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Small Ruminant Research 36 (2000) 215±226

Review

Frequency of the proli®cacy gene in ¯ocks
of Indonesian thin tail sheep: a review
J.A. Roberts
Schultz Road, Witta, via Maleny 4552, Queensland, Australia
Accepted 15 November 1999

Abstract
Indonesian thin tail (ITT) sheep have a major proli®cacy gene (FecJF), the frequency of which is higher in the new born
lambs, than in the remainder of the ¯ock when mating is random, because carrier ewes produce more progeny than do non
carriers. The frequency of the gene may vary between ¯ocks, but remains relatively stable in ¯ocks with established husbandry
procedures. The countermanding selection pressures maintaining the equilibrium value for the frequency of FecJF are mainly
those deriving from higher mortality rates of lambs in larger litters. Embryo survival is not signi®cantly different across the
range of ovulation rates in ITT ewes, in contrast to observations in other proli®c breeds. Generation intervals and the
incidences of metabolic and infectious diseases in ewes carrying larger litters can also affect the frequency of FecJF in ¯ocks.
In turn, each of the factors affecting the frequency of FecJF is modulated by the level of nutrition and management in each
¯ock. The distribution of proli®cacy genotypes in the ewes of a standard ¯ock is calculated as FecJFFecJF/12; FecJFFecJ‡/44;
FecJ‡FecJ‡/44 giving a frequency of 0.34 for FecJF. The frequency of FecJF is then 0.43 in the lambs at birth, when their

numbers have been ampli®ed in the carrier ewes. There are heavier metabolic demands on ewes carrying larger litters and the
foetuses constitute a higher proportion of weight gain during pregnancy. Consequently, more of the lambs of carrier ewes are
smaller and weaker at birth, and the reserves of the ewes for colostrum and milk production are depleted. When low lamb
survival rates in larger litters are considered, the frequency of FecJF falls to 0.35 in the lambs at weaning in lean years and 0.38
in middling years. At a high level of husbandry, ewe weight gains during pregnancy and lamb survival rates improve
substantially, and after 3 years, the frequency of FecJF in the lambs at birth is estimated to have risen to 0.49; and 0.47 at
weaning. # 2000 Elsevier Science B.V. All rights reserved.
Keywords: Indonesian thin tail sheep; Proli®cacy; Gene frequency

1. Introduction
Indonesian thin tail (ITT) sheep are the predominant breed in the province of West Java where they are
well adapted to the hot humid environment. Traditionally, they are maintained in family ¯ocks of about
three ewes, many families relying on neighbours for a
ram. They are housed at night in small elevated pens

with slatted ¯oors, and are provided with feed cut and
carried from roadsides, woodland and fallow land. In
some areas family ¯ocks are permanently housed,
while in others they graze under supervision during
part of the day. Small closely supervised ¯ocks appear

to provide the conditions necessary to maintain genes
for proli®cacy (Mason, 1980), and a proli®cacy gene
with major effect (Bradford et al., 1986, 1991), occurs

0921-4488/00/$ ± see front matter # 2000 Elsevier Science B.V. All rights reserved.
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J.A. Roberts / Small Ruminant Research 36 (2000) 215±226

Table 1
Frequency distributions of the litter sizes produced by ewes of each of the proli®cacy genotypes of ITT sheep under different husbandry
regimes. Data from the RIAP ¯ock
Level of nutrition

Lean/middling

Good

Genotype

‡‡
F‡
FF
‡‡
F‡
FF

Frequency distributions of litter sizes (%)
Single

Twin

Triplet

76
24
14
85

13
16

24
56
33
15
59
39

0
20
34
0
27
25

in the ITT breed. On institutional farms, ewes are
usually kept in group pens and nutrition and management vary widely. Like most proli®c breeds of sheep
(Bindon et al., 1996), ITT sheep reach puberty early

(Sutama et al., 1988), resume ovarian activity shortly
after parturition (Sutama et al., 1988) and are non
seasonal breeders (Fletcher and Putu, 1985). With this
combination of traits, the breed produces meat ef®ciently (Reese et al., 1990; Iniguez et al., 1991; Inounu
et al., 1993), in spite of the small size of the ewes (17±
30 kg). The proli®cacy gene of ITT sheep is designated FecJF, with the standard allele FecJ‡, (COGNOSAG, 1989).
When mating is random, gene distributions of traits
which do not affect reproduction remain relatively
stable. However, for a proli®cacy gene, the frequency
in the zygotes is determined by the frequency in the
parental generation ampli®ed by the proli®cacy of the
ewes. That is, a homozygous normal ITT ewe, which
produces mainly single lambs, will contribute genes to
one zygote, whereas a homozygous carrier, which
produces mainly twins and triplets, Table 1, will
contribute genes to more than two zygotes. In the
absence of countermanding selection pressures, the
frequency of the fecundity gene would increase with
each generation. Nevertheless, distributions of litter
sizes in institutional and village ¯ocks in West Java,

