Animal Science 2003, 76: 119-136 1357-7298/03/22340119$20·00

© 2003 British Society of Animal Science

Resistance and resilience to gastro-intestinal nematode parasites and

relationships with productivity of Red Maasai, Dorper and Red
Maasai ✕ Dorper crossbred lambs in the sub-humid tropics
R. L. Baker1†, S. Nagda1, S. L. Rodriguez-Zas2, B. R. Southey2, J. O. Audho1, E. O. Aduda1 and W.
Thorpe1
1International LivestockResearch Institute (ILRI), PO Box 30709, Nairobi, Kenya
2Department of Animal Science, University of lllinois, Urbana-Champaign, USA

†E-mail : L.Baker@cgiar.org

Abstract
Resistance and resilience to naturally acquired gastro-intestinal (GI) nematode parasite infections (predominantly
Haemonchus contortus) were studied in 1785 lambs born over six lambings (1991 to 1996) consisting of 212 Red
Maasai, 311 Dorper and 1262 crossbred (Red Maasai-Dorper) lambs in the sub-humid coastal region of Kenya.
These lambs were the progeny of 41 Dorper and 35 Red Maasai rams. Live weights (LWT), blood packed cell volume
(PCV) and faecal egg counts (FEC) were recorded at 1- to 2-monthly intervals from birth until the lambs were
about one year of age. Red Maasai were more resistant and resilient post weaning to infections with GI nematodes
than Dorper lambs as shown by their significantly lower FEC and their significantly higher PCV, respectively. An
increasing proportion of Red Maasai genes in the crossbred lambs was associated with decreased FEC and higher
PCV, but there was no heterosis for logarithm-transformed FEC (LFEC) or PCV. From one month of age Red
Maasai lambs were significantly lighter than Dorper lambs by about 1 kg, but Red Maasai lambs had significantly
lower lamb mortality rate from birth to 12 months of age (proportionately 0·30 and 0·66, respectively). Heritability
estimates from a repeated measures analysis for records taken at 6 and 8 months of age were 0·14 (s.e. 0·05) for PCV
from an animal model and 0·12 (s.e. 0·05) for LFEC from a sire model. The heritability estimate for LFEC from a
repeated measures analysis including the four measurements recorded between 6 and 12 months of age was
significantly higher (P < 0·05) for Dorper-sired lambs (0·15, s.e. 0·05 for an animal model and 0·19, s.e. 0·07 for a
sire model) than for Red Maasai-sired lambs (0·00 and 0·01, s.e. 0·02). The phenotypic and genetic correlations
between PCV and LFEC were moderately to highly negative and averaged –0·34 and –0·81, respectively. None of
the genetic correlation estimates between LWT and PCV and LWT and LFEC for lambs post weaning were
significantly different from zero. The heritability estimates for PCV and LFEC have important implications for
within-breed genetic improvement programmes : for the Red Maasai, improvement should concentrate on resilience
(e.g. selection for high PCV); for the Dorper, selection should be feasible for both improved resistance (low FEC) and
resilience (high PCV).

Keywords: breed differences, genetic resistance, Haemonchus contortus, heritability, sheep.

Introduction follow polygenic inheritance, as do the production

There is ample evidence that genetic variation for
disease resistance in domestic animals exists (Owen
and Axford, 1991; Gray et al., 1995; Axford et al.,
1999). Genetic resistance to the important infectious
diseases of domestic livestock is usually found to
119
traits. Therefore, we are interested in estimating the
magnitude of genetic variation both among breeds or
strains and within breeds and ultimately utilizing
this genetic variation for host resistance in breeding
programmes (Woolaston and Baker, 1996).

