Why Plasmodium vivax and Plasmodium falciparum are so different? A tale of two clades and their species diversities

Abstract

The global malaria burden sometimes obscures that the genus Plasmodium comprises diverse clades with lineages that independently gave origin to the extant human parasites. Indeed, the differences between the human malaria parasites were highlighted in the classical taxonomy by dividing them into two subgenera, the subgenus Plasmodium, which included all the human parasites but Plasmodium falciparum that was placed in its separate subgenus, Laverania. Here, the evolution of Plasmodium in primates will be discussed in terms of their species diversity and some of their distinct phenotypes, putative molecular adaptations, and host-parasite biocenosis. Thus, in addition to a current phylogeny using genome-level data, some specific molecular features will be discussed as examples of how these parasites have diverged. The two subgenera of malaria parasites found in primates, Plasmodium and Laverania, reflect extant monophyletic groups that originated in Africa. However, the subgenus Plasmodium involves species in Southeast Asia that were likely the result of adaptive radiation. Such events led to the Plasmodium vivax lineage. Although the Laverania species, including P. falciparum, has been considered to share "avian characteristics," molecular traits that were likely in the common ancestor of primate and avian parasites are sometimes kept in the Plasmodium subgenus while being lost in Laverania. Assessing how molecular traits in the primate malaria clades originated is a fundamental science problem that will likely provide new targets for interventions. However, given that the genus Plasmodium is paraphyletic (some descendant groups are in other genera), understanding the evolution of malaria parasites will benefit from studying "non-Plasmodium" Haemosporida.

Keywords: Chitinases; Laverania; Malaria; Merozoite surface protein; Molecular clock; PfRH5-PfCyRPA-PfRipr complex; Phylogenomics; Plasmodium phylogeny.

Fig. 1

Phylogenetic tree of Plasmodium spp. based on complete mitochondrial genomes. Bayesian and Maximum Likelihood methods yielded identical topologies; only the Bayesian tree obtained using MrBayes v3.1.2 is shown. The alignment included approximately 5800 bp of the parasites’ mitochondrial genomes (mtDNA). The values above branches are posterior probabilities. The phylogeny branches leading to human malaria parasites are colored in red

Fig. 2

Phylogenomic analyses of the primate malarias using the available genomes. Consensus phylogeny on 1028 single-copy orthologous genes under the multi-species coalescent model implemented in ASTRAL III. Plasmodium gallinaceum and Plasmodium relictum were used as an outgroup to estimate the root of the primate malarias

Fig. 3

Evolution of the genes encoding the proteins in the RCR complex. Bayesian phylogenies for the proteins in the RCR complex were obtained using MrBayes v3.1.2. The two clades compared to assess differences in the strength of natural selection are indicated with different colors. In blue was the tested group corresponding with those closely related to P. vivax; the Laverania used as references are highlighted in green

Fig. 4

Evolution of the gene encoding the merozoite surface protein 2. A synteny map of the msp2 region is depicted. A msp2 ortholog is found in the avian parasites’ genomes. A Bayesian phylogeny obtained using MrBayes v3.1.2 on orthologous genes is provided. The branches with the two allelic forms in P. falciparum are colored in red

Fig. 5

Evolution of the genes encoding the merozoite surface protein 1 and its paralog. A synteny map of the msp1 region is depicted. Notice that an ortholog of the msp1 paralog originally described in P. vivax is found in the genomes of avian parasites. A Bayesian phylogeny on orthologous genes obtained using MrBayes v3.1.2 is provided. The branches with the two msp1 allelic forms in P. falciparum are colored in red. All the lineages leading to extant human malarias are indicated in red