2.36
19 5 11 2 9 46
1.65 1.83 1.82 2.00 1.65 1.72
Table 17.3 shows the litter size of the daughters of the five A - sires. The daughters have been separated into two groups, i.e. those having A - dams and those having B - dams. In each of the two groups the daughters have been further classified with respect to their own fertility status as either A - or B - daughters. The classification of the daughters in Table 17.3 is in excellent agreement with the hypothesis that all the sires in question carried a high fecundity gene in the heterozygous state. Only seven of the daughters have dams of type A. Among these daughters, some should be homozygous, but none of them show an excessively high fecundity. The difference in fecundity between A - and B - daughters is on the average 0.64 lambs born (Table 17.3). This difference indicates that the effect of the gene behind this trait is at least two standard deviations. The ^4-ewes in the investigation have had on average 6.8 years on record compared with 6.1 years for the B - ewes. These records do not include the number of lambs at 1 year of age. These results do not indicate that the high fecundity gene adversely affects the A - ewes. Of the 241 records of multiple births in the flock at Borgarhoefn, all except one could be traced back to the five rams descended from Thoka. When the descendants of the oldest ram, Tossi 58165, were traced for three generations, the results shown in Figure 17.1 were obtained. That the high fecundity under study is due to a single major gene is further borne out by the segregation results where a 1:1 ratio of A:B ewes is observed in accordance with expectation, as well as by the fact that the effect of the postulated high fecundity gene remains unchanged for three generations of outcrossing. TABLE 17.4. Number of times a ewe gives multiple birth classified according to her age at the first multiple birth Age at first multiple birth
Number of times with ^ 3 lambs 1
2 3 4 5 6 7 8 Total
1 2 3 4 3 2 1 16
2
3 2 4 6 1 1
3 3 1
4
5
6
7
8
Total
4 2
3 1
3
1
1
5
1
1
18 14 10 6 7 3 1 59
2
1 3 1
14
11
7
4
163
^£TL J νάΓΝ
B 9?
J A£^ 2-2.26
1-1.67
A
/ f \J
Ϋ
? 9
13-2.34
B£^ 2-1.25
10-2.49 | \
ACTCT K l\1 B££ 1-1.57
J A 9 9 5-2.25 B
3<&
Ί Β99 10-1.81
B?? 10- 1.62
χι
Acf x A ?9
&6ό y J
A99 2-2.44
BrfJJ-J
B99 6-1.53
BC#L J B99 2-1.65
4-2.65
Α(&
B?9
B??
19-1.65
2-1.67 A 99
Bdcf
1-2.00
Α ^ φ 1-2.43
A
B99l·· 11-1.68 \\ 3C&
N B99 1-1.57 BJ9 3-1.10
Unexpected
Figure J 7.1 The high fecundity condition in the Borgarhoefn flock traced for three generations. The /i-male on the left is Tossi 58165. He was only mated to ß-females. His daughters, granddaughters and greatgranddaughters are shown classified into A and B females and also classified according to whether their sire was of type A or B. The number of daughters of each type and their average litter size in each generation is shown in each female box
164
Single genes for fecundity
in Icelandic
sheep
Only one ewe in Figure 17.1 was classified as an A - ewe while having both parents of type B. This ewe gave birth to one set of triplets as an adult. Table 17.4 summarizes the results of the A - daughters of the five rams in Table 17.3, together with the appropriate descendants of ram 58165 in Figure 77.i.The ewes are classified with respect to the number of times they have had three or more lambs according to the age at which they first had a multiple birth. The ewes are on average 3.7 years old when they first give birth to three or more lambs, and on average they give birth to three or more lambs 2.9 times. It should be borne in mind that some of these ewes are still alive, and a few of them started in the recording scheme at an adult age.
