Host species and pathogenicity effects in the evolution of the mitochondrial genomes of Eimeria species (Apicomplexa; Coccidia; Eimeriidae)

Abstract

Background: Mitochondria are fundamental organelles responsible for cellular metabolism and energy production in eukaryotes via the oxidative phosphorylation pathway. Mitochondrial DNA is often used in population and species studies with the assumption of neutral evolution. However, evidence of positive selection in mitochondrial coding genes of various animal species has accumulated suggesting that amino acid changes in mtDNA might be adaptive. The functional and physiological implications of the inferred positively selected sites are usually unknown and are only evaluated based on available structural and functional models. Such studies are absent in unicellular organisms that show several crucial differences to the electron transport chain of animal mitochondria. In the present study, we explored Eimeria mitogenomes for positive selection. We also tested for association between mtDNA polymorphism and environmental variation (i.e. host species), parasite life cycle (i.e. sporulation period), and efficient host cell invasion (i.e. pathogenicity, prepatent period). Findings: We used site- and branch-site tests to estimate the extent of purifying and positive selection at each site and each lineage of several Eimeria parasite mitogenomes retrieved from GenBank. We founded sixteen codons in the three mtDNA-encoded proteins to be under positive selection compared to a strong purifying selection. Variation in the ratios of non-synonymous to synonymous changes of the studied parasites was associated with their different host species (F = 13.748; p < 0.001), whereas pathogenicity levels were associated with both synonymous and non-synonymous changes. This association was also confirmed by the multiple regression analysis. Conclusions: Our results suggest that host species and pathogenicity are important factors that might shape mitochondrial variation in Eimeria parasites. This supports the important role of mtDNA variations in the evolution and adaptation of these parasites.