Dissecting the Genomic Architecture of Resistance to Eimeria maxima Parasitism in the Chicken.

Kay Boulton,Pete Kaiser,Andrew Archer,David A Hume,Valentina Riggio,Matthew J Nolan,Androniki Psifidi,Oswald Matika,Damer P Blake,Nat Bumstead,Zhiguang Wu,Stephen C Bishop,Fiona M Tomley,Kimberley Harman,Paul M Hocking,Adrian L Smith,Pat Hesketh

doi:10.3389/fgene.2018.00528

Abstract

Coccidiosis in poultry, caused by protozoan parasites of the genus Eimeria, is an intestinal disease with substantial economic impact. With the use of anticoccidial drugs under public and political pressure, and the comparatively higher cost of live-attenuated vaccines, an attractive complementary strategy for control is to breed chickens with increased resistance to Eimeria parasitism. Prior infection with Eimeria maxima leads to complete immunity against challenge with homologous strains, but only partial resistance to challenge with antigenically diverse heterologous strains. We investigate the genetic architecture of avian resistance to E. maxima primary infection and heterologous strain secondary challenge using White Leghorn populations of derived inbred lines, C.B12 and 15I, known to differ in susceptibility to the parasite. An intercross population was infected with E. maxima Houghton (H) strain, followed 3 weeks later by E. maxima Weybridge (W) strain challenge, while a backcross population received a single E. maxima W infection. The phenotypes measured were parasite replication (counting fecal oocyst output or qPCR for parasite numbers in intestinal tissue), intestinal lesion score (gross pathology, scale 0–4), and for the backcross only, serum interleukin-10 (IL-10) levels. Birds were genotyped using a high density genome-wide DNA array (600K, Affymetrix). Genome-wide association study located associations on chromosomes 1, 2, 3, and 5 following primary infection in the backcross population, and a suggestive association on chromosome 1 following heterologous E. maxima W challenge in the intercross population. This mapped several megabases away from the quantitative trait locus (QTL) linked to the backcross primary W strain infection, suggesting different underlying mechanisms for the primary- and heterologous secondary- responses. Underlying pathways for those genes located in the respective QTL for resistance to primary infection and protection against heterologous challenge were related mainly to immune response, with IL-10 signaling in the backcross primary infection being the most significant. Additionally, the identified markers associated with IL-10 levels exhibited significant additive genetic variance. We suggest this is a phenotype of interest to the outcome of challenge, being scalable in live birds and negating the requirement for single-bird cages, fecal oocyst counts, or slaughter for sampling (qPCR).

Highlights

Coccidiosis is an intestinal disease caused by intracellular protozoan parasites of the genus Eimeria (Shirley et al, 2005)
The present study extends previous work in inbred chicken lines to determine the genetic architecture of E. maxima resistance, i.e., lack of per host genome (PR), and protection against secondary challenge with a heterologous E. maxima strain
After primary infection the pure line C.B12 birds produced fewer E. maxima oocyst counts compared to the pure line 15I and F2 birds, with the highest oocyst output recorded in the pure line 15I group

Summary

Introduction

Coccidiosis is an intestinal disease caused by intracellular protozoan parasites of the genus Eimeria (Shirley et al, 2005). The control of coccidiosis is a challenge to the international poultry industry, with economic losses estimated at USD 3 billion annually (Dalloul and Lillehoj, 2006). Current control of coccidiosis relies on the prophylactic use of anticoccidial drugs, or vaccination with formulations of live wild-type or attenuated parasites (Crouch et al, 2003; McDonald and Shirley, 2009). Use of some anticoccidial drugs has been curtailed by legislation, while the limited production capacity and costs of live attenuated vaccines compromise their utility in broiler flocks (Hong et al, 2006). There is a need for complementary strategies to control coccidiosis in poultry. A promising approach would be to breed chickens for increased genetic resistance and increased vaccine response to Eimeria parasitism since there is evidence for relevant host genetic variation (Johnson et al, 1986; Bumstead and Millard, 1992)

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Results

Conclusion