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Paleogenesis and Paleo-Epidemiology of Primate Malaria*

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Paleogenesis and Paleo-Epidemiology of Primate Malaria* Bull. Org. mond. Sante ) Bull. Wid Hith Org. 1965, 32, 363-387 Paleogenesis and Paleo-Epidemiology of Primate Malaria* L. J. BRUCE-CHWATI, M.D.1 The Haemosporidia, which comprise the malaria parasites, have probably evolved from Coccidia of the intestinal epithelium of the vertebrate host by adaptation first to some tissues of the internal organs and then to life in the circulating cells ofthe blood. The present opinion is that, among the malaria parasites ofprimates, the genus Hepato- cystis and the " quartan group " ofplasmodia are the most ancestral,followedby the " tertian group "; from the evolutionary viewpoint the subgenus Laverania isprobably the most recent. Studies recently completedandresearch in handon malariaparasites ofapesandmonkeys, combined with the possibility ofassessing the infectivity ofnew simianparasites to Anopheles and to man, will be ofgreat importancefora better understanding oftheprobable evolution of primate malarias. Thefact that several genera ofthe Anthropoidea evolved in an ecological area where the association with the existing insect vectors of various plasmodia was close is suggestive ofAfrica as the original home ofprimate malaria. It is probable that the disease spread up the Nile valley to the Mediterranean shores and Mesopotamia, to the Indian peninsula and to China. From these main centres malaria invaded a large part ofthe globe. It is also probable (though not proved) that malaria existed in the Americas before the Spanish conquest, and there is some likelihood that sea-going peoples brought it to the New World long before Columbus's voyages. Modern immunological methods applied to the study of the mummified remains of ancient inhabitants of America may help to solve this question. "Des especes, des races se sont 6teintes, d'autres ont evolue. Et, si nous ne pouvons faire la preuve de 1'existence de maladies anciennes, aujourd'hui disparues, du moins restons-nous reveurs devant la conti- nuite de certaines affections dont le temps, les milieux, le passage sur les etres les plus divers n'ont pu modifier les caracteres. Des millions d'an- n&es s'eoulent, des etres disparaissent, d'autres surgissent; mais, tou- jours, la maladie est 1a pour les marquer de ses stigmates. "1 Dans la vie de notre planete, elle a jou6 certainement un r6le considerable, aussi bien dans l'apparition des moyens de defense que dans l'evolution des etres." PALES (1930) The study of origins of disease is once again at- precise biochemical and immunological methods that tracting some attention. Among the many reasons offer much promise for future research. for the awakening interest in the prehistory of malaria, three may have the greatest weight: recent discoveries about the evolution of man, the explo- PALEOGENESIS OF " MALARIA PARASITES sion of new knowledge about malaria of our simian Much has been written about the evolutionary ancestors, and the development of marvellously approach to the study of infections caused by pro- tozoa commonly and loosely referred to as " malaria parasites ", as defined by Garnham (1963b). * Revised version of a paper presented at the First Inter- From the national Congress of Parasitology, Rome, September 1964. early period of work on Haemospori- 1 Chief, Research and Technical Intelligence, World dia, some parasitologists, and Mecnikov (1887) Health Organization, Geneva, Switzerland. among the first, were struck by the similarity of their 1575 363 364 L. J. BRUCE-CHWATT cycle of development to that of certain intestinal cells of the capillaries of this organ (e.g., Haemo- parasites of the order Coccidiida.1 Pfeiffer (1892), proteus) or in the liver cells themselves (Hepatocystis, Mesnil (1899), Schaudinn (1899) and Reichenow Plasmodium). (1912) are quoted in this respect by Wenyon (1926), Manwell's hypothesis (1955) that the plasmodia by Missiroli (1934) and by Manwell (1955), who state developed from Coccidia via haemogregarines has that Haemosporidia evolved from Coccidia which been vigorously developed by Bray (1957, 1963b), had adapted themselves to life in the blood and in who maintains that in the subclass Coccidiomorpha the process of this adaptation acquired a second the orders Coccidiida, Adeleida and Haemospori- host. In both types of parasite, the infection of the diida should be given equal taxononomic status, the vertebrate starts with the entry of the sporozoite last of the three orders having derived from the first into the cell; the subsequent schizont produces via the second. merozoites and these again become schizonts pro- The fundamental consideration is that of phylo- ducing more merozoites. During the sexual develop- geny, since Bray (1957) postulates that the ancestors ment, the fusion of male and female gametes results of the Plasmodidae were haemogregarine-like para- in the formation of an oocyst and division into sites, whose first appearance in the blood-stream sporozoites which recommence the asexual cycle. would facilitate transmission by blood-sucking Although