Theileria lestoquardi displays reduced genetic diversity relative to sympatric Theileria annulata in Oman

• This study identified, and confirmed the species specificity, of ten micro- and mini-satellites spread across the T. lestoquardi genome and used them for analysis of genetics of four T. lestoquardi populations in Oman.
• In addition, we examined two antigens genes in T. annulata (Tams1 and Ta9) and their orthologues in T. lestoquardi (Tlms1 and Tl9).
• We compared the above data with previously published data, for comparable panels of markers, for sympatric T. annulata.
• Despite a comparably high prevalence, T. lestoquardi has lower genetic diversity and multiplicity of infection (MOI) compared to sympatric T. annulata populations.
• Similar to microsatellites, sequence diversity of the antigen genes, Tams1 and Ta9 in T. annulata, was higher than the orthologous Tlms1 and Tl9 in T. lestoquardi.
• It is, therefore, likely that T. lestoquardi evolved from an ancestor of present day T. annulata.

The Apicomplexan parasites, Theileria lestoquardi and Theileria annulata, the causative agents of theileriosis in small and large ruminants, are widespread in Oman, in areas where cattle, sheep and goats co-graze. Genetic analysis can provide insight into the dynamics of the parasite and the evolutionary relationship between species. Here we identified ten genetic markers (micro- and mini-satellites) spread across the T. lestoquardi genome, and confirmed their species specificity. We then genotyped T. lestoquardi in different regions in Oman. The genetic structures of T. lestoquardi populations were then compared with previously published data, for comparable panels of markers, for sympatric T. annulata isolates. In addition, we examined two antigen genes in T. annulata (Tams1 and Ta9) and their orthologues in T. lestoquardi (Tlms1 and Tl9).The genetic diversity and multiplicity of infection (MOI) were lower in T. lestoquardi (He = 0.64–0.77) than T. annulata (He = 0.83–0.85) in all populations. Very limited genetic differentiation was found among T. lestoquardi and T. annulata populations. In contrast, limited but significant linkage disequilibrium was observed within regional populations of each species. We identified eight T. annulata isolates in small ruminants; the diversity and MOI were lower among ovine/caprine compared to bovine. Sequence diversity of the antigen genes, Tams1 and Ta9 in T. annulata (π = 0.0733 and π = 0.155 respectively), was 10-fold and 3-fold higher than the orthologous Tlms1 and Tl9 in T. lestoquardi (π = 0.006 and π = 0.055, respectively).Despite a comparably high prevalence, T. lestoquardi has lower genetic diversity compared to sympatric T. annulata populations. There was no evidence of differentiation among populations of either species. In comparison to T. lestoquardi, T. annulata has a larger effective population size. While genetic exchange and recombination occur in both parasite species, the extent of diversity, overall, is less for T. lestoquardi. It is, therefore, likely that T. lestoquardi evolved from an ancestor of present day T. annulata and that this occurred either once or on a limited number of occasions.

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