Cryptic Eimeria genotypes are common across the southern but not northern hemisphere

Emily L Clark,Xun Suo,Saroj Kumar,Jonathan Rushton,Boniface Namangala,Kumarasamy Thangaraj,Fiona M Tomley,Claire M Mugasa,Damer P Blake,Arni S.R Srinivasa Rao,Simeon Ayoade,Sarah E Macdonald,Joseph A Awuni,Isa Danladi Jatau,Matthew J Nolan,A.O Adebambo,Rajat Garg,Ramón Álvarez Zapata,G Dhinakar Raj,Abdalgader Moftah,A K Tewari ,Kanika Kundu ,Idris Alao Lawal ,P S Banerjee ,Thenmozhi Venkatachalam ,Sudhakar Natarajan ,H D Chapman ,Kimberly Fornace ,Esron D Karimuribo ,Muthusamy Raman

doi:10.1016/j.ijpara.2016.05.006

Abstract

The phylum Apicomplexa includes parasites of medical, zoonotic and veterinary significance. Understanding the global distribution and genetic diversity of these protozoa is of fundamental importance for efficient, robust and long-lasting methods of control. Eimeria spp. cause intestinal coccidiosis in all major livestock animals and are the most important parasites of domestic chickens in terms of both economic impact and animal welfare. Despite having significant negative impacts on the efficiency of food production, many fundamental questions relating to the global distribution and genetic variation of Eimeria spp. remain largely unanswered. Here, we provide the broadest map yet of Eimeria occurrence for domestic chickens, confirming that all the known species (Eimeria acervulina, Eimeria brunetti, Eimeria maxima, Eimeria mitis, Eimeria necatrix, Eimeria praecox, Eimeria tenella) are present in all six continents where chickens are found (including 21 countries). Analysis of 248 internal transcribed spacer sequences derived from 17 countries provided evidence of possible allopatric diversity for species such as E. tenella (FST values ⩽0.34) but not E. acervulina and E. mitis, and highlighted a trend towards widespread genetic variance. We found that three genetic variants described previously only in Australia and southern Africa (operational taxonomic units x, y and z) have a wide distribution across the southern, but not the northern hemisphere. While the drivers for such a polarised distribution of these operational taxonomic unit genotypes remains unclear, the occurrence of genetically variant Eimeria may pose a risk to food security and animal welfare in Europe and North America should these parasites spread to the northern hemisphere.

Highlights

Apicomplexan protozoan parasites of the genus Eimeria are obligate intracellular pathogens of huge economic and veterinary importance
Regional surveys of Eimeria spp. in chickens have commonly identified the presence of multiple species of parasite but have often suggested that one or more species are absent from particular geographic regions (e.g. (Al-Natour et al, 2002; Haug et al, 2008; Hamidinejat et al, 2010; Gyorke et al, 2013))
Analysis of a large panel of Eimeria genomic DNAs extracted from faeces collected from chicken farms around the world has shown the occurrence of all seven recognised Eimeria spp. in every country and region tested

Summary

Introduction

Apicomplexan protozoan parasites of the genus Eimeria are obligate intracellular pathogens of huge economic and veterinary importance. Chicken is one of the most efficient sources of animal-derived protein (Smil, 2002), pathogens that compromise the efficiency of chicken production can pose a serious threat to global food supplies and human poverty (Perry et al, 2002; Godfray et al, 2010). Eimeria spp. that cause coccidiosis in domestic chickens (Gallus gallus domesticus) have a major impact on animal welfare and the economics of chicken farming (Shirley et al, 2005; Dalloul and Lillehoj, 2006). Through a combination of parasite ubiquity, fecundity and pathogenicity, coccidiosis is among the 10 most economically significant endemic livestock diseases in the UK and the developed world, and is one of the top 10 veterinary diseases detrimental to the poor in southern Asia (Perry et al, 2002; Bennett and Ijpelaar, 2005)

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