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 120 Baker, Nagda, Rodriguez-Zas, Southey, Audho, Aduda and Thorpe
Current control methods for gastro-intestinal (GI)
nematode parasites (endoparasites) focus on
reducing contamination of pastures through
anthelmintic treatment and/or controlled grazing
(Barger, 1996 and 1999). In Africa, the use of these
control methods is limited by the high cost of
anthelmintics, their uncertain availability, increasing
frequency of drug resistance (Waller, 1997a) and
limited scope in many communal pastoral systems
for controlled grazing. It appears unlikely that new
broad-spectrum anthelmintics will be available in the
near future because of the major costs associated
with the development of new products (Geary et al.,
1999). To date, no commercial vaccines are available
to control GI nematode parasites (Smith, 1999).
Alternative approaches to control endoparasites are
therefore being considered (Barger, 1996; Waller,
1997b). One such approach is the characterization
and utilization of host genetic variation for resistance
or resilience to endoparasites.
Resistance is defined as the initiation and
maintenance of responses provoked in the host to
suppress the establishment of parasites and/or
eliminate parasite burdens. Resilience (or tolerance)
is defined as the ability of the host to survive and be
productive in the face of parasite challenge (Clunies-
Ross, 1932; Woolaston and Baker, 1996). The degree
of resistance has usually been assessed in terms of
worm counts at necropsy or faecal egg counts (FEC),
the measure of resistance used in this study, during
an infection period in live animals. In lambs it is well
documented that faecal egg counts are highly
correlated with worm counts (Woolaston and Baker,
1996). Resilience has been defined in terms of
productivity (e.g. live-weight gain or wool
production) under nematode challenge compared to
productivity in non-infected animals (Albers et al.,
1987). In New Zealand resilience has been defined as
the number of anthelmintic treatments required over
a given period of pasture challenge (usually several
months) with nematode parasites (Bisset and Morris,
1996). In this study we have used packed red cell
volume (PCV) and mortality rates as proxies for
resilience. When sheep are infected with the blood-
sucking parasite Haemonchus contortus they become
anaemic and this is measured by PCV, which is a
good indication of how the animal is managing to
cope with the pathogenic effects of the parasite and
survive when infected. However, other studies (e.g.
Albers et al., 1987) treated both FEC and PCV as two
different measures of resistance.
There have been many reports since the mid-1930s of
variation among breeds of sheep in resistance or
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resilience to GI nematode parasites, particularly to H.
contortus, Ostertagia spp. and Trichostrongylus spp.
Gray (1991) summarized and reviewed 23
publications on this subject and this was expanded to
34 studies in a review by Baker et al. (1992). A
number of indigenous ‘unimproved’ breeds of sheep
in Africa (Red Maasai, Djallonké and Sabi), the
Caribbean (St Croix and Barbados Blackbelly), North
America (Florida Native, Louisiana Native and
Navajo), India (Garole) and Indonesia (Javanese Thin
Tail) have been shown to be more resistant and/or
resilient to endoparasites relative to the breeds with
which they have been compared. There is now strong
evidence that the indigenous Red Maasai sheep of
East Africa are both more resistant and resilient to
naturally acquired and artificial infections with GI
nematode parasites than the breeds with which they
have been compared, and particularly to the highly
pathogenic abomasal worm, H. contortus (Preston
and Allonby, 1978 and 1979; Baker et al., 1994, 1998
and 1999; Baker, 1998; Mugambi et al., 1996 and 1997;
Wanyangu et al., 1997).
Most of the published within-breed genetic variation
estimates (i.e. heritabilities and genetic correlations)
for resistance or resilience to endoparasites in sheep
are from Merino or Romney sheep in Australasia
(Gray and Woolaston, 1991; Gray et al., 1995; Bisset
and Morris, 1996), but estimates have also been
reported from research undertaken in France (Bouix
et al., 1995), Scotland (Bishop et al., 1996) and Poland
(Bouix et al., 1998). Prior to the initiation of this study
by the International Livestock Centre for Africa
(ILCA, now ILRI) in 1991 there were no published
estimates of the heritability of resistance or resilience
to internal parasites in tropical sheep (ILCA, 1991;
Baker et al., 1992). In addition, there was very limited
evidence for tropical sheep or goats that related
genetic and phenotypic variation for resistance or
resilience to individual animal and flock
productivity.
This paper reports a 6-year study (1991 to 1996)
investigating both between-breed and within-breed
genetic resistance and resilience to endoparasites
(predominantly H. contortus) in Red Maasai, Dorper
and Red Maasai ✕ Dorper crossbred lambs in sub-
humid coastal Kenya. Preliminary results of this
study have been reported by Baker et al. (1994 and
1998) and Baker (1998). The performance of the ewes,
the dams of the lambs being evaluated in this study,
was reported by Baker et al. (1999), where it was
shown that the Red Maasai ewes were significantly
more resistant and resilient to GI nematode parasites
and more productive than Dorper ewes.
 Genetics of resistance and resilience to internal parasites in tropical lambs
Material and methods
Experimental site
This study was carried out at the Diani Estate farm
located 20 km south of Mombasa in the sub-humid
coastal region of Kenya. Rainfall is bimodally
distributed with rainy seasons in March-June and
October-December. Rainfall data were collected daily
at Diani Estate and over the 6-year study period
(1991-96) the average annual rainfall was 819 mm
(ranging from 425 mm in 1993 to 1237 mm in 1994).
The monthly mean maximum temperatures range
between 28 and 33°C, while relative humidity ranges
between 0·60 and 0·90 (Jaetzold and Schmidt, 1983).
The soils on the farm are sandy, well drained and are
characterized by very low levels of nitrogen and
phosphorus, organic matter, cation exchange and
water-holding capacity. The vegetation is composed
of natural pasture and bush, with Heteropogon
contortus and Hyparrhenia rufa the predominant
perennial grass species.
Experimental design and data recorded
Red Maasai (R) sheep are a fat-tailed, hair breed,
which is principally associated with the Maasai tribe,
and they are found in northern Tanzania and south-
central Kenya (Wilson, 1991). The Dorper breed was
developed in South Africa in the 1940s at the
Grootfontein College of Agriculture by interbreeding
F1 crosses between the Black Head Persian
(originally from Somalia) and Dorset Horn breeds
(Milne, 2000). The Dorper (D) has a reputation for
adaptability to harsh, arid conditions (Cloete et al.,
2000) and was first imported into Kenya from South
Africa in the 1960s. Dorper and Red
Maasai ✕ Dorper (sire breed ✕ dam breed) ewes
were already present at Diani Estate at the start of
the experiment in 1991. The Dorper flock was
established by Baobab Farm by backcrossing
purebred Dorper rams over a flock of about 300
Black Head Persian ewes starting in the late 1970s.
The Dorper rams were purchased from the flocks in
Kenya that were established by importing purebred
Table 1 Number of single-born lambs with birth weight by year of birth and breed/crossbreed
Breed/crossbreed†
1991 1992 1993
Dorper (D) 93 65
D ✕ (R ✕ D) 92 77
D✕R 0 7
R✕D 83 58
R ✕ (R ✕ D) 99 81
Red Maasai (R) 0 8
Total 367 296 372
† Sire breed ✕ dam breed.
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121
Dorper ewes and rams from South Africa and
Zimbabwe. It is estimated that the Dorper ewes used
in this experiment were at least third generation
backcrosses (i.e. 15/16 Dorper). The R ✕ D crossbred
ewes were bred by Baobab Farm between 1986 and
1990 for another experiment that investigated
various management interventions to control
endoparasite infections using both Dorper and R ✕ D
sheep (Bullerdiek, 1996). About 100 Red Maasai ewes
were purchased from pastoralists in south-central
Kenya in 1992. They were purchased from as wide a
range of flocks and owners as possible to ensure that
they were a representative genetic sample of the
breed. They were not selected on any particular
phenotypic characteristic, except that healthy sheep
in reasonable condition were purchased.
In the 1st year of the study (1991) the Dorper and
R ✕ D ewes were mated to 12 Dorper and 12 Red
Maasai rams in single-sire mating groups in a diallel
design. In the subsequent years (1992 to 1996) all
three ewe genotypes (Dorper, Red Maasai, R ✕ D)
were mated to 12 Dorper and 12 Red Maasai rams in
single-sire mating groups in a diallel design to
generate two purebred and four crossbred genotypes
(Table 1). Rams were joined with the ewes for a 6-
week period each year. About seven or eight new
rams of each breed were used at each mating so that
35 different Red Maasai rams and 41 different Dorper
rams were used over the entire study. All Dorper and
Red Maasai rams purchased were as unrelated as
possible to ensure a representative genetic sample.
Lambs were weighed as close to birth as possible,
usually within 24 h, and then as a group every
month up to weaning at an average age of 3 months.
All male lambs were castrated within two weeks
from birth. PCV and FEC were recorded on all lambs
at 1 and 2 months of age. If individual lambs had a
FEC greater than 2000 eggs per gram (e.p.g. ) and/or
a PCV less than 20% at these samplings, they were
treated with an anthelmintic drug. All the lambs
Year of birth
1994 1995 1996 Total
54 30 39 30 311
93 70 65 35 432
38 24 27 27 123
57 13 14 9 234
96 61 69 67 473
34 45 64 61 212
243 278 229 1785
 122 Baker, Nagda, Rodriguez-Zas, Southey, Audho, Aduda and Thorpe
were treated with an anthelmintic at weaning. They
were then grazed on pasture until a monitor group of
about 50 lambs (consisting of approximately equal
proportions of the six genotypes and the two sexes),
from which samples were taken every week, reached
a FEC averaging about 2000 e.p.g. All the lambs were
then weighed and faeces and blood samples were
taken on two consecutive days. All lambs were then
treated with an anthelmintic. This procedure was
repeated until the lambs reached about 1 year of age,
which involved five sampling times in all years
except 1994 and 1996. In 1994, the year with the
highest rainfall, there were eight post-weaning
samplings and in 1996 six samplings. No lambs were
drenched individually during any of the post-
weaning infection periods. Lambs and ewes were
allowed to graze from about 07:00 to 17:00 h and
then housed in a simple roofed shed for security
reasons. Most of the lambs that died had the cause of
death ascertained at a post-mortem examination
(Nguti et al., 2003).
Faecal egg counts were determined using the
modified McMaster method (Whitlock, 1948; Hansen
and Perry, 1994) with a lower limit of detection of 50
e.p.g. of faeces. PCV was measured by the
microhaematocrit method. At each sampling time,
faecal samples bulked by breed/crossbreed and sex
were cultured and the larvae identified (Hansen and
Perry, 1994). The larval differentiation averaged over
169 bulked cultures by breed/crossbreed and sex at
different sampling times showed that the
predominant larvae were H. contortus (mean 73%,
range 49 to 99%), Trichostrongylus spp. (mean 17%,
range 0 to 36%) and Oesophagostomum spp. (mean
7%, range 0 to 41%).
In the 2nd year of the experiment (1992) it was
ascertained that the GI nematode parasites of both
sheep and goats on this farm were resistant to both
Ivermectin and Fenbendazole (Mwamachi et al.,
1995). Therefore, all the lambs born from 1993
onwards were treated with Levamisole (Wormacid
Plus, Cosmos, Nairobi, Kenya) at the recommended
dose rate for sheep (i.e. 7·5 mg/kg live weight based
on the heaviest lamb at any sampling time) and this
anthelmintic treatment remained effective
throughout the rest of the experiment.
All ewes and lambs were sprayed every 2 weeks
with an acaricide (Triatix, Coopers, Kenya) to control
tick infestations and prevent tick-borne diseases.
Whenever the PCV fell below 20%, infections with
trypanosomes were monitored using the dark
ground/phase contrast buffy coat technique (Paris et
al., 1982). This was to ensure that the anaemia being
measured by PCV was due to H. contortus rather than
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to trypanosomosis, which also causes anaemia.
While there have been reports of trypanosomosis in
cattle on the same farm, no cases were diagnosed in
the sheep during this study.
Statistical analyses
The traits analysed at each sampling time were live
weight (LWT), PCV, and FEC. The records at birth, 1,
2 and 3 months of age were single records taken on
one day. The post-weaning records (i.e. those taken at
4·5, 6, 8, 10 and 12 months of age) were all averages
of the records taken on two consecutive days.
Because of a skewed distribution, FEC was analysed
using a logarithmic transformation (LFEC = log10
(FEC + 25)). The results were back-transformed by
taking anti-logarithms of the estimated means and
presented as geometric means (GFEC). All statistical
tests for FEC were applied to the transformed data.
LWT, PCV and LFEC at each sampling time (i.e. birth,
1, 2, 3, 4·5, 6, 8, 10 and 12 months of age) were
analysed with a mixed model analysis of variance
using restricted maximum likelihood (REML). The
ASREML programme of Gilmour et al. (1999) was
used to estimate simultaneously both fixed effects
and variance components. The model included
(when significant) the fixed effects of year of birth
(six classes, 1991-96), breed/cross (six classes – D, R,
D ✕ R, R ✕ D, D ✕ (R ✕ D), R ✕ (R ✕ D)), sex (two
classes, male and female), age of dam (four classes, 2,
3, 4, 5 + years of age), lamb age as a linear covariate
and any significant (P < 0·05) first-order interactions.
Only single-born lambs were analysed as very few
twin or multiple births were recorded
(proportionally 0·028 of the total number of lambs
born) and the majority of these died before weaning.
An animal model was fitted to the data recorded at
each sampling time and variance components and
heritabilities were estimated for the direct additive
and maternal effects. Because of the limited depth of
the pedigree structure of the data (i.e. for most lambs
just the sire and dam were known but not the
Table 2 Coefficients for expected genetic effects for each lamb breed
and crossbreed†
Lamb breed
crossbreed‡ GI GM HI HM
D✕D 1·0 1 0 0
D ✕ (R ✕ D) 0·5 0 0·5 1
D✕R 0 –1 1·0 0
R✕D 0 1 1·0 0
R ✕ (R ✕ D) –0·5 0 0·5 1
R✕R –1·0 –1 0 0
† Individual genetic (GI), maternal genetic (GM),
individual heterosis (HI) and maternal heterosis (HM) effects.
‡ Sire breed ✕ dam breed. D = Dorper; R = Red Maasai.
 Genetics of resistance and resilience to internal parasites in tropical lambs 123

