Bayesian analysis of new and old malaria parasite DNA sequence data demonstrates the need for more phylogenetic signal to clarify the descent of Plasmodium falciparum

Abstract

Molecular systematic studies published during the last 15 years to clarify the phylogenetic relationships among the malaria parasites have led to two major hypotheses on the descent of Plasmodium falciparum: One supports an avian origin as a result of a relatively recent host switch, and another one favours the evolutionary development of P. falciparum together with its human host from primate ancestors. In this paper, we present phylogenetic analyses of three different Plasmodium genes, the nuclear 18 small sub-unit (SSU) ribosomal ribonucleic acid (rRNA), the mitochondrial cytochrome b (cyt b) and the plastid caseinolytic protease C (ClpC) gene, using numerous haemosporidian parasite DNA sequences obtained from the GenBank as well as several new sequences for major malaria parasites including the avian one Plasmodium cathemerium, which has never been considered in molecular phylogenetic analyses before. Most modern and sophisticated DNA substitution models based on Bayesian inference analysis were applied to estimate the cyt b and ClpC phylogenetic trees, whereas the 18 SSU rRNA gene was examined with regards to its secondary structure using PHASE software. Our results indicate that the data presently available are generally neither sufficient in number nor in information to solve the problem of the phylogenetic origin of P. falciparum.

The origin of malignant malaria

“…These authors showed that P. falciparum and P. reichenowi form an independent clade distinct from other malaria parasites, including the other three human malaria parasites, which appear to have originated in Old World monkeys (4,5). The close phylogenetic relationship between P. falciparum and P. reichenowi, their distinctness from the other human malaria parasites, and their remoteness from bird or lizard parasites was soon confirmed by other studies (6)(7)(8).…”

“…is thought to be best for recovering the deeper divergences within the genus (7,8), well illustrates the results from all three gene fragments (for the clpC and 18S rRNA phylogenies, see Fig. S1 and Fig.…”

“…If hypotheses ii or iii are correct, the level of neutral polymorphism should be greater in the ancestral parasite than in the derived species. In the absence of the molecular characterization of multiple strains of P. reichenowi, of which only one strain was available, Escalante and Ayala (4) and Escalante et al (5) favored the co-speciation hypothesis, as soon did other investigators (6)(7)(8). The two alternative transfer hypotheses were largely ignored because of the availability of only one known isolate of P. reichenowi (from Cameroon, described in 1917 and 1920, ref.…”

African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus

“…It was shown in 1994/1995 that the closest relative of Plasmodium falciparum, the agent of malignant malaria was Plasmodium reichenowi, a chimpanzee parasite, the only ape malaria parasite that had been molecularly characterized (1)(2)(3)(4). The close phylogenetic relationship between P. falciparum and Plasmodium reichenowi, their distinctness from the three other known human malaria parasites (Plasmodium vivax, Plasmodium ovale, and Plasmodium malariae), as well as from other primate parasites, and their remoteness from bird or lizard parasites, was soon confirmed by other studies (5)(6)(7). It was assumed, as a working hypothesis, that P. falciparum and P. reichenowi had evolved from a common ancestor parasite, independently in their respective hosts, humans and chimpanzees, as these two lineages gradually diverged from one another over the last 5-7 million years-the cospeciation hypothesis.…”

Malaria's Many Mates: Past, Present, and Future of the Systematics of the Order Haemosporida

“…However, though it is very tempting to plow ahead and continue to do more and more phylogenetic analyses, all of the studies that have been performed to date havehad a very incomplete sampling of the taxa of the order and very little genetic information, which have no doubt biased our perceptions regarding the history of this group (Hagner et al, 2007). Although there are profound challenges to obtaining the specimens in the first place and then to generate the sequence data, including genomic information, only via these intense efforts will we come even close to a complete picture of the relationships and the history of the group.…”