Heritability estimate, and records of one-year-old ewes The available data are somewhat limited for heritability estimation. The heritability of litter size was estimated in the Borgarhoefn material, on 1072 records from 417 ewes, in the age classes 2-4 years, out of 58 sires. The heritability was found to be 0.16±0.07, and the repeatability 0.32±0.03. These results agree well with previous heritability estimates on Icelandic data, but the repeatability estimate in the present study is appreciably higher, as one would expect (Jonmundsson, Adalsteinsson and Steingrfmsson, 1977). Only a certain proportion of the ewe lambs in the Borgarhoefn flock is mated during their first winter. Furthermore, lambing records for ewe lambs in the flock are only available for the last few years. TABLE 17.5. Number of lambs born at 1 year of age to ewes classed A- or Bin later records Ewe type
Number of lambs at one year of age 1 2
,4-ewe ß-ewe
9 98
9 11
Table 17.5 shows the fecundity at 1 year of age of the A - and B - ewes which have lambing records at that age. These limited data show a significantly higher twinning rate at 1 year of age in the A - ewes. Studies on the fecundity records in the sheep breeding associations have shown a clear connection between twinning at 1 year of age and occurrence of multiple births in adult life (Jonmundsson, 1982).
Miscellaneous information on the high fecundity condition The high fecundity has, if anything, been selected against in the Borgarhoefn flock. For that reason there are fewer A - ewes in the younger age classes than in the older ones. A few rams have been sold from the flock to neighbouring flocks and, in many cases, high fecundity has occurred in these flocks when the daughters of the bought-in rams matured. Almost all examples of quintuplets and sextuplets in Icelandic ewes can be traced to this high fecundity strain of sheep. In the Smyrlabjoerg flock where Thoka, the ewe of origin, was born, a strain of highly fecund ewes has been maintained by consecutive breeding for daughters of high fecundity ewes.
The high fecundity sheep at Skriduklaustur
165
Lambing record at age 2 - 1 0 years
O Thoka
1
Q
Rispa
3 - 2 - 3 - 1 - 3 - 3 - 3 - 3
Q
Brenna
2 - 3 - 3 - 2 - 2 - 2 - 3
1 1 I
Q Katla 70302
3 _ 3 _ 2 - 4 - 3 - 4 - 4 - 4 - 3
0
2 - 4 - 3 - 4 - 4 - 4 - 3 - 1
Prila 73034
>1
_J O
Angi 79608
Age of daughters
\
Number of lambs 2 3
4
x
1
16
16
3
2
2
23
11
3
2.38
4
4
2
2.80
3
1.63
Figure 17.2 The line of female ancestry between the ewe Thoka at Smyrlabjoerg and the ram Angi 79608, with their lambing records. The lower part of the figure shows the litter size of the daughters of Angi 79608 at 1, 2 and 3 years of age
The pedigree of one ram, no. 79608, is shown in Figure 17.2, together with the available information on the fecundity of his daughters up to the age of 3 years. As the figure shows the daughters of this ram show an outstanding fecundity. Ram 79608 was mated to A - ewes. In the spring of 1983, seven of his daughters were barren because they have never shown heat. All these ewe are out of large litters of A - dams. This phenomenon needs further investigation because these ewes could possibly be the first ewes which are homozygous for the high fecundity gene. Owen (1982) reported a similar phenomenon in the high fecundity Cambridge sheep and suggested that it was due to a prenatal effect.