grandparents or great grandparents), it was not
possible to separate the maternal effect into a genetic
component and a permanent environmental
component. Additional REML animal model
analyses were undertaken to estimate additive
heritability estimates for all traits for each sire breed
separately. The significance of the difference in
heritabilities between sire breeds was ascertained by
summing the variances of the two estimates and
assuming that the covariance between the two
breeds was zero. Repeated measures REML analyses
were also undertaken for PCV and LFEC for
combinations of different records measured after
weaning. In these analyses, the additive effect and
the permanent environmental effect among
measurement times were fitted as random effects.
Genstat (Payne et al., 1997) was used for mixed
model analyses in which sire and dam were fitted as
random effects and the same fixed effects were fitted
as above except that the breed/cross effect was
replaced with four multiple regression coefficients to
estimate the genetic effects shown in Table 2. The
genetic basis of crossbreeding is due to both additive
and non-additive effects (Dickerson, 1969). Following
an approach first used in an animal breeding setting
by Robison et al. (1981), additive genetic effects can
be determined by fitting coefficients indicating the
contribution of the parental breeds to the genes in the
lamb (GI – individual genetic effect) and its dam (GM
– maternal genetic effect) (Table 2). The non-additive
(heterosis) effects are indicated by coefficients
showing the proportion of loci in the lamb (HI –
individual heterosis effect) or its dam (HM – maternal
heterosis effect) with alleles originating from
different parental breeds. Heterosis can be due to
both genetic interactions within loci (dominance) and
between loci (epistasis), but the present study does
not include sufficient crossbred genotypes to be able
to estimate epistatic effects. The coefficients for both
the HI and the HM effects (Table 2) are based on the
assumption that a linear relationship exists between
dominance and the degree of heterozygosity.
Genetic and phenotypic correlations were estimated
using an animal model in the REML program
(AIREML) of Johnson and Thompson (1995) fitting
just the additive genetic random effect. Bivariate
analyses were undertaken for LWT and PCV, LWT
and LFEC and PCV and LFEC at each sampling time.
Because it was not possible to fit different fixed
effects for different traits in AIREML, all the
significant fixed effects for either trait and any
significant interactions for each pair of traits were
fitted in these analyses.
Lamb mortality was analysed by ASREML as a
binary trait (y = 0, 1 for dead or alive) using a logit
transformation (loge (y/(1-y)). Mortality was
assessed pre-weaning (birth to 3 months of age), post
weaning (3 months to 365 days of age) and from
birth to 365 days of age.
Results
Breed and crossbreed effects
Overall means and residual standard deviations
from the REML analyses for LWT, PCV and LFEC at
each measurement time are shown in Table 3.
Measurement times post weaning varied among
years because these depended on when the average
FEC reached about 2000 e.p.g. in the monitor group

Table 3 Overall means and residual standard deviations (s.d.) at the different sampling times for live weight (LWT, kg), packed cell volume
(PCV, percent), logarithm-transformed faecal egg count (LFEC = log10 (FEC (e. p. g. ) + 25)) and the geometric mean of faecal egg count
(GFEC, e. p. g. )

Range in LWT PCV LFEC GFEC

Sampling average
time (average age among Residual Residual Residual
age, days) years (days) No. Mean s. d. No. Mean s. d. No. Mean s. d. Mean

Pre-weaning
Birth 1785 2·4 0·52
1 month (34) 30-39 1580 6·4 1·44 1576 33·0 4·20 1143 1·79 0·56 62
2 months (66) 57-70 1526 8·7 2·02 1526 27·6 5·27 1437 2·83 0·60 676
3 months (92) 84-106 1432 10·7 2·25 1426 26·3 5·44 1169 2·87 0·53 741
Post weaning
4·5 months (132) 110-160 1274 11·4 2·15 1274 23·3 4·45 1255 3·26 0·39 1820
6 months (189) 139-233 1162 13·8 2·29 1162 23·1 3·66 1144 3·37 0·34 2328
8 months (245) 173-336 1075 14·8 2·21 1075 23·3 3·74 1068 3·33 0·30 2138
10 months (296) 208-389 1044 16·9 2·41 1044 24·6 3·66 1043 3·20 0·38 1585
12 months (369) 237-450 980 18·2 2·46 980 25·3 3·31 965 3·23 0·33 1698

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 124 Baker, Nagda, Rodriguez-Zas, Southey, Audho, Aduda and Thorpe

Table 4 Estimated means (standard errors in parentheses) by breed/crossbreed from mixed model restricted maximum likelihood analyses
for live weight (LWT, kg), packed cell volume (PCV, percent), logarithm transformed faecal egg count (LFEC), the geometric mean of faecal
egg count (GFEC, eggs per gram) and mortality rates (proportion) at the different sampling times

Trait and sampling time Breed/crossbreed†

Significance
Dorper (D) D ✕ (R ✕ D) D✕R R✕D R ✕ (R ✕ D) Red Maasai (R) of breed

LWT
Birth 2·53 (0·07) 2·50 (0·06) 2·51 (0·07) 2·35 (0·07) 2·30 (0·06) 2·28 (0·07) ***
1 month 6·7 (0·15) 6·7 (0·13) 6·4 (0·17) 6·4 (0·15) 6·3 (0·13) 5·9 (0·16) ***
2 months 9·0 (0·20) 9·0 (0·16) 8·8 (0·24) 8·8 (0·20) 8·7 (0·16) 8·0 (0·21) ***
3 months (weaned) 11·0 (0·19) 10·9 (0·16) 10·7 (0·25) 10·6 (0·20) 10·7 (0·15) 10·1 (0·21) *
4·5 months 11·8 (0·23) 11·8 (0·20) 11·4 (0·29) 11·3 (0·23) 11·3 (0·18) 10·7 (0·23) **
6 months 14·2 (0·35) 14·3 (0·33) 13·7 (0·41) 14·0 (0·35) 13·7 (0·32) 13·0 (0·35) **
8 months 15·2 (0·25) 15·1 (0·20) 14·7 (0·31) 14·9 (0·25) 14·7 (0·19) 13·9 (0·25) **
10 months 17·3 (0·29) 17·3 (0·23) 16·9 (0·35) 17·0 (0·28) 17·0 (0·21) 16·2 (0·28) *
12 months 18·4 (0·32) 18·4 (0·31) 18·3 (0·39) 18·6 (0·26) 18·2 (0·24) 17·5 (0·30) *
PCV
1 month 32·8 (0·35) 32·8 (0·30) 33·0 (0·43) 33·3 (0·37) 32·9 (0·29) 33·2 (0·38)
2 months 26·8 (0·50) 26·4 (0·43) 27·2 (0·61) 27·9 (0·52) 28·7 (0·42) 28·4 (0·52) ***
3 months (weaned) 24·2 (0·42) 25·7 (0·35) 26·7 (0·59) 26·4 (0·45) 27·1 (0·31) 27·8 (0·45) ***
4·5 months 21·9 (0·44) 22·0 (0·39) 22·3 (0·59) 23·6 (0·43) 24·7 (0·35) 25·3 (0·45) ***
6 months 21·9 (0·57) 21·9 (0·55) 22·2 (0·66) 23·7 (0·57) 24·1 (0·52) 24·6 (0·57) ***
8 months 22·3 (0·39) 22·2 (0·31) 22·5 (0·51) 23·8 (0·37) 24·3 (0·28) 24·7 (0·38) ***
10 months 23·9 (0·40) 23·6 (0·33) 23·7 (0·52) 25·1 (0·38) 25·4 (0·29) 25·7 (0·39) ***
12 months 24·4 (0·34) 24·6 (0·25) 25·1 (0·46) 25·8 (0·31) 25·7 (0·20) 26·3 (0·31) ***
LFEC (GFEC)
1 month 1·87 (0·04) 1·82 (0·04) 1·72 (0·06) 1·75 (0·05) 1·75 (0·03) 1·80 (0·05)
(74) (66) (53) (55) (55) (63)
2 months 2·82 (0·05) 2·84 (0·05) 2·85 (0·07) 2·85 (0·06) 2·77 (0·04) 2·76 (0·06)
(661) (692) (708) (708) (589) (575)
3 months (weaned) 2·92 (0·04) 2·98 (0·04) 2·87 (0·06) 2·79 (0·05) 2·81 (0·03) 2·83 (0·04)
(832) (955) (741) (617) (646) (676)
4·5 months 3·35 (0·04) 3·32 (0·04) 3·28 (0·05) 3·23 (0·04) 3·21(0·03) 3·16 (0·04)
(2239) (2089) (1905) (1698) (1622) (1445) ***
6 months 3·45 (0·05) 3·36 (0·05) 3·42 (0·06) 3·36 (0·05) 3·32 (0·05) 3·29 (0·05)
(2818) (2291) (2630) (2291) (2089) (1950) ***
8 months 3·37 (0·03) 3·38 (0·03) 3·40 (0·04) 3·27 (0·03) 3·25 (0·02) 3·29 (0·03)
(2344) (2399) (2512) (1862) (1778) (1950) ***
10 months 3·26 (0·04) 3·26 (0·03) 3·25 (0·05) 3·15 (0·04) 3·16 (0·03) 3·10 (0·04)
(1820) (1820) (1778) (1413) (1445) (1259) ***
12 months 3·30 (0·04) 3·23 (0·03) 3·30 (0·05) 3·17 (0·04) 3·17 (0·03) 3·19 (0·04)
(1995) (1660) (1995) (1479) (1479) (1549) **
Mortality
Pre-weaning 0·29 (0·03) 0·22 (0·02) 0·17 (0·03) 0·18 (0·03) 0·16 (0·02) 0·12 (0·02) **
Post weaning 0·53 (0·03) 0·41 (0·03) 0·33 (0·04) 0·28 (0·03) 0·17 (0·02) 0·21 (0·03) **
Birth to 12 months 0·66 (0·03) 0·53 (0·02) 0·44 (0·04) 0·42 (0·03) 0·31 (0·02) 0·30 (0·03) **

