The polyphyly of Plasmodium : comprehensive phylogenetic analyses of the malaria parasites (order Haemosporida) reveal widespread taxonomic conflict

Abstract

The evolutionary relationships among the apicomplexan blood pathogens known as the malaria parasites (order Haemosporida), some of which infect nearly 200 million humans each year, has remained a vexing phylogenetic problem due to limitations in taxon sampling, character sampling and the extreme nucleotide base composition biases that are characteristic of this clade. Previous phylogenetic work on the malaria parasites has often lacked sufficient representation of the broad taxonomic diversity within the Haemosporida or the multi-locus sequence data needed to resolve deep evolutionary relationships, rendering our understanding of haemosporidian life-history evolution and the origin of the human malaria parasites incomplete. Here we present the most comprehensive phylogenetic analysis of the malaria parasites conducted to date, using samples from a broad diversity of vertebrate hosts that includes numerous enigmatic and poorly known haemosporidian lineages in addition to genome-wide multi-locus sequence data. We find that if base composition differences were corrected for during phylogenetic analysis, we recovered a well-supported topology indicating that the evolutionary history of the malaria parasites was characterized by a complex series of transitions in life-history strategies and host usage. Notably we find that Plasmodium, the malaria parasite genus that includes the species of human medical concern, is polyphyletic with the life-history traits characteristic of this genus having evolved in a dynamic manner across the phylogeny. We find support for multiple instances of gain and loss of asexual proliferation in host blood cells and production of haemozoin pigment, two traits that have been used for taxonomic classification as well as considered to be important factors for parasite virulence and used as drug targets. Lastly, our analysis illustrates the need for a widespread reassessment of malaria parasite taxonomy.

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

“…Avian malaria parasites (Order Haemospirida) of the genus Plasmodium and the two related genera Parahaemoproteus and Haemoproteus are vector-transmitted protozoan parasites that infect avian blood cells (Martinsen, Perkins, & Schall, 2008;Borner et al, 2016;Galen et al, 2018). These haemosporidian parasites are globally distributed and diverse in most bird families (Valkiūnas, 2005;Clark, Clegg, & Lima, 2014).…”

Neotropical migratory and resident birds occurring in sympatry during winter have distinct haemosporidian parasite assemblages

“…The genus Plasmodium comprises the causative agents of malaria, which are parasites that replicate clonally within red blood cells in the vertebrate host and are transmitted by Culicidae mosquitos (Valkiūnas et al, ). The subgenera Haemoproteus and Parahaemoproteus have been traditionally grouped within the genus Haemoproteus , though comprehensive phylogenetic analyses of haemosporidian relationships have retrieved Haemoproteus + Parahaemoproteus as a paraphyletic group (Borner et al, ; Galen et al, ; Martinsen, Perkins, & Schall, ). The subgenus Haemoproteus is restricted to a few groups of non‐passerine hosts and parasites are transmitted by hippoboscid flies (Hippoboscidae).…”

Genomic and transcriptomic evidence for descent from Plasmodium and loss of blood schizogony in Hepatocystis parasites from naturally infected red colobus monkeys

“…Species of the genus Hepatocystis are single-celled eukaryotic parasites infecting Old World monkeys, fruit bats and squirrels (1). Phylogenetically, they are thought to reside within a clade containing Plasmodium species, including the parasites causing malaria in humans (2). They were originally considered distinct from Plasmodium and have remained in a different genus because they lack the defining feature of asexual development in the blood, known as erythrocytic schizogony (3).…”