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mosquitoes to convey them from human to human, it is not in the interests of the parasite to harm its vector. That might adversely affect transmission of the parasite to new hosts. Consequently none of the species of human malaria causes any great harm to mosquitoes, or at least mosquito immune defence systems appear to be adequate to limit damage. However, the situation with regard to the human host is much more complicated. In an environment where transmission from host to host is possible all the year round, as in the tropics, the type of parasite which will achieve the greatest evolutionary fitness is the one which achieves the highest rate of reproduction in the host, irrespective of what that does to the host.

P. falciparum achieves a very high rate of reproduction in a number of ways, for example by having the ability to invade erythrocytes of all ages, whereas P. vivax only invades reticulocytes (immature erythrocytes) with the Duffy antigen. P. falciparum may infect up to 80% of all erythrocytes, whereas P. vivax does not infect more than about 2%, and P. malariae more than about 1% of all red blood cells.

In cold environments, on the other hand, where transmission by mosquito is not possible all the year round, the parasite requires the host to survive during the winter in order to have an opportunity for transmission to new hosts the following year. These ecological considerations explain why extreme virulence is adaptive for P.

falciparum in its home in tropical Africa, while avirulence is adaptive for P. vivax and P. malariae in colder environments. Consequently the extreme virulence of P. falciparum does not constitute evidence for a recent evolutionary origin.²

The exponential expansion of DNA sequencing in recent years has yielded the important result that the human parasite P. falciparum forms a monophyletic clade with P. reichenowi, a malaria species which infects chimpanzees in Africa. This clade is not closely related to any of the other three species of human malaria.

Analysis of DNA sequences from ribosomal RNA genes (see Fig. 1) and from the circumsporozoite protein gene suggests that the ² e.g. Fiennes (1978: 105–12) regarded P. falciparum as a recent pathogen of man because of its virulence, but Garnham (1966: 279) was sceptical of such theories. Ewald (1994: 42–6), Anderson and May (1991: 648–52, cf. 392–419), and Coluzzi (1999) give various views on the significance of its virulence; Mackinnon and Read (1999 a) and (1999 b). Marchiafava and Bignami (1894: 103) observed that ‘malignancy coincides with an exceptionally abundant quantity of parasitic forms, a quantity much more abundant—where the cases terminate fatally—in the blood of the viscera than in the blood of the finger’.

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Evolution of malaria

common ancestor of the P. falciparum/P. reichenowi clade diverged from the common ancestor of the P. vivax/P. malariae clade about 165 million years ago. Anopheles mosquitoes, which transmit human malaria, do not appear in the fossil record until the Oligo-cene period (26–38 million years ago), but studies of molecular evolution suggest that the Anopheles family is very ancient. The protein and DNA sequences of the 35kb circular DNA molecule and the enolase gene of P. falciparum manifest very ancient kinship, or at least very extensive horizontal transfers of DNA, embracing not only organellar but also nuclear DNA, with a plant-related lineage.³ It remains controversial whether the various species of malaria were originally parasites of vertebrates or parasites of mosquitoes. It is possible that they were originally parasites of vertebrates because of the similarity of their developmental cycles to those of coccidian intestinal parasites of the suborder Eimeriina.⁴

However, the most interesting result of this research in molecular biology for current purposes is that statistical analysis of the degree of divergence between the DNA sequences of the human parasite P. falciparum and the chimpanzee parasite P. reichenowi puts their date of divergence in the time range of 5–11 million years ago.

Given the inevitable margin of error in these statistical calculations, this date approximates the date of divergence between humans and chimpanzees given by palaeoanthropologists. Consequently it is likely that P. falciparum has been attacking humans and their hominid ancestors since the dawn of human evolution, the split from the chimpanzee lineage.⁵ Similarly recent research suggests ³ Escalante et al. (1995) and Qari et al. (1996) on the molecular evolution of Plasmodium from rRNA gene sequences, cf. Escalante et al. (1998 a) for data from the cytochrome b gene and Rathore et al. (2001) for data from plastid sequences; Capasso (1991), Besansky et al. (1992), and Coluzzi (1999) on mosquito evolution; Hyde et al. (1994), Read et al. (1994) (nuclear DNA), and Köhler et al. (1997) (plastid DNA) on the links of P. falciparum to plant-related lineages; Felger et al. (1997) illustrate the sort of genetic variation which is now being discovered.

⁴ Missiroli (1934: 10–11) was one prominent Italian malariologist who advocated the theory of the close evolutionary relationship of malaria parasites to coccidian intestinal parasites. Capasso (1985: 301) supported the alternative theory that malaria parasites were originally parasites of the salivary glands of mosquitoes. This theory leaves unresolved the transmission question, namely how did the parasites get from mosquito to mosquito, since mosquitoes don’t bite each other. Going back even further in time, Halevy (1998) suggested that plasmodial parasites owe their similarities to plant genomes to descent from toxic algae which infected fish.

⁵ Rich et al. (1998 a) and Ayala and Rich (2000) found a very low rate of synonymous sub-stitutions in housekeeping genes of P. falciparum. They drew the inference from the apparent lack of genetic variation in housekeeping genes of modern strains that all currently existing P. falciparum populations are derived from a single ancestor that lived a

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