† Sire breed ✕ dam breed.

of lambs. Both the overall average age at each
measurement time and the range in mean age among
years are shown in Table 3. The quite large variation
among years for mean ages at each sampling time
was accounted for in the analyses by the significant
interaction between year and the lamb age covariate.
Additional analyses were also undertaken for LWT,
PCV and LFEC using the final measurement taken in
each year in an attempt to reduce the large between-
year variation in age at measurement. However, the
results were very similar to those for the fifth
sampling each year and are not, therefore, tabulated.
GFEC increased up to 6 months of age (2328 e.p.g.)
after which it reached a plateau. Conversely, PCV
decreased with age pre-weaning, reached a plateau
post weaning at about 23% from 4·5 to 8 months of
age and then gradually increased after that.
Estimated means for each of the six breed/
crossbreeds for LWT, PCV, LFEC and mortality are
shown in Table 4 and the estimates of individual and
maternal additive genetic and heterosis effects in

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 Genetics of resistance and resilience to internal parasites in tropical lambs 125

Table 5 Estimates of individual genetic (GI), maternal genetic (GM), individual heterosis (HI) and maternal heterosis (HM) effects (standard
errors in parentheses) for live weight (LWT, kg), packed cell volume (PCV, percent), logarithm transformed faecal egg count (LFEC) and
mortality rates (proportion) at the different sampling times

Trait and sampling time GI GM HI HM

LWT
Birth 0·20 (0·03)*** –0·08 (0·03)** 0·03 (0·03) –0·03 (0·03)
1 month 0·31 (0·07)*** –0·01 (0·08) 0·09 (0·10) 0·10 (0·09)
2 months 0·42 (0·12)*** 0·01 (0·12) 0·24 (0·15) 0·18 (0·13)
3 months (weaned) 0·34 (0·13)*** 0·04 (0·14) 0·08 (0·17) 0·17 (0·15)
4·5 months 0·51 (0·14)*** –0·01 (0·15) 0·12 (0·18) 0·22 (0·15)
6 months 0·51 (0·16)*** 0·10 (0·17) 0·28 (0·20) 0·26 (0·16)
8 months 0·42 (0·17)*** 0·20 (0·16) 0·23 (0·20) 0·21 (0·16)
10 months 0·39 (0·19)*** 0·12 (0·18) 0·18 (0·23) 0·29 (0·17)
12 months 0·38 (0·21)*** 0·10 (0·19) 0·40 (0·25) 0·20 (0·18)
PCV
1 month –0·23 (0·25)*** 0·10 (0·24) 0·16 (0·32) –0·22 (0·22)
2 months –1·84 (0·36)*** **0·69 (0·31)* –0·15 (0·41) –0·03 (0·28)
3 months (weaned) –1·47 (0·30)*** –0·28 (0·31) –0·61 (0·43) 0·12 (0·31)
4·5 months –2·51 (0·29)*** *0·72 (0·29)* –0·62 (0·39) 0·14 (0·27)
6 months –2·12 (0·29)*** * 0·83 (0·25)** –0·32 (0·34) –0·02 (0·22)
8 months –1·98 (0·27)*** 0·67 (0·26)* –0·34 (0·36) –0·06 (0·24)
10 months –1·70 (0·28)*** * 0·79 (0·26)** –0·45 (0·36) –0·10 (0·24)
12 months –1·12 (0·25)*** 0·27 (0·25) –0·23 (0·34) –0·35 (0·22)
LFEC
1 month 0·05 (0·04)*** –0·01 (0·03) –0·09 (0·05) –0·00 (0·03)
2 months 0·11 (0·03)*** –0·05 (0·03) 0·08 (0·05) 0·03 (0·03)
3 months (weaned) 0·05 (0·03)*** –0·02 (0·03) –0·05 (0·05) –0·02 (0·03)
4·5 months 0·12 (0·03)*** –0·02 (0·03) 0·00 (0·03) 0·01 (0·02)
6 months 0·07 (0·02)*** –0·01 (0·02) 0·01 (0·03) –0·03 (0·02)
8 months 0·13 (0·02)*** ***–0·08 (0·02)*** 0·00 (0·03) –0·02 (0·02)
10 months 0·12 (0·03)*** –0·04 (0·03) 0·01 (0·04) 0·02 (0·02)
12 months 0·09 (0·03)*** *–0·05 (0·02)* –0·02 (0·03) –0·03 (0·02)
Mortality
Pre-weaning 0·07 (0·02)*** –0·02 (0·03) 0·01 (0·03) –0·01 (0·02)
Post-weaning 0·22 (0·03)*** –0·01 (0·03) –0·05 (0·04) –0·00 (0·03)
Birth to 12 months 0·22 (0·03)*** –0·02 (0·03) –0·04 (0·04) –0·00 (0·03)

† The GI and GM additive genetic effects are for the Dorper breed so the Red Maasai effects are of the opposite sign – see Table
2 for the coefficients used.

Table 5. Dorper lambs were significantly heavier than
Red Maasai lambs from birth to 12 months of age
(Table 4). There was a maximum difference between
the two purebreeds averaging 1·25 kg in 6- and 8-
month-old lambs (proportionately an advantage of
about 0·09). The highest GI estimates for LWT were
0·51 kg for 4·5- and 6-month-old lambs (Table 5)
indicating an estimated breed effect of 1·02 kg (Table
5). To establish the average breed difference from the
GI and the GM effects the estimates in Table 5 must be
doubled (i.e. the Dorper was coded as + 1 and the
Red Maasai as –1 in the coefficients used, Table 2).
All the GM effects were small and not significant
(P > 0·05) except for the significant (P < 0·01) estimate
for birth weight of –0·08 kg. This indicated that Red
Maasai dams gave birth to lambs that were 0·16 (s.e.
0·06) kg heavier than lambs from Dorper dams, in
contrast to the 0·40 (s.e. 0·06) kg advantage for the
Dorper lambs for the individual genetic effect. None
of the individual and maternal heterosis effects for
LWT was significant (P > 0·05).
Resistance to GI nematode parasites was manifested
by significant breed/crossbreed differences for LFEC
in lambs from 4·5 to 12 months of age with the Red
Maasai and 3⁄4 Red Maasai lambs having significantly
(P < 0·001) lower LFEC than the Dorper and 3⁄4
Dorper lambs (Table 4). This was associated with
significant individual genetic effects while the
maternal genetic effects were smaller and generally
not significant (Table 5). There was also evidence for
resilience to the endoparasite infection as shown by
significantly higher PCV (P < 0·001) in Red Maasai
and 3⁄4 Red Maasai lambs than in Dorper and 3⁄4

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 126 Baker, Nagda, Rodriguez-Zas, Southey, Audho, Aduda and Thorpe

Dorper lambs from 2 to 12 months of age (Table 4).
These differences were primarily associated with
highly significant (P < 0·001) GI effects which,
corrected for the GM effects, reached a maximum
value of 2·51 (s.e. 0·29) percentage units in favour of
the Red Maasai (i.e. an estimated breed difference of
5·02 percentage units) at 4·5 months of age (Table 5).
There were, however, in contrast smaller, but
significant (P < 0·05), GM effects for lambs from 4·5 to
10 months of age, which favoured lambs from
Dorper dams rather than Red Maasai dams. The
largest GM effect was 0·83 (s.e. 0·25) percentage units
for 6-month-old lambs (i.e. an estimated breed effect
of 1·66 percentage units). Neither the individual nor
maternal heterosis effects were significant for LFEC
and PCV (Table 5).
Another measure of resilience to endoparasite
infections is lamb mortality rate, especially when a
high proportion of the mortality can be attributed to
GI nematode infections (and specifically in this study
to H. contortus infections). This was the case for post-
weaning mortality for which proportionately 0·48 of
all deaths in the period from weaning (3 months) to
365 days of age were due to GI nematode infections
(Nguti et al., 2003). There was a highly significant
(P < 0·001) breed/crossbreed effect for the rates of
pre-weaning, post-weaning and total (from birth to
365 days of age) mortality with the Red Maasai and
3⁄ Red Maasai lambs having a much lower mortality
4
rate than Dorper or 3⁄4 Dorper lambs (Table 4). This
difference was entirely due to the highly significant
individual genetic effect. The GI estimate for total

Table 6 Additive heritability (h2a) and maternal effect (m) estimates (standard errors in parentheses) for live weight (LWT, kg), packed cell
volume (PCV, percent), logarithm-transformed faecal egg count (LFEC) and lamb mortality from animal model REML analyses