Table 2, remain relatively stable. Bradford et al. (1986,
1996) have suggested that the proli®cacy gene is in all
populations of ITT sheep at a frequency of 0.05±0.25.
Factors which may modulate the frequency of FecJF in
¯ocks of Indonesian sheep on institutional farms and
in villages are assessed in this review, and distributions
of genotypes and the corresponding frequencies of
FecJF under different husbandry conditions, are cal-

Quadruplet
0
17
0
20

Reference
Quintuplet

2

0

Mean
1.24
1.95
2.59
1.15
2.14
2.48

Inounu et al., 1993

Subandriyo and Inounu, 1994

culated. In addition, some of the characteristics of
other proli®c breeds are compared with those of ITT
sheep.
2. Modulation of the frequency of FecJF
The frequency of FecJF in ¯ocks is modulated by
nutrition and husbandry practices which are re¯ected

in ovulation rates, survival and growth of lambs in
larger litters, generation intervals, and metabolic diseases of ewes carrying large litters.
2.1. Ovulation rate
High levels of supplementary feeding over several
months increased ovulation rates. The diet was free
access to freshly cut grass, plus concentrate, 10 MJ/kg
dry matter and 15% crude protein, either ad lib., or
700 g/day, and was compared with a maintenance diet
of the same ingredients. In the study of Henniawati
and Fletcher (1986), the mean body weights of the
supplemented 2 and 4 tooth ewes increased from
19.5 kg to 24.5 kg over 22 weeks and the mean
ovulation rate increased to a maximum of 2.65 at
the sixth oestus after the beginning of the feeding
regime, compared with 1.69 at the maintenance level.
Nevertheless, mean litter size was only 1.78 compared
with 1.50 at the maintenance level. At the same level
of supplementation young ewes had a mean ovulation
rate of 2.1 and a litter size of 1.8 compared with
control ewes with 1.6 and 1.5 respectively (Sutama

et al., 1988). So with prolonged supplementation at a
high level, there was a higher ovulation rate, lower
embryo survival and a small increase in litter size.

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J.A. Roberts / Small Ruminant Research 36 (2000) 215±226

Table 2
Distributions of litter sizes in institutional ¯ocks of ITT sheep. There would be overlap in the data bases used to compile the results from the
RIAP ¯ock
Parity

Frequency distributions of litter sizes (%)
Single

Twin

Triplet

Quadruplet

Quintuplet

33
35
24
31
38
41

11
14
18
20
16
13

0
12

21
7
9
3

0
3
1
1

45
40

38
39

14
17

31
48
41
55
49
56

38
35
37
34
38
36

24
13
20
11
11
7

Single

Twin

29
38
68

50
44
28

Triplet and
above
21
17
4

71

26

Institutional farms
First
57
Second 40
Latter
32
41
41
43

Sextuplet

Mean

Founding
stock

Location

Reference

1.54
2.00
2.47
1.96
2.06
1.76

Garut

RIAP

Bradford et al., 1986

Garut
Garut
Garut

RIAP
RIAP
RIAP

3
4

1.71
1.86

Garut
Garut

RIAP
RIAP

7
4
2
1
2
1

2.07
1.73
1.86
1.58
1.66
1.53

Not stated
Not stated
Garut
Bogor
Garut
N. Sumatra

Bogor
Bogor
Ciawi
Ciawi
Margawati
N. Sumatra

Inounu et al., 1984
Bradford et al., 1989
Iniguez and
Gunawan, 1990
Inounu et al., 1993
Subandriyo and
Inounu, 1994
BPPH, 1955a
IPB, 1977a
Obst et al., 1980
Obst et al., 1980
Atmadilaga, 1992
Iniguez et al., 1991

1

1

Villages

a

3

1.97
1.77
1.36

West Java
West Java
West Java

1.32

Sumatra

Inounu et al., 1984
Subandriyo, 1986
Means of data from
Mason, 1980
Verwilghen
et al., 1992

Data cited by Mason (1980).