the differences between the Coccidia arthropods. and Haemosporidia are many and considerable,2 Tracing lines of development in the Haemospori- it is generally agreed that their common evolutionary dia, Bray (1957) believes that the older line typified history started with an ancestral, free-living proto- by Haemoproteus gave rise to the malaria parasites zoon which invaded the intestinal tract and main- of amphibia, reptiles and birds while the more tained a simple life-cycle without an alternation of recent line typified by Hepatocystis represents the generations by multiplying within the same host evolutionary stem of malaria parasites of mam- and forming cysts discharged with the faeces. The mals. This is in agreement with the trend of evolu- next evolutionary steps comprised (as in Eimeria tionary change in the parasites since the original and Isospora) an invasion of the epithelial cells of separation of birds and reptiles from the main the gut, with a life-cycle consisting of several asexual evolutionary stem. Reptilian and avian species of generations followed by a sexual generation and malaria parasites are more numerous, have a wider formation of an oocyst which is discharged and geographical distribution and are better adapted to serves to infect a new host when swallowed. their hosts (Cameron, 1950) if one admits low patho- In the Lankesterellidae of amphibia and reptiles, genicity as a criterion of adaptation. there is a gradual adaptation of an intestinal coc- In the light of the present knowledge the most cidium to the blood habitat (Adler, 1933); the primitive known parasite of the avian and saurian schizogony and sporogony take place either in the line is Plasmodium (Haemamoeba) mexicanum. In the dnlestinal wall or in the endothelial cells of the blood case of mammals the most primitive is the " quartan vessels, but the sporozoites penetrate the free cells group " of parasites, followed by the " benign tertian of the blood and can be transmitted by a blood- group " and by Plasmodium knowlesi with its Hepato- sucking non-winged arthropod or by a leech. A cystis-like dependence on the liver; the subgenus parallel or previous evolutionary step can be traced in Laverania (P. falciparum and P. reichenowi), the least the invasion ofthe liver, through the portal system, to dependent on the development in the liver, is pro- establislh the developmental cycle in the bile duct bably the most recent. For malaria parasites of epithelium (e.g., Eimeria stiedae) or in the endothelial man this hierarchy was suggested by Knowles & Senior-White (1930). l "Judging by what has been learnt about the micro- Too little is known about malaria parasites of organisms of malaria one should regard them as belonging other animals to attempt any explanation of their to a group of Coccidia, some representatives of which live within the cells of various animals ... The micro-organisms evolutionary relationship. One step in the evolu- of malaria differ from Coccidia since the former have no tionary history of Haemosporidia was of para- envelope or capsule which protects their ameboid body mount importance-namely, the time when the during the developmental stages " (Mecnikov, 1887; trans.) as ' In the first the fertilization process and encystment of blood-adapted parasites acquired the insect their the zygote takes place in the vertebrate host, while in the invertebrate host. second this takes place in the blood-sucking invertebrate, No better example of a " deployment " in Huxley's which shelters the oocyst in its body until it produces spor- ozoites. (1953) sense could be found: an original single group PALEOGENESIS AND PALEO-EPIDEMIOLOGY OF PRIMATE MALARIA 365 became more numerous and more diversified and in The fact that, as far as we know, malaria parasites doing so spread over the environment using the of primates develop only in anopheline mosquitos evolutionary opportunities available and enabling it leads to the assumption of a long evolutionary as- to exploit the new environment more extensively. sociation and suggests that from an early stage Study of the paleogenesis of malaria may be the anophelines adapted themselves to feeding on best example of Fischer's reference to natural mammals and culicines on birds (Mattingly, 1960, selection as a " mechanism for generating a high 1965). Naturally, the insect-vertebrate life-cycle of degree of improbability ", and the longer the selec- the malaria parasite could not have evolved before tion acts, the more improbable the results. the mosquitos developed their blood-sucking habits. It is admitted that the close dependence of a group If the original home ofmalaria was in the Ethiopian of parasites on a group of hosts indicates a degree of region it is certain that the Anopheles existed there phylogenetic specificity which testifies to a long well before the first hominids and the same is also evolutionary relationship. Our existing insect fauna true for the temperate climates where the penetration is only a small fragment of the aggregation of insects of man was preceded by that of the insect vector that occupied the earth during the past 250 million (Ross, 1964).
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