Total data set Analysis by sire breed†

Trait and sampling time No. h2a m Dorper h2a Red Maasai h2a

LWT
Birth 1785 0·08 (0·03)** 0·40 (0·03)*** 0·07 (0·05) 0·08 (0·05)
1 month 1580 0·02 (0·03) 0·26 (0·03)*** 0·10 (0·07) 0·02 (0·04)
2 months 1526 0·08 (0·04)* 0·26 (0·03)*** 0·11 (0·07) 0·09 (0·06)
3 months (weaned) 1432 0·06 (0·04) 0·30 (0·04)*** 0·04 (0·06) 0·09 (0·06)
4·5 months 1274 0·11 (0·05)* 0·27 (0·04)*** 0·18 (0·11) 0·05 (0·05)
6 months 1162 0·15 (0·06)* 0·30 (0·04)*** 0·17 (0·11) 0·10 (0·06)
8 months 1075 0·17 (0·07)* 0·24 (0·05)*** 0·23 (0·15) 0·13 (0·08)
10 months 1044 0·21 (0·08)** 0·21 (0·05)*** 0·20 (0·15) 0·18 (0·09)*
12 months 980 0·24 (0·09)** 0·17 (0·05)*** 0·20 (0·15) 0·23 (0·10)*
PCV
1 month 1576 0·04 (0·04) 0·04 (0·03) 0·06 (0·06) 0·05 (0·05)
2 months 1526 0·10 (0·05) 0·00 (0·03) 0·18 (0·09) 0·03 (0·05)
3 months (weaned) 1426 0·01 (0·03) 0·06 (0·04) 0·03 (0·06) 0·03 (0·05)
4·5 months 1274 0·05 (0·05) 0·07 (0·04) 0·11 (0·10) 0·02 (0·05)
6 months 1162 0·16 (0·06)** 0·00 (0·04) 0·17 (0·12) 0·14 (0·08)
8 months 1075 0·07 (0·06) 0·02 (0·04) 0·18 (0·13) 0·06 (0·06)
10 months 1044 0·12 (0·07) 0·01 (0·04) 0·32 (0·16) 0·02 (0·05)
12 months 980 0·07 (0·06) 0·00 (0·04) 0·10 (0·12) 0·10 (0·09)
LFEC
1 month 1143 0·01 (0·04) 0·00 (0·04) 0·00 (0·05) 0·00 (0·05)
2 months 1441 0·01 (0·04) 0·00 (0·04) 0·00 (0·06) 0·05 (0·06)
3 months (weaned) 1169 0·02 (0·04) 0·00 (0·04) 0·05 (0·07) 0·04 (0·06)
4·5 months 1255 0·08 (0·05) 0·00 (0·04) 0·05 (0·05) 0·05 (0·05)
6 months 1144 0·02 (0·04) 0·00 (0·04) 0·17 (0·11) 0·00 (0·05)
8 months 1068 0·09 (0·05) 0·00 (0·04) 0·31 (0·14)* 0·00 (0·05)
10 months 1043 0·03 (0·05) 0·01 (0·04) 0·15 (0·12) 0·00 (0·05)
12 months 963 0·03 (0·05) 0·00 (0·04) 0·29 (0·16) 0·00 (0·05)
Mortality
Pre -weaning 1785 0·00 (0·09) 0·18 (0·09)* 0·00 (0·24) 0·07 (0·23)
Post weaning 1442 0·10 (0·15) 0·06 (0·14) 0·18 (0·14) 0·00 (0·12)
Birth to 12 months 1785 0·06 (0·09) 0·17 (0·09) 0·19 (0·12) 0·03 (0·11)

† The h2a estimates for LWT and mortality rates were derived from a REML animal model which fitted both the additive and
maternal effects while the h2a estimates for PCV and LFEC were derived from a model just fitting the additive effect.

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 Genetics of resistance and resilience to internal parasites in tropical lambs 127

mortality rate was 0·22 (s.e. 0·03), which converts to
an estimated breed effect of 0·44 (Table 5). Neither
the maternal genetic effect nor the heterosis effects
were significant (P > 0·05) for mortality rates.
Genetic parameters
Heritabilities were estimated for LWT, PCV and
LFEC at each measurement time and for lamb
mortality rate pre- and post weaning and overall
(birth to 12 months) using an animal model (Table 6).
A heritability estimate derived from the average of
two records taken on two consecutive days (as was
the case for all the post-weaning measurements) is
expected to be higher than if it had been derived
from a single record (which was the case for the
weaning records and the pre-weaning records). The
increased accuracy of heritabilities from repeated
measurements is a function of both the number of
measurements (n) and the repeatability (r) among
measurement times. The heritability of n measures is
n/[1 + (n-1)r] times the heritability of one measure
(Falconer, 1989). It can be seen that the benefit of
repeated measurements is greater when the
repeatability is low. The repeatability estimates
between the measurements on two consecutive days
averaged over the five post-weaning measurement
times were 0·96 for LWT, 0·74 for PCV and 0·63 for
LFEC. These moderate to high repeatabilities
indicate that the expected increase in heritability
from analysing a mean of two measurements was
small for LWT (2%) and moderate for PCV and LFEC
(15 to 20%).
In the total data set (where variance components
were pooled across sire breeds), the heritability
estimates for LWT from birth to weaning were low
(less than 0·10) and then steadily increased post
weaning with the highest estimate being that for 12-
month-old lambs (0·24, s.e. 0·09). The maternal effect
for LWT was significantly (P < 0·001) different from
zero at all ages and declined from a value of 0·40 (s.e.
0·03) at birth to 0·17 (s.e. 0·05) for 12-month-old
lambs. There was no evidence at any individual
sampling time that heritability estimates for LWT
were significantly different between sire breeds
(Table 6). However, the trend in heritability estimates
with age post weaning (i.e. from 4·5 to 12 months of
age) was different for the two sire breeds. The
estimates for Dorper-sired lambs were very similar
post weaning (ranging from 0·17 to 0·23), while there
was a significant (P < 0·01) linear increase in the
estimates across sampling times (0·04, s.e. 0·01) for
Red Maasai-sired lambs from 0·05 (s.e. 0·05) at 4·5
months of age to 0·23 (s.e. 0·10) at 12 months of age.
Although not tabulated the maternal effects for LWT
estimated separately by sire breed were almost
identical from birth to weaning. After weaning the
magnitude of the maternal effects declined faster in
Dorper-sired lambs than Red Maasai-sired lambs
with estimates of 0·08 (s.e. 0·08) and 0·20 (s.e. 0·07) at
12 months of age, respectively.
None of the heritability estimates for mortality rate
in the total data set were significantly different from
zero (Table 6). Heritability estimates for post-
weaning and for total mortality rates were higher for
Dorper-sired than Red Maasai-sired lambs, although
not significantly so. Conversely, the maternal effects
(not tabulated) for post-weaning and total mortality
rates were significant for Red Maasai-sired lambs

Table 7 Additive heritability (h2a) and permanent environment (PE) estimates (standard errors in parentheses) from repeated measures
animal model (AM) and sire model (SM) restricted maximum likelihood analyses for packed cell volume (PCV) and logarithm-transformed
faecal egg count (LFEC)

Total data set Dorper-sired Red Maasai-sired

Trait and sampling time h2a PE h2a h2a

PCV (AM)
4·5 and 6 months 0·14 (0·05)** 0·35 (0·05)*** 0·12 (0·08) 0·09 (0·05)
6 and 8 months 0·14 (0·05)** 0·25 (0·05)*** 0·17 (0·09)* 0·11 (0·06)
6, 8 and 10 months 0·16 (0·04)*** 0·25 (0·04)*** 0·21 (0·09)* 0·09 (0·05)*
6, 8, 10 and 12 months 0·11 (0·04)** 0·23 (0·04)*** 0·17 (0·08)* 0·08 (0·04)*
LFEC (AM)
4·5 and 6 months 0·05 (0·03) 0·01 (0·04) 0·06 (0·05) 0·03 (0·03)
6 and 8 months 0·05 (0·03) 0·03 (0·04) 0·13 (0·07) 0·00 (0·03)
6, 8 and 10 months 0·06 (0·03)* 0·07 (0·03)* 0·15 (0·06)* 0·02 (0·02)
6, 8, 10 and 12 months 0·06 (0·02)** 0·05 (0·02)* 0·15 (0·05)* 0·00 (0·02)
LFEC (SM)
4·5 and 6 months 0·09 (0·04) 0·02 (0·04) 0·07 (0·06) 0·05 (0·04)
6 and 8 months 0·12 (0·05)* 0·06 (0·04) 0·18 (0·09)* 0·02 (0·04)
6, 8 and 10 months 0·12 (0·04)** 0·10 (0·02)*** 0·19 (0·08)* 0·03 (0·03)
6, 8, 10 and 12 months 0·10 (0·03)*** 0·08 (0·03)* 0·19 (0·07)** 0·01 (0·02)