Reese et al. (1990) provided energy supplementation
up to 826 kcal ME/day to ewes grazing on a rubber
plantation. Litter size at the highest level of supplementation was 1.49 compared with 1.26 at lower
levels, in ITT sheep from Sumatra, which have a
relatively low frequency of the proli®cacy gene. Lamb
birth weights, survival rates and growth rates all
improved. On the other hand, in the Research Institute
for Animal Production (RIAP) ¯ock (Inounu et al.,
1993), mean litter sizes produced by each of the
proli®cacy genotypes during years of good nutrition
(Subandriyo and Inounu, 1994), did not differ from
those of the lean and middling years (Inounu et al.,
1993), Table 2. Lower levels of supplementation,
provided strategically, did not affect ovulation rates
(Inounu et al., 1985; Chaniago et al., 1988).
If supplementation does increase litter sizes, and the
three proli®cacy genotypes respond in proportion to

their ovulation rates, then the frequency of FecJF
would increase in lambs from supplemented ewes.
2.2. Conception rate and embryo survival
Conception rates, embryo survival rates and net
rates of survival of ova in ITT ewes were high, and
embryo survival rates did not differ signi®cantly over
the range of litter sizes, Tables 3 and 4, and proli®cacy
genotypes (Bradford et al., 1991). Nevertheless, the
trend of decreasing embryo survival rates with
increasing ovulation rates in ITT ewes, was similar
to that of other proli®c breeds, Table 4, re¯ecting
decreasing marginal response of uterine ef®ciency
with increasing numbers of embryos (Meyer, 1985).
Thus, on the basis of the available data, conception
rate and embryo survival will not have signi®cant
effects on the frequency of FecJF in the progeny of

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J.A. Roberts / Small Ruminant Research 36 (2000) 215±226

Table 3
Conception rates and survival of embryos to lambing, for ewes producing different numbers of corpora lutea. Most ewes were served once
when oestrus was ®rst detected. Data of Javanese and Semarang strains of ITT sheep in Bradford et al. (1986)
Number of corpora lutea

Number of ewes mated
Number of ewes lambed
Fertility (%)
Embryo survival/ewe lambing (%)
Net survival of ova (%)

1

2

3

4±5

All

79
57
72
100
72

79
65
82
92
75

29
19
66
89
59

14
12
71
80
57

201
153
76
91
69

ITT sheep; but would reduce the frequencies in other
proli®c breeds.
2.3. Survival from birth to weaning
In the study of Obst et al. (1982), 31% of lambs
died. Of those lambs, 32% were stillborn, 5% died at
birth and 49% between birth and 3 days, and 60% of
the total deaths were from litters of triplets and above.
About 40% of the total deaths were attributed to lambs
being small, weak or immature, and 11% to mismothering. Inounu et al. (1993) found that stillbirths
constituted 52% of mortality to weaning.
Survival from birth to weaning is directly related to
the weights of individual lambs at birth, and there is a
strong inverse relationship between survival to weaning, and litter size, Table 5. Larger litters comprise a
larger proportion of ewe weight gain during gestation
than do singles (Inounu et al., 1993), Table 6, so after
parturition ewes with larger litters have lower body
reserves and are less able to provide colostrum and
milk for the small lambs in those litters. This leads to

lower survival rates of lambs to weaning, Table 7, and
lower litter weights at weaning, Table 6.
Moreover, the low survival rates in larger litters are
exacerbated when the level of nutrition is low, Tables 6
and 7.
The quality and quantity of milk produced by ITT
ewes is in the low range of sheep breeds (Sutama et al.,
1988), but the requirement of the small lambs is also
low. Level of nutrition and litter size affected weight
changes of ewes, Table 6, and milk production, but not
milk composition (Sitorus et al., 1985b). During 12
weeks from lambing, average milk production was
26 kg on a low level of nutrition and 31 kg on a higher
level (Sitorus et al., 1985b), similarly 25 and 37 kg
respectively (Sutama et al., 1988), and an average of
30 kg (Atmadilaga, 1958). Milk production was
higher during the second lactation on both levels of
nutrition (Sutama et al., 1988). Suckling of twins
increased milk production by 28% on a low level of
nutrition and 5% on a high level. Maximum production occurred 3±4 weeks after lambing (Atmadilaga,
1958; Sitorus et al., 1985b; Sutama et al., 1988).

Table 4
Distributions of the mean litter sizes, and survival rates, which correspond to each ovulation rate in lambing ewes of some proli®c breeds
Mean litter sizes (embryo survival %) at different ovulation rates
Breed

Ovulation rate
2

a

ITT
Romanov
Finn, sheep
D'man
Icelandic
a
b

Reference

1.83
1.90
1.72
1.80
1.76

3
(92%)
(95%)
(86%)
(90%)
(88%)

2.68
2.61
2.24
2.33
2.25

4
(89%)
(87%)
(75%)
(78%)
(75%)

Javanese and Semarang strains of ITT sheep.
Including ®ve.

