Phylogenetics, patterns of genetic variation and population dynamics of Trypanosoma terrestris support both coevolution and ecological host-fitting as processes driving trypanosome evolution

BACKGROUND: A considerable amount of evidence has favored ecological host-fitting, rather than coevolution, as the main mechanism responsible for trypanosome divergence. Nevertheless, beyond the study of human pathogenic trypanosomes, the genetic basis of host specificity among trypanosomes isolated from forest-inhabiting hosts remains largely unknown. METHODS: To test possible scenarios on ecological host-fitting and coevolution, we combined a host capture recapture strategy with parasite genetic data and studied the genetic variation, population dynamics and phylogenetic relationships of Trypanosoma terrestris, a recently described trypanosome species isolated from lowland tapirs in the Brazilian Pantanal and Atlantic Forest biomes. RESULTS: We made inferences of T. terrestris population structure at three possible sources of genetic variation: geography, tapir hosts and ‘putative’ vectors. We found evidence of a bottleneck affecting the contemporary patterns of parasite genetic structure, resulting in little genetic diversity and no evidence of genetic structure among hosts or biomes. Despite this, a strongly divergent haplotype was recorded at a microgeographical scale in the landscape of Nhecolândia in the Pantanal. However, although tapirs are promoting the dispersion of the parasites through the landscape, neither geographical barriers nor tapir hosts were involved in the isolation of this haplotype. Taken together, these findings suggest that either host-switching promoted by putative vectors or declining tapir population densities are influencing the current parasite population dynamics and genetic structure. Similarly, phylogenetic analyses revealed that T. terrestris is strongly linked to the evolutionary history of its perissodactyl hosts, suggesting a coevolving scenario between Perissodactyla and their trypanosomes. Additionally, T. terrestris and T. grayi are closely related, further indicating that host-switching is a common feature promoting trypanosome evolution. CONCLUSIONS: This study provides two lines of evidence, both micro- and macroevolutionary, suggesting that both host-switching by ecological fitting and coevolution are two important and non-mutually-exclusive processes driving the evolution of trypanosomes. In line with other parasite systems, our results support that even in the face of host specialization and coevolution, host-switching may be common and is an important determinant of parasite diversification.