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 128 Baker, Nagda, Rodriguez-Zas, Southey, Audho, Aduda and Thorpe
(0·34, s.e. 0·12 and 0·25, s.e. 0·12, respectively) but
both estimates were zero for Dorper-sired lambs.
The heritability and maternal effect estimates in the
total data set for PCV and LFEC at individual
sampling ages were small and not significantly
different from zero, with the exception of a
significant heritability estimate of 0·16 (s.e. 0·06) for
PCV in 6-month-old lambs (Table 6). The heritability
estimates for LFEC for lambs from 6 to 12 months of
age sired by Dorper rams ranged from 0·15 to 0·31
compared with 0·00 for Red Maasai-sired lambs,
although none of the Dorper estimates were
significantly different from zero (P > 0·05). None of
the differences in heritability estimates by sire breed
for either LFEC or PCV at any individual sampling
time was significant (P > 0·05). The trends in
heritability estimates in Table 6 (e.g. higher estimates
for LFEC post weaning than pre-weaning for Dorper-
sired lambs) were not due to the fact that each post-
weaning measurement was the average of
measurements on two consecutive days. Analysis of
the individual records (not tabulated) gave similar
results to the mean of two records, although as
expected the estimates had slightly larger standard
errors.
To investigate further the apparent contrast in the
heritability estimates of Dorper and Red Maasai
lambs between 6 and 12 months, repeated measures
REML analyses were undertaken for PCV and LFEC
for different combinations of all the post-weaning
measurements (Table 7). For PCV and LFEC the pair-
wise genetic correlations (Table 8) among post-
weaning measurement times were reasonably high
(and not significantly different from one) and,
therefore, these repeated measurements could be
considered as predictors of the same trait. The
repeated measures REML analyses for PCV and
LFEC included both the additive genetic effect and a
permanent environmental effect among
measurement times as random effects in the model
but ignored the maternal effect as this was not
significant (Table 6). The repeatability among
measurement times is the sum of the genetic and
environmental effects and can be easily derived from
Table 7, although it is not tabulated explicitly. All of
the heritability estimates in Table 6 were derived
from animal model REML analyses. Heritability
estimates were also estimated using a REML sire
model and for LWT, PCV and mortality rates the
estimates were very similar to those in Table 6.
However, for LFEC the sire model estimates were
consistently a little higher than those from the animal
model and this difference was seen most clearly in
the repeated measures analyses. Therefore, the
results from only the animal model repeated
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measures analyses for PCV are presented in Table 7,
while the results from both the animal model and
sire model analyses are presented for LFEC.
The repeated measures analyses for PCV in the total
data set yielded heritability estimates which were
significantly different from zero and which ranged
from 0·11 to 0·16 (Table 7). The heritability estimates
for PCV were consistently higher in Dorper-sired
lambs than in the Red Maasai-sired lambs, but this
difference was not significant for any combination of
repeated measurements. Except for the analysis
combining the 4·5- and 6-month measurements, all
the heritabilities for PCV for the Dorper-sired lambs
were significantly different from zero (range 0·17 to
0·21), while for the Red Maasai-sired lambs only the
estimates including 3 or 4 traits as repeated measures
were significantly different from zero. The
permanent environmental effect was significant
(P < 0·001) for all the PCV analyses. The repeatability
for PCV ranged from 0·34 to 0·49. The animal model
repeated measures analyses for LFEC in the total
data set showed that the heritability estimates were
only significantly (P < 0·05) different from zero for
the analyses which combined the 6-, 8- and 10-month
measurements and that which combined all 4
measurements between 6 and 12 months of age
(Table 7). However, the heritability estimate from the
sire model was also significant when the 6- and 8-
month measurements were combined. Both the
animal model and sire model heritability estimates
for LFEC were higher for the Dorper-sired than the
Red Maasai-sired lambs, and significantly (P < 0·05)
so when the four measurements between 6 and 12
months of age were included in the analysis (0·19 v.
0·01, respectively for the sire model estimates). The
permanent environment effect in the total data set
was small and not always significantly different from
zero (P > 0·05) for LFEC. The repeatability estimates
for LFEC ranged from 0·06 to 0·22 and the sire model
estimates were consistently higher than the animal
model estimates. The differences observed for the
heritabilities of PCV and LFEC for Dorper-sired
compared to Red Maasai-sired lambs in Table 7 were
due to differences in the genetic variance rather than
differences in the environmental variance. For
example, in the analysis of LFEC, with the 6-, 8-, 10-
and 12-month measurements included, the genetic
and environmental variances were 0·00011 and 0·115,
respectively for Red Maasai-sired lambs and 0·023
and 0·106 for Dorper-sired lambs, respectively.
Genetic and phenotypic correlations among
measurements taken at 4·5, 6, 8, 10 and 12 months of
age for PCV and LFEC are presented in Table 8. The
genetic correlation estimates were moderate to high
for LFEC (average 0·83) but only two estimates were
 Genetics of resistance and resilience to internal parasites in tropical lambs 129

Table 8 Genetic (Rg) and phenotypic (Rp) correlation estimates (standard errors in parentheses) for packed cell volume (PCV) and logarithm-
transformed faecal egg count (LFEC) among measurements at 4·5, 6, 8, 10 and 12 months of age from bivariate animal model REML
analyses

PCV LFEC

Measurement times correlated Rg Rp† Rg Rp

4·5 and 6 months 0·76 (0·19)*** 0·50 (0·02) 1·00 (0·53) 0·08 (0·03)**
4·5 and 8 months 1·00 (0·23)*** 0·41 (0·03) 0·76 (0·42) 0·05 (0·03)
4·5 and 10 months 1·00 (0·22)*** 0·30 (0·03) 1·00 (0·52) 0·02 (0·03)
4·5 and 12 months 0·40 (0·51)*** 0·21 (0·03) 0·17 (0·80) 0·04 (0·03)
6 and 8 months 0·95 (0·23)*** 0·48 (0·02) 0·88 (0·60) 0·16 (0·03)***
6 and 10 months 0·83 (0·21)*** 0·40 (0·03) 1·00 (0·66) 0·11 (0·03)***
6 and 12 months 0·45 (0·35)*** 0·28 (0·03) 0·79 (0·88) 0·06 (0·03)*
8 and 10 months 1·00 (0·14)*** 0·53 (0·02) 1·00 (0·47)* 0·22 (0·03)***
8 and 12 months 1·00 (0·31)*** 0·30 (0·03) 0·67 (0·73) 0·17 (0·03)***
10 and 12 months 0·99 (0·35)*** 0·32 (0·03) 1·00 (0·48)* 0·16 (0·03)***

† All estimates in this column are significantly different from zero (P < 0·001).

significantly (P < 0·05) different from zero. All but
two of the genetic correlation estimates were
significantly (P < 0·001) different from zero for PCV
(average 0·84). Phenotypic correlations for PCV were
all significantly (P < 0·001) different from zero and
averaged 0·37, but the average phenotypic
correlation for LFEC was lower (0·11) and three of
these estimates were not significantly different from
zero. Both the genetic and phenotypic correlation
estimates were higher for two consecutive
measurement times than those between more distant
measurement times (e.g. 4·5 and 12 months and 6 and
12 months). Genetic and phenotypic correlations
among LWT, PCV and LFEC at each measurement
time from 2 to 12 months of age are shown in Table 9.
All phenotypic correlations between LWT and PCV
were significantly (P < 0·001) different from zero
(average 0·33), but, except at 2 months of age, not the
corresponding genetic correlations. The post-
weaning phenotypic correlations between LWT and
LFEC averaged –0·11 and were all significant
(P < 0·001), except for the estimate at 6 months, but
none of the genetic correlations was significantly
different from zero. Phenotypic correlations between
PCV and LFEC were all significant (P < 0·001) and
averaged –0·34. The genetic correlation for PCV and
LFEC was only estimable at five sampling times and
two of these estimates were significant (P < 0·001).
The average of the five genetic correlation estimates
for PCV and LFEC was –0·81. Because of the small
data set and the low estimate of genetic variance for
LFEC in Red Maasai-sired lambs it is difficult to
make any meaningful comparisons between sire
breeds for the genetic correlation between PCV and
LFEC. Nevertheless, the genetic covariance between
PCV and LFEC was consistently lower in Red
Maasai-sired lambs than in Dorper-sired lambs (e.g.
–0·04 and –0·20 respectively for the 8-month
measurement). The heritability estimates from these
bivariate analyses for LWT, PCV and LFEC (not
tabulated) were very similar to those in Table 6
derived from univariate analyses.