3.30
3.17
2.63
2.83
2.48

55
b

(80%)
(79%)
(66%)
(71%)
(62%)

3.58
2.90
2.44
2.50

(72%)
(42%)
(46%)
(50%)

Bradford et al., 1986
Ricordeau et al., 1990
Ricordeau et al., 1990
Lahlou-Kassi and Marie, 1985
Eythorsdottir et al., 1991

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J.A. Roberts / Small Ruminant Research 36 (2000) 215±226

Table 5
Survival rates of individual ITT lambs from birth to weaning at 90 days, in relation to birth weight and litter size. Data from Chaniago et al.
(1988)a
Survival rates (%) of individual lambs by birth weights and litter sizes
Litter size

2.4 kg

All birth weights

Single
Twin
Triplet
Quadruplet
All litter sizes

0 (2)
25 (4)
0 (12)
0 (2)
5

75 (4)
43 (28)
21 (24)
0 (4)
33

86 (14)
70 (46)
60 (10)
0 (2)
69

89 (26)
79 (33)
0 (2)
± (0)
84

88 (24)
89 (9)
± (0)
± (0)
88

85
66
27
0
63

a

( )ˆNumber of lambs per class.

Survival of lambs, particularly those in larger litters,
is dependent on the levels of nutrition and management in a ¯ock. In turn, low survival rates of the small
lambs in large litters is the major pressure countermanding ampli®cation of the frequency of FecJF in the
zygotes of proli®c ewes. The survival rates of lambs in
larger litters, would increase from the commencement
of better husbandry in a ¯ock, and continue to improve
over a full reproductive cycle. Survival of lambs is
inversely related to litter size regardless of the level of
husbandry, Table 7, so the frequency of FecJF in the
¯ock would continue to rise as more large litters were
produced and more lambs survived. Ultimately, a new
equilibrium will be established between the distribution of litter sizes and lamb survival at the new level of
husbandry. At very high levels of nutrition, the
increased incidence of metabolic diseases in ewes
(Obst et al., 1980, 1982; Fletcher et al., 1982; Aitkin,

1996) would reduce the increase in the frequency of
FecJF. Lambs in larger litters have lower survival rates
in all proli®c breeds of sheep (Aitkin, 1996).
2.4. Breeding life of ewes
Age, weight and parity are generally inseparable in
the data available; but they have important effects on
ovulation rates and litter sizes, which were higher in
older, heavier, multiparous ewes. Mean ovulation rates
increased from 1.43 to 2.93 for ewe body weights from
17.1 to 29.6 kg (Bradford et al., 1986). Mean numbers
of lambs per litter increased from 1.54 for primipara
ewes to 2.47 for third and later parities (Bradford et al.,
1986), Table 2. Ewes carrying the proli®cacy gene
would be differentially affected to the extent that
average life span is reduced by the metabolic and
infectious diseases to which ewes with larger litters are

Table 6
Weight gains of ewes during gestation, and weaning weights of litters, related to the proli®cacy genotypes and litter sizes in the RIAP ¯ock of
ITT sheep, in years with different levels of husbandry
Level of
husbandry

Lambs in
litter

Prolificacy genotype

Litter size at birth

FF

Single

Twin

Triplet

Ewe weight gain during gestation (kg)
Lean
0.5
Middling
1.8
Good
3.8
Weaning weight of litter (kg)
Lean
6.7
Middling
12.2
Good
One
13.7
Two
20.2
Three/four
22.8
a

Including quad ruplets.

F‡

‡‡

Reference
Quadruplet

1.1
2.3
4.0

1.4
2.9
3.8

1.8
3.2
5.2

0.7
2.2
2.8

0.3
1.1
2.4

ÿ0.9
1.1
7.9

Inounu et al., 1993

7.4
11.9
12.7
19.0
18.2

7.7
10.9
14.2
23.0

7.7
10.5

7.6
12.3

6.1
13.1

5.3
11.9

Inounu et al., 1993

13.8

19.9

20.3a

Subandriyo and Inounu, 1994

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J.A. Roberts / Small Ruminant Research 36 (2000) 215±226

Table 7
Survival rates of individual ITT lambs to weaning related to proli®cacy genotypes of the ewes, and litter sizes, in the RIAP and Ciawi ¯ocks of
ITT sheep during years with different levels of husbandry. A village ¯ock is included for comparison
Level of
husbandry

Instutional farms
Lean
Middling
Good
Good

Lambs
in litter

One
Two
Three and
above

High nutrition/mixed
management
Strategic supplementation/
unknown management
Levels of supplementation/
good management
Village
Unknown nutrition/
management
a