The high fecundity sheep at Skriduklaustur In autumn 1976 an experiment on breeding a strain of high fecundity sheep was initiated at the Experimental Station, Skriduklaustur by collecting lambs out of
166
Single genes for fecundity in Icelandic sheep
high fecundity ewes. The procedure was similar to that adopted in several other countries in the preceding years, as described by Land, Atkins and Roberts (1983). Some of the experimental lambs were bought in from the flocks at Smyrlabjoerg and Borgarhoefn. At that time we were not aware of the mode of inheritance of this high fecundity, and the selection was not based on that principle. Up to now only limited selection has been carried out within the high fecundity strain, the main objective having been performance recording of individuals. Few records are available, but the daughters of classed ewes show a separation into two groups which agrees well with the hypothesis that their dams are heterozygous for a major fecundity gene. One of the bought-in ewes in the experiment has shown an exceptional fecundity. She had triplets at 1 year of age and from three to five lambs per lambing since then, the average being 3.83 lambs per year in 6 years of adult life. In autumn 1982 the testis weight of ram lambs from the Skriduklaustur flock was recorded at around 120 days. Sires from the high fecundity strain sired ram lambs with significantly heavier testicles, 257 g (84 lambs) compared with 226 g (163 lambs) for the progeny of other sires. It is not known whether the rams in the high fecundity strain carry the major gene under study. We propose to refer to the gene described as the Thoka gene in reference to the ewe Thoka, the first known carrier.
The utilization of the high fecundity gene It is obvious that through proper utilization of a gene with as large effect as that described here, a marked increase in ewe fecundity can be achieved in a relatively short time. Much research on the condition is needed, however, and some of the items needing further investigation will be pointed out in the following. In the material described here it has not been possible to find individuals which can be classified as homozygous. The breeding carried out so far has not been aimed at producing such individuals. However, until such individuals are identified nothing can be deduced about the dominance or additive effects of the gene. At present the only way to establish whether a ram carries the gene is to test his daughters. There, it is of importance to find out how early in the life of the daughter the condition manifests itself. The daughters of ram no. 79608 shown in Figure 17.2 indicate that the condition is partly visible at 1 year of age. The possibility of finding methods to select rams for breeding on their own phenotype should be investigated, such as selection on testis size, hormonal level, etc. The measure of fecundity in the present investigation has been number of lambs born. Lamb mortality in this strain should be investigated further. The owners of the sheep under study indicate, however, that this is not a serious problem. It is of interest to study the effect of the high fecundity gene in ewes of different colours. The foundation ewe, Thoka (means Fog), was of grey colour, and grey as well as other non-white colours are frequent in this strain. Hanrahan's hypothesis about the relationship between number of ova shed and number of lambs born is of particular interest in this connection (Hanrahan, 1980; Hanrahan and Piper, 1982). From this hypothesis it must be assumed that separation of homozygous and heterozygous ewes is very difficult on the basis of number of lambs born. It therefore seems of great importance to initiate studies on
The utilization
of the high fecundity
gene
167
