Prospects for breeding for resistance to endoparasites in small ruminants in Africa a new ILCA research programme

R. L Baker¹, L. Reynolds², A. Lahlou Kassi³, J.E.O. Rege³ Tekelye Bekelye³, E. Mukassa-Mugerwa³ and B. Rey⁴

¹ILCA, P. O. Box 46847, Nairobi, Kenya

²ILCA, P. O. Box 80147, Mombasa, Kenya

³ILCA, P. O. Box 5689, Addis Ababa, Ethiopia

⁴IEMVT, France, seconded to ILCA, P. O. Box 5689, Addis Ababa, Ethiopia

Abstract
Introduction
Genetic resistance
ILCA's research project
Some preliminary Kenyan results
References

Abstract

This paper briefly reviews the evidence for genetic resistance to endoparasites both between and within breeds of sheep and goats. There is extensive evidence for genetic variation in resistance among breeds of sheep outside Africa. Some evidence exists for breed variation in Africa. Almost all published reports to date suffer from poor experimental design, particularly in terms of the small numbers of each breed sampled and lack of information on how the animals were sampled. The evidence for genetic variations in resistance to endoparasites within breeds is more convincing. Heritabilities average about 0.35. In the light of this evidence, ILCA has developed a Pan-African multidisciplinary research programme to investigate and characterise genetic resistance to endoparasites in some indigenous African sheep and goat breeds. This includes the evaluation of: Menz and Horro sheep breeds in Ethiopia; Dorper and Red Maasai sheep and Galla and Small East African goats in coastal Kenya; Peul Peul (Fulani) and Djallonké sheep and West African Dwarf and Sahel goats in Senegal. The experimental design and research protocol for this research programme is outlined and some preliminary results of the research in the Kenyan coastal site are presented.

Perspectives de sélection sur la résistance aux endoparasites chez petits ruminants africains un nouveau programme de recherche du CIPEA

Résumé

Le présent article brosse un tableau rapide des facteurs qui démontrent l'existence d'une résistance génétique aux endoparasites inter- et intraspécifique chez les ovins et les caprins. La variabilité génétique de cette résistance entre races de moutons non africains est bien établie. Certains documents font état d'une variabilité interrace en Afrique. Toutefois, la quasi-totalité des rapports publiés à ce jour pèche par l'inadéquation du schéma expérimental, notamment pour ce qui est du petit nombre d'animaux échantillonnés dans chaque race et du manque d'information sur la manière dont les animaux ont été échantillonnés. Les preuves de l'existence de variations génétiques de la résistance aux endoparasites à l'intérieur d'une même race sont plus convaincantes. L'héritabilité est en moyenne de 0,35. A la lumière de ces observations, le CIPEA a engagé un programme panafricain de recherche pluridisciplinaire visant à étudier et à caractériser la résistance génétique aux endoparasites chez certaines races indigènes de moutons et de chèvres en Afrique. Parmi celles-ci figurent les moutons Menz et Horro d'Ethiopie; les moutons Dorper et Massaï et la chèvre Galla et la petite chèvre de l'Afrique de l'Est dans la région côtière du Kenya; les moutons peul peul et Djallonké et la chèvre naine d'Afrique occidentale ainsi que la chèvre du Sahel au Sénégal. Le dispositif expérimental et le protocole de recherche de ce programme sont exposés dans leurs grandes lignes et certains des premiers résultats des recherches effectuées dans la zone côtière du Kenya sont présentés.

Introduction

Gastrointestinal nematodes impose severe economic constraints on sheep and goat production in pastoral systems worldwide. Losses occur through mortalities, reduced production due to subclinical parasitism and direct costs associated with control (Barger, 1982; ILCA, 1992). Existing procedures to control endoparasites rely almost exclusively on curative or preventive treatment with anthelmintics. However, widespread and indiscriminate use of these potent drugs has resulted in the emergence of anthelmintic-resistant strains of nematodes (Waller, 1991). There are also increasing environmental concerns about chemical residues in meat and on pasture resulting from anthelmintic use.

