Mode and Rate of Evolution of Haemosporidian Mitochondrial Genomes: Timing the Radiation of Avian Parasites

Abstract

Haemosporidians are a diverse group of vector-borne parasitic protozoa that includes the agents of human malaria; however, most of the described species are found in birds and reptiles. Although our understanding of these parasites’ diversity has expanded by analyses of their mitochondrial genes, there is limited information on these genes’ evolutionary rates. Here, 114 mitochondrial genomes (mtDNA) were studied from species belonging to four genera: Leucocytozoon, Haemoproteus, Hepatocystis, and Plasmodium. Contrary to previous assertions, the mtDNA is phylogenetically informative. The inferred phylogeny showed that, like the genus Plasmodium, the Leucocytozoon and Haemoproteus genera are not monophyletic groups. Although sensitive to the assumptions of the molecular dating method used, the estimated times indicate that the diversification of the avian haemosporidian subgenera/genera took place after the Cretaceous–Paleogene boundary following the radiation of modern birds. Furthermore, parasite clade differences in mtDNA substitution rates and strength of negative selection were detected. These differences may affect the biological interpretation of mtDNA gene lineages used as a proxy to species in ecological and parasitological investigations. Given that the mitochondria are critically important in the parasite life cycle stages that take place in the vector and that the transmission of parasites belonging to particular clades has been linked to specific insect families/subfamilies, this study suggests that differences in vectors have affected the mode of evolution of haemosporidian mtDNA genes. The observed patterns also suggest that the radiation of haemosporidian parasites may be the result of community-level evolutionary processes between their vertebrate and invertebrate hosts.

Diversification by host switching and dispersal shaped the diversity and distribution of avian malaria parasites in Amazonia

“…As expected, the topologies for both Plasmodium and Parahaemoproteus did not change (Supplementary material Appendix 4 and 5 for trees). However, when using the Pacheco et al (2018) rates, the first cladogenic events were older for both genera. Nevertheless, the diversification of most lineages within each parasite genus occurred in the late Miocene, with increasing frequency of lineage splitting in the Pliocene and Quaternary.…”

“…To obtain absolute ages for cladogenetic events through malaria trees, we used the mutation rate of 0.006 per lineage per million years estimated by Ricklefs and Outlaw (2010). Secondly, we conducted a second set of time tree analyses using a recently published substitution rate for avian malaria parasites estimated by Pacheco et al (2018) based on whole mitochondrial genome sequences, as a uniform prior ranging from 0.00334 to 0.00487 substitutions per lineage per million years. Convergence and performance of runs were inspected using Tracer 1.6 ( http://beast.bio.ed.ac.…”

“…The greatest conflict was with Silva et al (2015), who estimated an older time of origin and radiation of mammalian Plasmodium compared to Ricklefs and Outlaw (2010). To assess the effect of using different published clock rates, we ran an alternative BEAST dating scheme using the most recent molecular clock substitution rate published by Pacheco et al (2018) and compared that to our analysis using the substitution rate published by Ricklefs and Outlaw (2010). As expected, the topologies for both Plasmodium and Parahaemoproteus did not change (Supplementary material Appendix 4 and 5 for trees).…”

Avian host composition, local speciation and dispersal drive the regional assembly of avian malaria parasites in South American birds

“…We generated two independent runs for each alignment with parameters as follows: an uncorrelated lognormal relaxed clock, Yule process, 100 million generations of MCMC (Markov chain Monte Carlo), parameters sampled every 10,000 generations and 10% of generations discarded as burn‐in. To obtain absolute ages for cladogenetic events through parasite trees, we used a recently published substitution rate for avian malaria parasites estimated by Pacheco et al (), based on whole mitochondrial genome sequences, as a uniform prior ranging from 0.00334 to 0.00487 substitutions per lineage per million years. Convergence and performance of runs were inspected using tracer 1.6 (http://beast.bio.ed.ac.uk/Tracer), to ensure that ESS (effective sample size) values exceeded 200.…”

Genomic sequence capture of haemosporidian parasites: Methods and prospects for enhanced study of host–parasite evolution

“…Multihost, multiparasite systems provide extensive opportunities to advance research in ecology and evolution. Haemosporidians (malaria and relatives, Order Haemosporida), the intracellular, protozoan parasites that infect vertebrates, are one great example, with studies ranging in scope from regional and temporal patterns of community turnover (Fallon, Bermingham, & Ricklefs, 2005;Fallon, Ricklefs, Latta, & Bermingham, 2004;Fecchio et al, 2017; Olsson-Pons, Clark, Ishtiaq, & Clegg, 2015), to host-switching and diversification across long evolutionary timescales (Galen, Borner, et al, 2018;Martinsen, Perkins, & Schall, 2008;Pacheco et al, 2018;Ricklefs et al, 2014). Avian haemosporidians in particular (genera Plasmodium, [Para]Haemoproteus and Leucocytoozoon) have attracted a large research community seeking to describe global patterns of diversity, abundance and host range and uncover mechanisms underlying parasite diversification, hostswitching and host susceptibility (Bensch, Hellgren, & Pérez-Tris, 2009;Clark, Clegg, & Lima, 2014;Lutz et al, 2015;Scheuerlein & Ricklefs, 2004).…”