ovulation rate in ewes of this strain in order to be able to assess the behaviour of the trait more accurately. At present very few rams seem to be carriers of the high fecundity gene, ram no. 79608 being the only one which is known with certainty to be a carrier. It seems highly relevant to take such rams into insemination stations in order to distribute the condition more widely. In the Borgarhoefn county there are now between 100 and 200 ewes which are assumed to carry the gene. In order to ensure the best possible utilization of the gene these ewes should be mated extensively to elite rams at the artificial insemination stations. Their sons should then be retained for breeding and taken through a planned progeny testing scheme. It is of great importance to widen the breeding base before pure-breeding within the strain is started. It is clear that several traits in addition to the high fecundity condition have to be included in the breeding stock in order to secure general utilization of this important gene in practical sheep breeding in Iceland. Acknowledgement We want to express our thanks to the farmers in the Borgarhoefn County who provided information on the high fecundity condition. Particular thanks are due to the farmers Ragnar Sigurdsson, Borgarhoefn and Karl Bjarnason, Smyrlabjoerg. References ADALSTEINSSON, S. (1970). Journal of Agricultural Research in Iceland, 2, 3-135 ADALSTEINSSON, S. (1971). Journal of Agricultural Research in Iceland, 3, 28-38 ADALSTEINSSON, S. (1975). Annales de Genetique et de Selection animale, 7, 445-447 ADALSTEINSSON, S. (1984). First World Congress on Coloured Sheep and Their Products, New Zealand, edited by H.T. Blair, pp. 237-241 ADALSTEINSSON, S. and HALLGRf MSSON, S. (1977). Journal of Agricultural Research in Iceland, 9, 77-82 BRADFORD, G.E. (1972). Journal of Reproduction and Fertility, Suppl. 15, 23-41 BRUERE, A.N. (1974). Proceedings of the First World Congress on Genetics Applied to Livestock Production, 1, 151-175 DAVIDSSON, J. (1966). Freyr, 62, 15-17 DAVIS, G.H., MONTGOMERY, G.W., ALLISON, A.J., KELLY, R.W. and BRAY, A.R. (1982). New Zealand Journal of Agricultural Research, 25, 525-529 DENNIS, S.M. and LEIPOLD, H.W. (1976). Zughthygiene, 11, 105-112 DYRMUNDSSON, O.R. and ADALSTEINSSON, S. (1980). Journal of Heredity, 71, 363-364 EDEY, T.N. (1969). Animal Breeding Abstracts, 37, 173-190 EDEY, T.N. (1979). In Sheep Breeding, 2nd edn, edited by G.J. Tomes, D.E. Robertson, R.J. Lightfoot and W. Haresign, pp. 315-325. London: Butterworths GLAHN-LUFT, B. and WASSMUTH, R. (1980). Proceedings EAAP, Sheep and Goat Commission, München HALLGRf MSSON, S. (1966). Thesis for Licentiate in Agriculture, Agricultural University of Norway HÄMORI, D. (1964). Allatenyesztes, 13, 133-140 HANRAHAN, J.P. (1980). Proceedings of the Australian Society of Animal Production, 13, 405-408 HANRAHAN, J.P. and PIPER, L.R. (1982). Proceedings EAAP, Sheep and Goat Commission, Leningrad JONMUNDSSON, J.V. (1977). Journal of Agricultural Research in Iceland, 9, 31-42 JONMUNDSSON, J.V. (1982). Freyr, 78, 578-579 JONMUNDSSON, J.V., ADALSTEINSSON, S. and STEINGRIMSSON, J.T. (1977). Journal of Agricultural Research in Iceland, 9, 50-62 KUROWSKA, Z. and DANELL, Ö. (1982). Färskötsel, 62, 14-15 LAND, R.B., ATKINS, K.D. and ROBERTS, R.C. (1983). In Sheep Production, edited by W. Haresign, pp. 515-535. London: Butterworths OWEN, J.B. (1982). Proceedings EAAP, Sheep and Goat Commission, Leningrad
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Single genes for fecundity
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sheep
PIPER, L.R. and BINDON, B.M. (1982). Proceedings of the World Congress on Sheep and Beef Cattle Breeding, 1, 395-400 PURSER, A.F. and HALL, J.G. (1974). Proceedings of the British Society of Animal Production, 3, 95 QUIRKE, J.F., ADAMS, T.E. and HANRAHAN, J.P. (1983). In Sheep Production, edited by W. Haresign, pp. 409-429. London: Butterworths R A E , A.L. (1956). Advances in Genetics, 8, 189-265 RASMUSEN, B.A. (1975). In Handbook of Genetics, 4, edited by R.C. King, pp. 447-457. New York: Plenum Press RICORDEAU, G., TCHAMITICHIAN, L., RAZUNGLES, J., LEFEVRE, C. and BRUNEL, J.C. (1982). 2nd World Congress on Genetics Applied to Livestock Production. Madrid, VII, 596-598 SAPERSTEIN, G., LEIPOLD, H.W. and DENNIS, S.M. (1975). Journal of American Veterinary Medical Association, 167, 314-322 TURNER, H.N. (1982). In The Booroola Merino, edited by L.R. Piper, B.M. Bindon and R.D. Nethery, pp. 1-7. Melbourne: CSIRO TURNER, H.N. and YOUNG, S.S.Y. (1969). Quantitative Genetics in Sheep Breeding. Ithaca, New York: Cornell University Press