Survival rates (%)
Genotype

Location

Reference

Cicadas
Cicadas
Bogor

Inounu et al., 1993

Bogor

Subandriyo and
Inounu, 1994

Litter size

FF

F‡

‡‡

Single

Twin

Triplet

Quadruplet

41
59
88
90
88

58
75
80
93
84

74
89
90
93
97

81
91
94

55
78
84

30
52
83

21
35
73

93

86

65a

71

60
94

73

46

0

Ciawi

Obst et al., 1982

85

66

27

0

Ciawi

Chaniago et al., 1988

92

77

67

55

Sumatra

Iniguez et al., 1991

97

88

70

Village

Inounu et al., 1993

Inounu et al., 1993

Including quad.

more prone (Aitkin, 1996). In the Ciawi ¯ocks with a
continuous high level of nutrition, 11% of breeding
ewes in one ¯ock died per lambing interval (Obst et
al., 1980), the main causes being vaginal prolapse and
pregnancy toxaemia (Obst et al., 1982), and dystocia
(Fletcher et al., 1982). In the same ¯ock, the mortality
of ewes was halved when strategic supplementation
replaced continuous high level feeding (Chaniago
et al., 1988).

intervals were directly related to the postpartum body
condition of the ewes (Sutama, 1992), and so were
prolonged by about 9 days for ewes with previous
larger litters (Sitorus et al., 1985a).
Low nutrition of lambs, and the draining effects on
ewes bearing large litters, would increase generation
intervals for carriers of the proli®cacy gene, with the
main effect being on the time taken for ewe lambs to
reach puberty. There would be minor, long term
selection against carriers of FecJF.

2.5. Generation intervals
2.6. Husbandry procedures
ITT ewe lambs attained puberty when their body
weights averaged 17±18 kg, so the slower growing
lambs reared in larger litters, were up to 80 days older
when they produced their ®rst litters (Sutama et al.,
1988). Similarly ewe lambs on high and low levels of
nutrition, reaching puberty at similar body weights,
were 221 days old on the high level, and 297 days on a
low level (Sutama et al., 1988).
ITT ewes on a higher level of nutrition conceived
about 60 days after lambing and those on a lower level
about 14 days later (Sutama et al., 1988). Lambing

The management procedures which can improve
survival of ITT lambs are seldom recorded. At Ciawi,
ewes were joined continuously with rams except for 2
weeks after parturition when ewes were in individual
pens with their lambs. Dystocia cases were assisted,
pregnancy toxaemia was treated and weak lambs were
assisted to suckle (Obst et al., 1982). Nevertheless,
there was a husbandry problem in that ¯ock because
no quadruplets survived over a number of years, Table
7 (Obst et al., 1982; Chaniago et al., 1988). Ewes and

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J.A. Roberts / Small Ruminant Research 36 (2000) 215±226

lambs need space, time and quiet to promote mothering and bonding (Gatenby et al., 1994; Poindron et al.,
1996). Most mature ITT ewes lambed within 30 min,
and licked the newborn lamb. Lambs stood within
30 min and ewes encouraged them to suckle by nuzzling the rump. There were no differences between
lambs from single and multiple births (Sutama and
Inounu, 1993; Gatenby et al., 1994). Assisting weak
lambs to suckle, hand feeding and fostering can
improve survival of weak lambs if suitable carers
are available (Tiesnamurti, 1992a,b). Some village
families supplement weak lambs with milk substitutes
(Bell and Inounu, 1982), but fostering and hand rearing are rare on institutional farms. Self weaning of
lambs from large litters at about 5 weeks probably
occurs (Sutama et al., 1988), as it does in other
proli®c breeds (Poindron et al., 1996). Again, the frequency of FecJF is raised when lambs in larger litters
survive.
Only a few rams are required for breeding and the
remainder must be culled, so, if the best ram lambs are
kept they will probably have been singles, and there
will have been selection reducing the frequency of
FecJF. Weight was the main selection criterion for
rams and ewes for the ¯ocks of village families (Bell
and Inounu, 1982).
2.7. Frequencies of FecJF and distributions of litter
sizes
The reported distributions of litter sizes in the RIAP
¯ock from 1981 to 1989 are relatively consistent,
Table 2, probably because ¯uctuations in the level
of husbandry were random at Cicadas, where there
were lean years (1982, 1985, 1986, 1988) and middling years (1981, 1983, 1984, 1987, 1989), (Bradford
et al., 1991; Inounu et al., 1993). The frequency of
FecJF would be around that corresponding to the
average level of husbandry over the period, being
buffered as the maiden ewes from each lambing,
entered a ¯ock containing older ewes reared under
differing husbandry regimes. In 1990, the ¯ock was
moved to Bogor and the husbandry was good from
1991 to 1993 (Inounu et al., 1993; Subandriyo and
Inounu, 1994). Ewe weight gains during gestation,
survival rates of individual lambs to weaning, and
litter weaning weights, are presented as indicators of
the respective levels of husbandry, Tables 6 and 7.