Table 9 Genetic and phenotypic correlation estimates (standard errors in parentheses) among live weight (LWT), packed cell volume (PCV)
and logarithm-transformed faecal egg count (LFEC) at each measurement age from bivariate animal model REML analyses

Sampling Genetic correlations Phenotypic correlations

time
(months) LWT-PCV LWT-LFEC PCV-LFEC LWT-PCV LWT-LFEC PCV-LFEC

2 0·48 (0·16)** n. e. n. e. 0·31 (0·03)*** 0·02 (0·03) –0·28 (0·02)***

3 0·29 (0·30) –0·41 (0·28) –0·63 (0·58) 0·38 (0·02)*** –0·03 (0·03) –0·33 (0·03)***
4·5 0·19 (0·24) –0·20 (0·26) –0·98 (0·24)*** 0·44 (0·02)*** –0·14 (0·03)*** –0·47 (0·02)***‘
6 0·18 (0·17) –0·19 (0·37) –0·72 (0·42) 0·34 (0·03)*** –0·03 (0·03) –0·24 (0·03)***
8 0·04 (0·25) –0·14 (0·24) –0·96 (0·27)*** 0·34 (0·03)*** –0·11 (0·03)*** –0·36 (0·03)***
10 0·19 (0·22) –0·07 (0·43) –0·77 (0·56) 0·29 (0·03)*** –0·12 (0·03)*** –0·42 (0·03)***
12 0·17 (0·34) –0·37 (0·54) n. e. 0·20 (0·03)*** –0·15 (0·03)*** –0·31 (0·03)***

n. e. Not estimable – analysis did not converge.

