Comparative Gene Evolution in Haemosporidian (Apicomplexa) Parasites of Birds and Mammals

Haemosporidian parasites of birds and mammals reproduce asexually inside nucleated and nonnucleated host erythrocytes, respectively. Because of these different parasite environments and because bird parasites are paraphyletic, we evaluated whether patterns of parasite molecular evolution differ between host groups. We compared two mitochondrial (mt) genes and one apicoplast gene across mammal Plasmodium, bird Plasmodium, and bird Parahaemoproteus. Using a molecular phylogenetic approach, we show that the parasite mt cytochrome b (cyt b), mt cytochrome oxidase I (COI), and the apicoplast caseinolytic protease C (ClpC) exhibit similar levels of sequence divergence, yet each gene tree presents a strikingly different pattern of internal versus terminal branch lengths. In cyt b, the ratio of nonsynonymous (NS)-to-synonymous substitutions (d(N)/d(S)) is markedly elevated along the internal branch linking mammalian and avian parasites despite the sister relationship between mammal and bird Plasmodium. This is not the case for either COI or ClpC. When NS substitutions are excluded from the parasite cyt b alignment, the resulting phylogenetic tree resembles that of COI (both with and without NS substitutions). The high d(N)/d(S) ratio in the cyt b branch separating avian and mammalian parasites and a mammal-parasite codon bias suggest that adaptive evolution has distinguished mammal and bird parasites.