Table 8
Approximate frequency distributions of litter sizes, at different
frequencies of the proli®cacy gene in ITT ewes, based on a Hardy
Weinberg distribution of the gene as discussed in the text. The
distributions of litter sizes reported by Inounu et al. (1993) for each
proli®cacy genotype, have been used in the calculation
Frequency distributions (%) of litter sizes
Frequency
of F

Single

Twin

Triplet

Quadruplet

Quintuplet

0.0
0.1
0.2
0.3
0.35
0.4
0.5
0.6
0.7
0.8
0.9
1.0

76
66
57
49
45
41
35
29
24
20
16
14

24
30
35
38
40
41
42
43
42
40
37
33

0
4
8
11
13
14
19
22
25
28
31
34

2
2
3
4
6
8
11
14
17

1
1
2
2

The distribution of litter sizes at birth in a ¯ock,
re¯ects the distribution of proli®cacy genotypes of the
ewes, as each genotype produces a distribution of litter
sizes, Table 1. Empirically, each of the distributions of
litter sizes in ¯ocks, Table 2, approximates the distribution of litter sizes which would result from a
Hardy Weinberg distribution of proli®cacy genotypes
in the breeders, Table 8. The reason for this relationship will be discussed when survival rates of lambs in
different litter sizes are considered below. The distribution of litter sizes in the RIAP ¯ock during lean
and middling husbandry periods (Inounu et al., 1993),
Table 2, approximates that for a frequency of 0.35 for
the proli®cacy gene, Table 8. At that frequency of the
proli®cacy gene, the distribution of litter sizes for each
genotype, Table 1, can be transposed to provide the
distribution of proli®cacy genotypes for each litter
size, Table 9. Application of those values to the
observed distribution of litter sizes from Inounu et
al. (1993), Table 2, gives the actual distribution of
proli®cacy genotypes in the ewes as FecJFFecJF/12;
FecJFFecJ‡/44; FecJ‡FecJ‡/44, compared with the
Hardy Weinberg approximation of FecJFFecJF/12;
FecJFFecJ‡/46; FecJ‡FecJ‡/42. The actual distribution of genotypes in the ewes is then used to calculate
the number of lambs of each genotype in each litter
size, being the product of the frequency of the proli-

222

J.A. Roberts / Small Ruminant Research 36 (2000) 215±226

Table 9
Calculated frequency distributions (%) of each of the proli®cacy
genotypes of ITT sheep in each litter size, on the basis of a
frequency of 0.35 for the gene, as discussed in the text. Data
transposed from Inounu et al. (1993)
Frequency distributions of genotypes (%)
Litter size

FF

F‡

‡‡

Single
Twin
Triplet
Quadruplet
Quintuplet

4
11
33
100
100

26
65
67
0
0

70
24
0
0
0

®cacy genotype of the ewe, by the litter size, by the
frequency of that litter size in the appropriate proli®cacy genotype, Table 1 (Inounu et al., 1993). The
sums of the values gives the distribution of proli®cacy
genotypes in the progeny at birth as FecJFFecJF/18;
FecJFFecJ‡/50; FecJ‡FecJ‡/32, and the frequency of
FecJF as 0.43. In all cases, it is assumed that the
distribution of proli®cacy genotypes of rams is the
same as that of ewes.
Survival rates from birth to weaning, Table 7, are a
consequence of litter size, not of the proli®cacy gene
carrier status of the dam per se, so litter size distributions have been calculated for each genotype and the
appropriate survival rate has been applied to each litter
size at each of the levels of husbandry. The frequency
of FecJF in the progeny at weaning in a lean year
reduces to 0.35 with a genotype distribution FecJFFecJF/12; FecJFFecJ‡/46; FecJ‡FecJ‡/42, and in a
middling year to a frequency of FecJF of 0.40 with a
genotype distribution FecJFFecJF/15; FecJFFecJ‡/50;
FecJ‡FecJ‡/35. So with the additional losses associated with carrier ewes and their progeny discussed
above, the frequency of FecJF would be maintained in
the ¯ock at a value of about 0.35. Clearly at these
levels of husbandry, survival of lambs from birth to
weaning is the major selection force countermanding
the ampli®cation of the FecJF gene in carrier ewes.
Consequently, in a ¯ock in which the frequency of
FecJF is at the equilibrium level for the prevailing
level of husbandry, the effects on the frequency of
FecJF of ampl®cation of genotypes at conception, and
of mortality rates of lambs in larger litters from birth to
weaning, will be opposite, and approximately equal.
So the distribution of litter sizes in the ewes will