In most countries in sub-Saharan Africa, endoparasite control options are limited. Access to anthelmintics by smallholder livestock producers is often restricted due to expense or unavailability. In addition, communal pastoral systems do not allow for regulated grazing as a means of lowering exposure to infective larvae on pasture. These considerations provide an impetus to develop alternative or complementary control options which eliminate or at least reduce the reliance on anthelmintics. Exploiting genetic variations in host resistance to endoparasites is an attractive option both to control endoparasites and improve the production efficiency of small ruminants.

Genetic resistance

Breed differences

There have been many reports since the mid-1930s of substantial variations among sheep breeds in resistance to internal parasites, particularly to Haemonchus contortus, Ostertagia circumcincta and Trichostongylus colubriformis. Gray (1991) tabulated and summarised 23 publications on this subject and this was expanded to 34 studies in a review by Baker et al (1992). For example, the East African Red Maasai (Preston and Allonby, 1978, 1979) and the Florida Native, St Croix, Barbados Blackbelly and Navajo (Courtney et al, 1984; Knight et al, 1973; Gamble and Zajac, 1992) are all relatively resistant to H. contortus in comparison with European breeds such as the Rambouillets or Merinos. There are also indications that some of the West African sheep and goat breeds, such as the Djallonké sheep and the West African Dwarf goat, may be relatively resistant to both internal parasites and trypanosomiasis (Osinowo and Abubakar, 1989; Smith, 1989).

Nearly all the studies reviewed by Gray (1991) and Baker et al, (1992) are characterised by very poor experimental design, due to both the numbers of animals of each breed tested, and lack of information on how the breeds were sampled. In addition, very few of the studies took account of variations among sires within breeds. The magnitude of the differences between sires can be the same as the largest differences between breeds (Gray et al, 1987). Many of the breed differences reported could reflect a single sire effect and hence should be interpreted cautiously.

While many of the publications on breed variation for resistance to disease can be criticised due to their poor experimental design, it is reassuring that some breeds have been identified as resistant in a number of independent studies. This applies particularly to the Florida Native, St Croix and Red Maasai sheep breeds. It is very likely these breeds have a real resistance to internal parasites. It is worthy of note that the St Croix sheep breed originated from West Africa and is probably related to the Djallonké sheep (Bradford and Fitzhugh, 1983).

Within-breed genetic variation

Baker et al (1992) tabulated and reviewed the substantial body of evidence reporting heritability estimates for resistance to internal parasites in sheep and goats. Resistance has commonly been assessed by either faecal egg counts (FEC) or haematocrit (packed cell volume-PCV). FEC has been shown to be a good indicator of actual worm burdens (especially in young animals) but can depend on the parasite species. PCV is a good indicator of worm burdens for blood-sucking parasites such as Haemonchus contortus.

From the 14 Australian and New Zealand studies that were reviewed by Baker et al (1992) the average heritability for a single FEC measurement following natural or artificial infection was 0.32. Heritabilities were similar for natural and artificial modes of infection and infection with a number of different parasite genera (both single genus infections and mixed infections). The average heritability of PCV (0.35) was similar to that for FEC. The advantage in taking more than one measurement of FEC depends on the repeatability estimate. The repeatability within a single artificial infection with Haemonchus contortus is high (0.60) and relatively little is to be gained in selection accuracy from more than one measurement (Woolaston et al, 1991). However, with natural challenge in New Zealand, the repeatability between two separate infections separated by an anthelmintic treatment is lower at about 0.30 to 0.40. This results in a heritability of 0.53 for the average of two FECs taken in lambs at about five and seven months old (Baker et al, 1991).

Estimates of genetic parameters (i.e. heritabilities and repeatabilities) of resistance to endoparasites in sheep and goats in Africa are limited. Those available were reviewed by Baker et al, (1992). Only three heritability estimates are available (Rohrer et al, 1991; Baker, 1992 (unpublished)). These range from 0.22 to 0.40, similar to those found in Australia and New Zealand. There are more repeatability estimates available. These are quite variable, ranging from 0.05 to 0.42. In some studies the low repeatability estimates for FEC have been shown to be affected by the egg counting procedure used. The improved modified McMaster egg counting technique (MAFF, 1977) is recommended and usually gives higher repeatability estimates. It is important that the egg counting technique is standardised in any experimental study on resistance to endoparasites and the procedure finally used is clearly documented in subsequent publications.

