Abstract

BackgroundPlasmodium falciparum shares its most recent common ancestor with parasites found in African apes; these species constitute the so-called Laverania clade. In this investigation, the evolutionary history of Plasmodium lineages found in chimpanzees (Pan troglodytes) was explored.MethodsHere, the remainders of 74 blood samples collected as part of the chimpanzees’ routine health examinations were studied. For all positive samples with parasite lineages belonging to the Laverania clade, the complete mitochondrial genome (mtDNA), the gene encoding dihydrofolate reductase-thymidylate synthase (dhfr-ts), the chloroquine resistance transporter (Pfcrt), the circumsporozoite protein (csp), merozoite surface protein 2 (msp2), and the DBL-1 domain from var2CSA were amplified, cloned, and sequenced. Other Plasmodium species were included in the mtDNA, dhfr-ts, and csp analyses. Phylogenetic and evolutionary genetic analyses were performed, including molecular clock analyses on the mtDNA.Results/ConclusionsNine chimpanzees were malaria positive (12.2%); four of those infections were identified as P. falciparum, two as a Plasmodium reichenowi-like parasite or Plasmodium sp., one as Plasmodium gaboni, and two as Plasmodium malariae. All P. falciparum isolates were resistant to chloroquine indicating that the chimpanzees acquired such infections from humans in recent times. Such findings, however, are not sufficient for implicating chimpanzees as an animal reservoir for P. falciparum.Timing estimates support that the Laverania clade has co-existed with hominids for a long-period of time. The proposed species P. gaboni, Plasmodium billbrayi, and Plasmodium billcollinsi are monophyletic groups supporting that they are indeed different species.An expanded CSP phylogeny is presented, including all the Laverania species and other malarial parasites. Contrasting with other Plasmodium, the Laverania csp exhibits great conservation at the central tandem repeat region. Msp2 and var2CSA, however, show extended recent polymorphism in P. falciparum that likely originated after the P. reichenowi-P. falciparum split. The accumulation of such diversity may indicate adaptation to the human host. These examples support the notion that comparative approaches among P. falciparum and its related species will be of great value in understanding the evolution of proteins that are important in parasite invasion of the human red blood cell, as well as those involved in malaria pathogenesis.

Highlights

  • Plasmodium falciparum shares its most recent common ancestor with parasites found in African apes; these species constitute the so-called Laverania clade

  • Evidence of host switches in modern times are found in the case of the macaque parasite Plasmodium knowlesi infecting humans in specific ecological settings [14,15] and the cases of Plasmodium vivax-Plasmodium simium and Plasmodium malariae-Plasmodium brasilianum that are shared between humans and several species of New World monkeys [12,16]

  • Species diversity and phylogenetic analyses Seventy-four chimpanzee (47 males and 27 females) blood samples were screened for Plasmodium parasites

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Summary

Introduction

Plasmodium falciparum shares its most recent common ancestor with parasites found in African apes; these species constitute the so-called Laverania clade. In this investigation, the evolutionary history of Plasmodium lineages found in chimpanzees (Pan troglodytes) was explored. Part of the challenge emerges from the fact that the four Plasmodium species commonly found infecting humans exhibit noticeable differences in their clinical manifestations, geographic distributions, and basic biological characteristics [3]. Such differences are explained, at least in part, by their independent origins as human parasites [4,5]. It is worth noting that, whereas P. knowlesi is a zoonosis transmitted from macaques [15], there is no data of malaria transmission from non-human primates to humans in the other cases [18]

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