approximate that for a Hardy Weinberg distribution
of the genotypes of the ewes.
Application of the survival rates of lambs from birth
to weaning for the ®rst of the good years in 1991
(Inounu et al., 1993), Table 7, yields a distribution of
proli®cacy genotypes at weaning of FecJFFecJF/17;
FecJFFecJ‡/49; FecJ‡FecJ‡/34, and a frequency of
0.42 for FecJF. Subandriyo and Inounu (1994) studied
the ¯ock during the good years 1991±93. It is apparent
from the improved growth and survival rates, Tables 6
and 7 that nutrition was much better then, but there is
no information on management changes which might
also have contributed. The frequency distribution of
proli®cacy genotypes calculated above for the good
year 1991, from the results of Inounu et al. (1993), can
be applied to the observed litter size distribution in the
¯ock from 1991±93, Table 2, and the frequency distributions of litter sizes for each genotype in the good
years Subandriyo and Inounu (1994), Table 1, to
calculate the distribution of genotypes in the progeny
at birth. The values are FecJFFecJF/21; FecJFFecJ‡/
56; FecJ‡FecJ‡/23 giving a frequency of 0.49 for
FecJF. When the lamb survival rates from birth to
weaning in those years are applied, Table 7 (Subandriyo and Inounu, 1994), the distribution of genotypes
in the weaners becomes FecJFFecJF/20; FecJFFecJ‡/
54; FecJ‡FecJ‡/26 and a frequency of 0.47 for FecJF.
So if the higher level of husbandry is maintained, and
there is no planned selection against FecJF, it would be
expected that the frequency in the RIAP ¯ock will
continue to rise for some time.
2.8. ITT sheep in villages
Levels of nutrition and management vary between
and within villages (Knipscheer and Soedjana, 1982;
van Eye et al., 1984; Inounu et al., 1984; Tiesnamurti
et al., 1984). Mason (1980) lists nine student surveys
of litter sizes in villages in West Java. One result is
unrealistic with 75% twins, and the others give mean
s.d. values of singles 6816, twins 2814, triplets
44 and 0.1 quintuplets. Two of the results could have
indicated that the FecJF gene was not in the sample,
and no village gave values as high as those on institutional farms. An estimate of the average frequency of
FecJF in the villages, from Table 8, would be 0.1,
indicating a low level of husbandry. Nevertheless,
there are villages where husbandry is good (Tiesna-

J.A. Roberts / Small Ruminant Research 36 (2000) 215±226

murti et al., 1984), survival of lambs from birth to
weaning can be better than on instutional farms, Table
7 (Inounu et al., 1993), and there is a high proportion
of larger litters, Table 2 (Inounu et al., 1984; Subandriyo, 1986). There are other factors which may
in¯uence the results of village studies. Whereas record
keeping can be reliable on institutional farms where a
responsible person can check the animals daily, in
villages, data may be collected intermittently by an
outsider who can only obtain that information which
can be recalled by those who are willing to cooperate.
Moreover, culturally, villagers may provide information which they believe will please a guest, and village
people may have different perceptions, such as farmers generally not counting lambs which die within 3
days of birth (Bell and Inounu, 1982).

3. Comparisons with other proli®c breeds
As described above, the frequency of the proli®cacy
gene in ITT sheep is, in the main, an equilibrium
between the amplifying effect of the higher ovulation
rates of carrier ewes, balanced by lower survival rates
of the smaller lambs from litters with multiple lambs.
The equilibrium point is set by the level of husbandry
in the ¯ock which affects survival rates of lambs, and
perhaps litter sizes. A similar equilibrium might be
expected when proli®cacy is controlled by many
genes. In that case the frequencies of minor proli®cacy
genes would be in equilibrium with the survival rates
of lambs in larger litters, the equilibrium level being
modulated by the level of husbandry.
Of the proli®cacy genes with large effect in sheep,
none are known to be alleles, the Booroola gene is
linked to markers from a region of the human chromosome 4q (Montgomery et al., 1993), the Inverdale
gene of Romney sheep is on the X chromosome
(Fahmy and Davis, 1996) and the locations of the
Thoka gene of Icelandic sheep, the Olkuska gene and
FecJF of ITT sheep are not known. Ovulation rates are
a more direct measure of the effects of a proli®cacy
gene than are litter sizes, which are affected by
embryo wastage, which varies between breeds, Table
4. Breeds and synthetics into which a major proli®cacy
gene has been incorporated recently (Booroola, Cambridge and Belclare), tend to have wide ranges (1±14)
of ovulation rates (Bindon et al., 1996), whereas those