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 130 Baker, Nagda, Rodriguez-Zas, Southey, Audho, Aduda and Thorpe
Discussion
Breed differences for resistance to endoparasites and for
productivity
The results of this study confirm those of previous
studies (Preston and Allonby, 1978 and 1979;
Mugambi et al., 1996 and 1997; Wanyangu et al., 1997;
Baker et al., 1999) which showed that Red Maasai
sheep were more resistant and resilient to
endoparasites (predominantly H. contortus) than
Dorper and a number of other sheep breeds (e.g.
Hampshire, Corriedale, Merino and Romney). It is
interesting that significant breed differences for PCV
(i.e. resilience) occurred first in 2-month-old lambs
while significant breed differences for FEC
(resistance) occurred first in 4·5-month-old lambs.
For both PCV and FEC these breed differences then
persisted through to the yearling measurement and
were also manifested in the ewes (Baker et al., 1999).
This relatively early onset of both resilience and
resistance in Red Maasai lambs is in contrast to more
susceptible breeds such as the Romney and Merino
in which resistance (sometimes referred to as ‘self-
cure’ and manifested as a clear decline in egg counts
and worm burdens due to the development of
immunological competence) has been shown to be
first manifested at about 6 months of age (Colditz et
al., 1996). However, other resistant breeds show the
same early onset of resistance. The resistant Gulf
Coast Native sheep first manifested significantly
lower FEC than susceptible Suffolk lambs at 2
months of age when infected with H. contortus
(Bahirathan et al., 1996). Relative to susceptible
Dorset Horn lambs, resistant St Croix lambs
naturally and experimentally infected with H.
contortus first manifested resistance (assessed by FEC
and worm counts) at 3 to 4 months of age (Gamble
and Zajac, 1992).
None of the previous studies related resistance and
resilience to productivity. In the hot humid
conditions which apply at the Kenya coast, the
Dorper lambs only had a small advantage in growth
rate over the Red Maasai lambs. This contrasts with
the much larger advantage in growth rate observed
in other studies in Kenya undertaken in semi-arid
environments (Inyangala et al., 1992; Kiriro,
1994 : Baker et al., 2002). Similarly, the very high
mortality rates observed for Dorper lambs at the
Kenyan coast were not found in semi-arid climates in
Kenya (Baker et al., 2002) or South Africa (Cloete et
al., 2000; Schoeman, 2000). About one-fifth of the
deaths pre-weaning and about a half of the deaths
post weaning were associated with endoparasite
infections (predominantly H. contortus infections) as
ascertained by post-mortem examination (Nguti et
al., 2003). These results suggest that not only is the
Dorper breed susceptible to endoparasites, but it is
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also poorly adapted to hot humid conditions. This
finding is not surprising because the Dorper breed
was originally bred in South Africa for use in arid
veld conditions, which are characterized by high
altitude, extremely high summer temperatures, and
cold and wet conditions in other seasons (Milne,
2000; Cloete et al., 2000; Schoeman, 2000).
The breed differences for resistance (FEC) and
resilience (PCV) to endoparasites estimated in this
study are probably underestimates of the true genetic
differences. Firstly, all the lambs were grazed and
managed together to meet the requirements of a
valid breed comparison for the production traits. If,
however, each breed and crossbreed group had been
grazed in separate paddocks at the same stocking
rate, the resistant genotypes (i.e. the Red Maasai and
the 3⁄4 Red Maasai) would have had a lower exposure
to endoparasites than they experienced in this study.
The magnitude of this effect was demonstrated by
Bisset et al. (1997) in a New Zealand study which
showed that nemotode larval infestation levels on
pasture were about five-fold greater on a farmlet
grazed by susceptible genotype Romney female
lambs than on a separate farmlet grazed by resistant
genotype Romney female lambs. This resulted in
about a 50-fold greater FEC in susceptible compared
to resistant lambs, which was considerably greater
than in their male half-siblings grazed together.
Secondly, the very high mortality rate in this study,
particularly for the Dorper and 3⁄4 Dorper lambs,
meant that the surviving lambs were the more
resilient and resistant animals within each genotype
which would have tended to have higher PCV and
lower FEC than those that died (Nguti et al., 2003).
The underestimation of the breed effect is likely to be
more marked for PCV than FEC because of the
higher average phenotypic correlation for PCV (0·37)
than for LFEC (0·11) among measurement times
(Table 8).
Crossbreeding parameters
Relatively few studies have estimated crossbreeding
parameters for sheep breeds in the tropics (e.g.
Boujenane et al., 1998; Boujenane and Kansari, 2002),
in contrast to those undertaken in temperate climates
(e.g. Clarke, 1982; Young et al., 1986). For the reasons
discussed above, the estimates of GI in this study for
PCV and LFEC (Table 5) are likely to underestimate
the true genetic differences. They are also only
relevant to the hot humid conditions under which
they are estimated, and in which the Dorper breed is
poorly adapted. This means that, relative to
estimates derived for environments more suited to
the Dorper, the observed breed differences will be
smaller for LWT and higher for mortality rate. The
small differences among genotypes for LWT possibly
 Genetics of resistance and resilience to internal parasites in tropical lambs
account for the lack of significant heterosis estimates
(HI or HM) for LWT. Small positive estimates have
been reported in many other studies (e.g. as reviewed
by Nitter, 1978).
In the present study none of the estimates of HI or
HM for PCV or FEC was significant. This is also in
contrast to the few published estimates of heterosis
for resistance or resilience to endoparasites. From
relatively small crossbreeding experiments involving
resistant Florida Native and susceptible Rambouillet
sheep Amarante et al. (1999a) reported significant
heterosis for susceptibility (assessed by both FEC
and worm burdens), while Amarante et al. (1999b)
reported significant heterosis for resistance (assessed
by FEC). A larger study compared resistance to
endoparasites (predominantly H. contortus) under
pasture challenge of F1 lambs and their Suffolk
(susceptible) and Gulf Coast Native (resistant)
parental breeds (Li et al., 2001). There was strong
evidence for heterosis in the direction of the resistant
breed for both FEC and PCV. The estimates of HI for
mortality rates were negative for post-weaning and
total mortality (i.e. F1 crossbred lambs had lower
mortality rates than the average of the two
purebreds), but these effects were not significant.
Genetic parameter estimates
The magnitude of, and the trends for, the heritability
estimates and the maternal effects for LWT are
consistent with the literature, both for tropical (Liga
et al., 2000; Rege et al., 2002) and temperate (Maria et
al., 1993; Tosh and Kemp, 1994) sheep. The large
maternal effect for LWT in lambs between birth and
weaning gradually declines post weaning.
Conversely, the additive heritability for LWT is
usually relatively low at weaning (about 0·10) and
then increases post weaning to a value of about 0·20
to 0·30 at about 12 months of age. Results from the
present study (Table 6) confirm the existence of a
significant maternal effect for LWT from birth to
weaning (range 0·26 to 0·40), several-fold greater
than the heritability estimates (range 0·02 to 0·08).
However, for 12-month-old lambs the heritability
estimate had increased to 0·24 (s.e. 0·09), while the
maternal effect had declined to 0·17 (s.e. 0·05). There
was no evidence at any age that the heritability
estimates for LWT were significantly different
between the two sire breeds. However, there were
different trends in the heritability estimates post
weaning, with the Red Maasai-sired lambs having
relatively low heritabilities compared with the
Dorper-sired lambs at 4·5 months of age (0·05 v. 0·18,
respectively) but almost identical heritabilities at 10
to 12 months of age (0·21 v. 0·20, respectively).
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131
Maternal effects for PCV and LFEC were not
significant at any measurement time, which is
consistent with the results reported by Woolaston
and Piper (1996) and Rege et al. (2002). There was a
consistent trend from 6 to 12 months of age for the
heritability estimate for LFEC to be higher in Dorper-
sired lambs than in Red Maasai-sired lambs. There
was a similar trend for PCV although in this case the
difference in heritabilities was not so large. While
this study was not originally designed to compare
heritability estimates between sire breeds, the
differences found in these analyses were large
enough (especially for LFEC) to warrant
investigating these heritabilities further in a repeated
measures analysis. This method provided heritability
estimates for the post-weaning measurements that
were significantly different from zero for both PCV
(based on two or more measurements) and LFEC
(based on three or more measurements) (Table 7), in
contrast to the estimates at each sampling time (Table
6), which were mostly not significantly different from
zero. When the four post-weaning measurements
from 6 to 12 months for LFEC were included in the
repeated measures analysis the heritability estimates
for the Dorper-sired lambs (0·15, s.e. 0·05 for the
animal model and 0·19, s.e. 0·07 for the sire model)
were significantly higher (P < 0·05) than the
estimates for Red Maasai-sired lambs (0·00 and 0·01,
s.e. 0·02).
Heritability estimates for PCV post weaning in the
present study (about 0·15, Table 7) are slightly lower
than the heritability estimate for PCV decline (0·23,
s.e. 0·03) during infection with H. contortus in Merino
lambs (Woolaston and Piper, 1996). The heritability
of various transformations of FEC (e.g. typically
logarithms, square root or cube root transformations)
following natural pasture challenge of lambs with GI
nematode parasites (usually from about 3 to 10
months of age) mostly range from 0·20 to 0·40 in
studies undertaken in New Zealand with Romney or
Romney-derived breeds (Morris et al., 1995), in
studies in Australia with Merino sheep (Woolaston
and Eady, 1995; Woolaston and Piper, 1996), in a
study with Scottish Blackface sheep (Bishop et al.,
1996) and in a study with Polish long-wool sheep
(Bouix et al., 1998). The post-weaning heritability
estimates for LFEC for the susceptible Dorper-sired
lambs (0·15 to 0·19, Table 7) are close to the published
estimates, but the heritability estimates for the
resistant Red Maasai-sired lambs are not significantly
different from zero at any time from 1 to 12 months
of age (Tables 6 and 7). A possible explanation for
this difference is that after many hundreds of years
of natural selection many of the genes for resistance
in the Red Maasai breed have become fixed.
Conversely, the Dorper breed was originally
 132 Baker, Nagda, Rodriguez-Zas, Southey, Audho, Aduda and Thorpe
established by crossing the Dorset Horn and the
Black Head Persian breeds and because the Dorset
Horn is known to be particularly susceptible to
endoparasites (Ross, 1970; Gamble and Zajac, 1992),
alleles for both resistance and susceptibility are likely
to be segregating in the Dorper. While the current
study may be criticized as being not large enough to
establish the difference in heritability estimates for
the two sire breeds (i.e. based on 35 Red Maasai sire
groups and 41 Dorper sire groups), it is pertinent to
note that other studies have used fewer sires – e.g. 22
sires in a study with Scottish Blackface lambs (Bishop
et al., 1986) and 32 sires in a Polish study (Bouix et al.,
1998), and still generated useful results. As far as we
are aware, there have not been published reports of
heritabilities of resistance or resilience to
endoparasites in other tropical breeds known to be
relatively resistant to H. contortus (e.g. the St Croix
and the Javanese Thin Tail). Such studies would be of
considerable interest as they would help substantiate
the hypothesis above that natural selection in
tropical environments may reduce within-breed
genetic variation for resistance to endoparasites. The
increase in the heritability of LFEC in Dorper-sired
lambs with age is consistent with the trend observed
in Scottish Blackface lambs naturally infected
predominantly with Ostertagia circumcincta (Bishop et
al., 1996), for which heritability increased from zero
in 1- and 2-month-old lambs to 0·22 (s.e. 0·13) in 6-
month-old lambs.
The heritability estimate for pre-weaning lamb
mortality in the present study was 0·00 (s.e. 0·09)
which is consistent with most of the literature (e.g.
Fogarty, 1995; Lopez-Villalobos and Garrick, 1999) in
which estimates for mortality rate from birth to
weaning range from zero to 0·01 and are commonly
not significantly different from zero. Rege et al. (2002)
reported heritability estimates for logit-transformed
pre-weaning mortality rate of zero, but 0·23 (s.e. 0·06)
for post-weaning mortality rate. Significant
heritability estimates for lamb mortality for five
periods between birth to one year of age (ranging
from 0·12 to 0·21) were reported by Southey et al.
(2001), but with no indication of significantly
different estimates for pre-weaning compared to
post-weaning mortality rates. Nguti et al. (2003)
analysed mortality in the present data set using
survival analysis. From a mixed model analysis with
a random term for sire, the sire variance component
estimate was similar to its standard error for pre-
weaning mortality but larger for post-weaning
mortality. When adjusted for lamb body weight the
sire variance component for post-weaning mortality
increased to three times its standard error. The
significant maternal effect for pre-weaning mortality
rate in the present paper is consistent with the
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significant estimates reported by Rege et al. (2002)
and Southey et al. (2001).
Most of the genetic correlation estimates in the
present study are characterized by high standard
errors and are therefore imprecisely estimated. The
non-significant genetic correlation estimates between
LWT and LFEC are consistent in size with most of
the published estimates for this genetic correlation in
lambs in Australasia (Morris et al., 2000). These
contrast with significant negative correlation
estimates (i.e. favourable) in Scottish Blackface lambs
between 3 and 6 months of age (Bishop et al., 1996)
and in Polish long-wool sheep between 2 and 7
months of age (Bouix et al., 1998). The European
studies were done with pasture challenge involving
different nematode taxa and in younger lambs than
the Australasian studies; both these factors may
influence the genetic correlation estimates between
LWT and LFEC. However, there is no indication of
an age trend for either the phenotypic or genetic
correlation estimates in this study (Table 9). When
sheep were infected with the blood-sucking parasite
H. contortus both the phenotypic and genetic
correlations between FEC and PCV were consistently
negative (Albers et al., 1987; Woolaston and Piper,
1996; Baker et al., 1999) as in this study.
Conclusion
The results of this study, in conjunction with the ewe
production and reproduction results reported earlier
(Baker et al., 1998 and 1999), have important
implications for smallholder farmers in coastal
Kenya and other humid/sub-humid regions of East
Africa. Not only are Red Maasai sheep more resistant
and resilient to endoparasites (particularly H.
contortus), but the combined effect of a higher
reproductive rate, lower lamb and ewe mortality and
similar yearling live weights results in about a three-
fold increase in offtake (flock productivity) of a
purebred Red Maasai v. a purebred Dorper flock
(Baker et al., 1999). This increases to about a five-fold
difference when total flock efficiency is estimated
(Baker et al., 2002). However, it is important to
acknowledge that, because of genotype by
environment interactions, it may not be valid to
extrapolate these results to other environmental
conditions. Baker et al. (2002) compared the results
from this study in coastal Kenya with another study
where Red Maasai and Dorper sheep were evaluated
in a semi-arid environment in Kenya. At both
locations the Red Maasai ewes and lambs were
consistently more resistant and resilient to
endoparasites (predominantly H. contortus).
However, there were important breed by
environment interactions for ewe reproduction,
mortality rates and live weights, because the Dorper
 Genetics of resistance and resilience to internal parasites in tropical lambs
sheep performed much better in a semi-arid
environment than in a humid environment. The net
result was that a Dorper flock had a higher
productivity (offtake in terms of weight of sheep
sold) than a Red Maasai flock in the semi-arid
environment, although when the higher food
requirements of the heavier Dorper sheep were
accounted for, there was no significant difference in
flock efficiency.
The heritabilities for PCV, LFEC and LWT estimated
in this study have important implications for within-
breed genetic improvement programmes. Any
genetic improvement programme for Red Maasai
sheep should concentrate on improvement of
resilience (e.g. select for higher PCV), while selection
for both improved resistance (FEC) and resilience
(PCV) would be advocated in a Dorper flock. While
selection for improved lamb growth rate is also
clearly feasible in both breeds, it may not necessarily
be recommended depending on the breeding
objective being pursued and the relative economic
values of each trait (Kosgey et al., 2001). For example,
if the Red Maasai is considered to be predominantly
a breed that is well adapted to tropical conditions,
then there may be little to be gained by breeding
bigger sheep, which have a higher food requirement
in an environment where both food availability and
quality are often limiting. Conversely, if the Dorper is
used mainly as a sire breed to produce crossbred
lambs which are all slaughtered, then selection for
growth rate may be warranted. If selection for
growth rate is deemed appropriate, then the
heritability estimates suggest that selection for
growth can start at a younger age in Dorper sheep (4
to 6 months of age) than in Red Maasai sheep (10 to
12 months of age).
Acknowledgements
We are extremely grateful to Dr R. Haller, Managing
Director, Baobab Farm for provision of land, animals
and facilities at Diani Estate for this research. Dr L.
Reynolds and Dr J. Miller assisted with the initiation
of this study and D. Mwamachi from the Kenyan
Agricultural Research Institute (KARI) was the
resident veterinarian in the early years of the study.
Dr R. Bain and the staff of the KARI helminthology
laboratory at Muguga provided valuable assistance
with training the technical staff at Diani Estate in egg
counting and larval identification. We also thank Dr
J. Rowlands and two anonymous referees for
critically reviewing earlier versions of this paper and
making constructive suggestions to improve it.
ILRI’s research within its Livestock Genetics and
Genomics programme was supported by The United
Kingdom, Japan and the European Union through
the Consultative Group on International Agricultural
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133
Research (CGIAR). This is ILRI publication no.
200213.
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