A number of divergent selection experiments in sheep for resistance or susceptibility to a number of different internal parasite genera are currently being carried out. In Australia there are five studies, in New Zealand three studies and in France one study. They were reviewed by Baker et al (1992). Successful response to selection has been reported in some of these studies (Baker et al, 1991; Cummins et al, 1991; Woolaston et al, 1991; Windon, 1991). This confirms the moderate to high heritabilities for resistance to endoparasites.

ILCA's research project

Objectives

The primary objective of the first phase of this research project is to identify and quantify genetic variations in resistance to internal parasites between and within some indigenous breeds of sheep and goats in Africa. Other important objectives include: determining the specificity of genetic variations in resistance to different parasite genera; undertaking parasite epidemiology studies; establishing the relations between FEC, PCV and actual worm burdens; and carrying out a comparative economic evaluation of the use of breeding and chemotherapy for parasite control (ILCA, 1991, 1992).

The second phase of this project will investigate immunological and genetic mechanisms of resistance to endoparasites. Breeds or groups of animals that are most resistant and most susceptible to endoparasites will be used. This may identify immunological or genetic markers of resistance. A desirable marker would be one that does not need infection and that would not be influenced by other environmental or physiological factors. Direct selection for resistance using parasitological measurements (e.g. FEC or PCV) requires artificial challenge or unchecked field infection with endoparasites. It is time-consuming, subject to sampling errors and may interfere with other traits under selection.

Experimental design

Phase 1 of the research was initiated in 1990 in coastal Kenya and in 1992 in Ethiopia and Senegal.

In Ethiopia, Menz and Horro sheep breeds are being evaluated at ILCA's Debre Berhan research site. Each year 340 ewes and 10 rams of each breed will be evaluated. Each breed will be split into two groups (150 ewes mated and 20 unmated) and mated to lamb in two distinct seasons of the year (i.e. wet and dry). In addition to the primary objective of assessing resistance to internal parasites, other studies using the same sheep will assess parasite epidemiology, undertake reproductive physiology studies, measure food intake and investigate fat metabolism and gut capacity.

In coastal Kenya (near Mombasa), during 1990 and 1991, approximately 200 Dorper and 200 Red Maasai x Dorper ewes were mated to 12 Dorper and 12 Red Maasai rams in a diallel crossbreeding design. In 1992 a group of about 100 Red Maasai ewes were added to the study, also being mated to both sire breeds. At the same site Galla goats have been monitored in 1990 and 1991. In 1992 a group of Small East African goats was added to the study to provide a breed comparison with the Galla goats. Beginning in 1993 the Galla and Small East African does (about 120 of each) will be mated to five bucks of each of the same breeds in a diallel crossbreeding design.

In Senegal both on-farm and on-station research components are planned. The on-farm study will monitor Peul Peul (Fulani) sheep and Sahel goats in the northern Sahelian arid zone and Djallonké sheep and West African Dwarf goats in the southern humid zone. This study was initiated in July 1992 and utilises the PPR (Pathology and Productivity of Small Ruminants) programme developed by ISRA (Institut Sénégalais de Recherche Agricole) and IEMVT (Institut d'Elevage et de Médécine Vétérinaire des Pays Tropicaux). The on-station component is being developed in collaboration with the ILCA Trypanotolerance Thrust. It is currently proposed that this will be initiated in 1993 at the ISRA Kolda research station in the southern humid zone of Senegal. Initially the Peul Peul and Djallonké sheep breeds will be evaluated, possibly in a diallel crossbreeding design.

Experimental protocol

The main experimental protocol that will be used to assess resistance to internal parasites at all research sites will involve measurements of faecal egg counts (FEC) and packed cell volume (PCV) in young lambs and kids from weaning (three months) to one year old. All animals will be given an anthelmintic treatment (drenched) at weaning. Then they will be left undrenched on pasture until a monitor group of about 50 lambs or kids (which are sampled weekly) reach a critical FEC which averages 1,500 epg (eggs per gram) in sheep and 1,000 egg in goats. At this stage all animals in the group will have faecal and blood samples taken and will then be drenched. The procedure will be repeated until the animals reach one year of age, about three or four samplings, depending on the environmental conditions. Ewes will be monitored at critical times throughout the reproductive cycle (e.g. mating, three months post-mating, just before parturition and 1,2 and 3 months post-parturition).