223

proli®c breeds which have evolved in small ¯ocks in
traditional societies, Romanov (Ricordeau et al.,
1990), D'man (Lahlou-Kassi and Marie, 1985), ITT
(Bradford et al., 1986) and Icelandic (Eythorsdottir et
al., 1991), regardless of whether proli®cacy is the
product of one or many genes, have compact ranges
(1±7) of ovulation rates, which may have evolved with
proli®cacy. Nevertheless, all of the proli®c breeds
have litter size ranges from 1 to 7, probably re¯ecting the common constraint of uterine ef®ciency
(Meyer, 1985). Ovulation rates and litter sizes of
different major proli®cacy genes are best compared
when the frequencies of the genes are known, or like
genotypes are available. Piper and Bindon (1996) have
selected for the proli®cacy gene within their Booroola
¯ock until the vast majority are homozygous carriers.
In the RIAP ¯ock of ITT sheep the ewes have been
retrospectively separated into genotypes on the basis
of their lifetime breeding records (Bradford et al.,
1991; Inounu et al., 1993; Subandriyo and Inounu,
1994). The mean litter sizes of the homozygous
carriers are comparable, Booroola 2.59 (Piper and
Bindon, 1996) and ITT 2.83 (Bradford et al., 1991).
However, there is a large difference between the
corresponding ovulation rates, Booroola 5.65 and
ITT 2.92, which re¯ects the means and variances of
ovulation rates discussed above.

4. Other small ruminants on Java
ITT sheep are the predominant breed of the wet
province of West Java, and Javanese fat tail (JFT)
sheep predominate in the drier province of East Java.
Both breeds of sheep have been on Java for centuries,
both are proli®c, and they have similar distributions of
litter size, Tables 2 and 10. The RIAP sheep are
referred to as a thin tail ¯ock, but approximately
20% of the genetic material came from JFT ewes
(Inounu et al., 1993). The ranges of the breeds overlap
in Central Java, and it is probable, but not certain, that
both breeds carry the same gene. There are two main
breeds of goat on Java, one a crossbred bean goat
(kambing kacang) which has been there for centuries,
and the other predominantly Jamnapari (Ettawah), a
more recent importation. Both are proli®c (Obst et al.,
1980), Table 10. So the animal husbandry environment on Java favours proli®cacy in small ruminants.

224

J.A. Roberts / Small Ruminant Research 36 (2000) 215±226

Table 10
Distributions of litter sizes in institutional ¯ocks of Javanese fat tail sheep and Javanese goats
Breed/species

Parity

JFT sheep
First
Second
Bean goat X
Jamnapari goat
a

Frequency distributions of litter sizes (%)
Single

Twin

Triplet

Quadruplet

51
51
52
46
50
25
32

43
33
42
33
35
46
55

5
14
6
20
12
24
13

1
2
0
0
3
5
0

Mean
litter size

Founding
stock

Reference

1.56
1.87
1.54
1.72
1.68
2.08
1.81

E. Java
Madura
E. Java

Wardojo and Adinata, 1956a
Obst et al., 1980
Bradford et al., 1986

Not stated
W. Java
C. Java

Iniguez and Gunawan, 1990
Obst et al., 1980
Obst et al., 1980

Data cited by Mason (1980).

5. Utility of ITT sheep
In a hot humid environment, ITT sheep are highly
productive (Reese et al., 1990; Iniguez et al., 1991;
Inounu et al., 1993). In a managed production program, it would be necessary to select the appropriate
mix of proli®cacy genotypes to optimise production
on the available feed (Bradford et al., 1991). Given the
lability of the frequency of FecJF, the equilibrium mix
of genotypes will respond to the level of husbandry
provided. If that mix is not that which is desired, then
the frequency could be maintained at a different level
by using rams of an appropriate carrier status. All
breeds in which a major gene for proli®cacy is segregating have the problem of rearing the large litters
produced by homozygous carrier ewes, and it unlikely
that a solution can be found in any realistic intensive
production system in a developing country. If a breed
is required for production of meat in a semi-intensive
system in the humid tropics, the ITT sheep offer
adaptation to hot wet climates, proli®cacy, 1.8 lambings per year and parasite resistance. Resistance of
ITT sheep against gastrointestinal nematodes is comparable with that of other resistant breeds (Romjali
et al., 1997), but there are still situations where
chemical control is bene®cial (Handayani and
Gatenby, 1988). ITT sheep have very high resistance
against Fasciola gigantica (Roberts et al., 1997a),
possibly controlled by a major gene (Roberts et al.,
1997b), which may be unique.
Acknowledgements
Opportunities to work for several years with
Indonesian colleagues in livestock industries on

ADAB, CIDA and ACIAR projects are greatly appreciated.
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