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

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.

Keywords: Chicken; Eimeria; Genetic diversity; Operational taxonomic units; Vaccine.

Graphical abstract

Fig. 1

Assembling a global panel of Eimeria field samples: countries sampled and parasite occurrence determined by species-specific PCR. Twenty-one countries were sampled for Eimeria spp. occurrence, including all six continents where domestic chickens can be found. The number of samples used for species detection by PCR in each country and the results per species are shown in Table 1. The line labelled 30°N indicates 30° latitude north. Species or operational taxonomic units (OTUs) found to be present in each country/region are shown in blue above the line in each circle, OTUs found to be absent are shown in black beneath the line. a, Eimeria acervulina; b, Eimeria brunetti; ma, Eimeria maxima; mi, Eimeria mitis; n, Eimeria necatrix; p, Eimeria praecox; t, Eimeria tenella; x, OTUx; y, OTUy; z, OTUz. ^∗Data produced in this study. Superscript numbers indicate data derived from the published literature ¹Schwarz et al. (2009); ²Cantacessi et al. (2008); ³Morgan et al. (2009).

Fig. 2

Eimeria spp. and operational taxonomic unit (OTU) internal transcribed spacer sequence (ITS) 1 and 2 diversity. (A) Tamura-Nei model Maximum Likelihood (ML) phylogeny of ITS1-5.8S-ITS2 sequences derived with 1000 bootstrap replication from samples collected in Asia, Africa, Europe and the Americas (GenBank accession numbers LN609768–LN609975). The number and origin of sequences used are shown in Table 1. Coloured spots indicate the country of origin for each sequence (Asia: China (blue), India (dark blue), Japan, (light blue). Europe: countries pooled (red). North Africa: Egypt (orange), Libya (dark red). Sub-Saharan Africa: Ghana (purple), Nigeria (pink), Tanzania (dark green), Uganda (green), Zambia (yellow). Americas: USA (black), Venezuela (grey)). L, long sequence form; S, short sequence form. Numbers shown in parentheses indicate the number of putative species partitioned per recognised species, sequence form or OTU by Bayesian species delimitation. (B) Mean genetic distance within each species and OTU genotype calculated using ML with 1000 bootstrap replications. Species and genotype identifiers are as follows: a, Eimeria acervulina; b, Eimeria brunetti; ma, Eimeria maxima; mi, Eimeria mitis; n, Eimeria necatrix; p, Eimeria praecox; t, Eimeria tenella; x, OTUx; y, OTUy; z, OTUz; L, long sequence form; S, short sequence form. The dotted line indicates the intersect between the combined and the separated long and short sequence forms.

Fig. 3

Internal transcribed spacer (ITS) 1-5.8S-ITS2 sequence principal co-ordinate analysis and Wrights Fixation Index (F_ST), illustrating variation for (A) Eimeria tenella in some regions, but not (B) Eimeria acervulina or (C) Eimeria mitis. N. Africa, North Africa; SS. Africa, sub-Saharan Africa. Pairwise and overall F_ST values are shown beside the equivalent plot.