At all sites both faecal cultures and worm counts from slaughtered animals will be undertaken to estimate the numbers and relative frequency of different parasite genera. At each faecal sampling time a buffy coat test for trypanosomiasis will be undertaken and blood stored for subsequent antigen identification of infection (in the Kenyan and Senegal sites).

Some preliminary Kenyan results

Results from the first crop of lambs born in this study at Diani Estate (near Mombasa) in mid-1990 showed that Red Maasai crosses required fewer drenches than Dorper lambs and had a higher survival rate to one year of age (Reynolds et al, 1992). In this crop of lambs, animals were treated with an anthelmintic when their PCV level dropped below 21 %. This results in severely censored data which makes it difficult to assess resistance in terms of FEC and PCV. For all subsequent lamb crops at Diani the new protocol described earlier was used which ensures FEC and PCV is measured in all animals at each sampling time.

Differences among breed groups for lambs born in 1991 (yearlings) and in 1992 (6-month old lambs) of resistance and production traits are shown in Tables 1 and 2, respectively.

Only 18 Red Maasai ewes were mated in 1992 which resulted in a small number of Dorper x Red Maasai and straightbred Red Maasai lambs. Subsequent matings at Diani will ensure that about 100 Red Maasai ewes are mated. Despite the small number of straightbred Red Maasai lambs evaluated there is clear evidence that an increasing proportion of Red Maasai blood results in more resistance to endoparasites than Dorper lambs. This is shown by higher PCV, lower FEC and lower mortality. This trend was consistent in both lamb crops. The small differences in live weight in favour of heavier Dorper lambs were not significant.

There is also preliminary evidence from this data for within-breed genetic variation. Restricted maximum likelihood (REML) animal model analyses for lambs of all genotypes born in 1991 and 1992 were carried out. Heritability estimates ( ± SE) were 0.21 ± 0.13 for FEC at weaning, 0.18 ± 0.11 for FEC in five-month old lambs and 0.24 ± 0.16 for live weight in five-month old lambs.

Table 1. Least squares means for live weight, PCV, FEC and mortality for lamb breed genotypes born in 1991.

Lamb breed (Sire breed x dam breed)			Yearling lambs			Mortality (birth-1 yr) (%)
		No. lambs	Weight (kg)	PCV (%)	FEC (epg)
Dorper x Dorper (D)		56	21.7	27.3	1846	45
Dorper x (RM x D)		54	21.7	27.3	1419	37
Red Maasai (RM) x Dorper		68	21.7	29.7	1112	23
Red Maasai x (RM x D)		77	21.0	29.2	1191	23
Significance¹
	Sire breed (SB)		ns	***	*	***
	Dam breed (DB)		ns	ns	ns	as
	SB x DB		ns	ns	ns	ns

¹. ns = P>0.05; * = P<0.05; *** = P<0.001.

Table 2. Least squares means for live weight, PCV, FEC and mortality for lamb breed genotypes born in 1992.

Lamb breed	6-month old lambs	Weight (kg)	PCV (%)	FEC (epg)	Mortality
	No. lambs				(birth-6 mo) (%)
(Sire breed x dam breed)
Dorper x Dorper (D)	44	12.2	21.9	3817	40
Dorper x (RM x D)	57	11.5	23.5	2467	20
Dorper x Red Maasai (RM)	4	11.0	23.2	85	43
RM x Dorper	47	11.9	24.3	1688	25
RM x (RM x D)	62	11.5	24.5	1759	22
RM x RM	7	11.7	26.3	1333	13
Signifcance¹
Sire breed (SB)		ns	**	ns	*
Dam breed (DB)		ns	ns	ns	ns
SB x DB		ns	ns	*	ns

¹ ns = P>0.05; * = P<0.05; ** = P<0.01.

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