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autumn, as seen, for example, in the population of Florence at the time of the Catasto (census) of  1427 (see Ch. 5. 2 below).³⁷ However, the association with the harvest is very significant. Peasants often slept out in the fields during the harvest, where they were very vulnerable to mosquito bites but far from stagnant sources of water in urban areas, the commonest source of enteric diseases. A very important practical reason for farmers in Lazio to stay in their fields at night was to prevent their crops being stolen. The vulnerability of farm workers to malaria infection during the harvest has frequently been noted in Italy and other Mediterranean countries, and indeed all over the world, wherever malaria occurs. In the village of Lodé in northeastern Sardinia, where in the 1930s the morbidity rate from malaria was 90%, 50% of the population slept outside the village during the summer.³⁸

Besides this Homeric text, there is another, completely different, but much stronger line of argument for the presence of P. falciparum malaria in Greece by the eighth century . The B+ IVS nt 110

mutation for b-thalassaemia, which confers some resistance to P. falciparum malaria, reaches its highest frequencies in Greece and was spread by Greek colonization. It is also common in the modern populations of those parts of southern Italy which were colonized by the Greeks in the seventh and eighth centuries . This indicates that the mutation was already present in human populations in Greece by then. The implication is that P. falciparum was already active in Greece by the eighth century  (see Ch. 5. 3 below for further discussion).

³⁷ Marchiafava and Bignami (1894); Grmek (1983: 65–6).

³⁸ For infection of harvesters see M. E. Danubio in Greene and Danubio (1997: 328) on Lodé; Bercé (1989: 242); Celli (1900: 176); North (1896: 243–4) on Lazio; Desowitz (1992: 111–12) on south-east Asia; M. T. Gillies in Wernsdorfer and McGregor (1988: i. 473) for Turkey; McNalty (1943) for infection of harvesters by P. vivax in Scotland in the eighteenth century. Plutarch, Moralia 137c, discussed by Jones (1908: 545), does not describe any symptoms of the ailments of harvesters. The Chronicle of Joshua the Stylite, ed. Wright (1882), ch. 85, p. 67, shows that in Syria at the end of the fifth century  it was normal for farmworkers to sleep outside on the threshing floor at the time of threshing.

3

Evolution and prehistory of malaria

Several quite different arguments have been proposed in favour of the theory of a late introduction (or reintroduction) of P. falciparum malaria to Greece and Italy. W. H. S. Jones was looking for an explanation for the decadence, as he saw it, of ancient Hellenic civilization. This approach can be safely dismissed now without further discussion. Zulueta and Grmek and other authors exploited a series of much more scientific arguments which certainly merit extensive discussion, one by one. These ideas are briefly summarized here, before discussion: (1) the hypothesis that P. falciparum must be a human pathogen of recent origin because its extreme virulence suggests that it has not had time to adapt to humans as a host;

(2) the hypothesis that large human population sizes would have been needed before malaria could become endemic in Greece and Italy;

(3) the hypothesis that the species of mosquito which were the most effective vectors of malaria in Europe would have taken several thousand years to spread into southern Europe after the end of the last Ice Age;

(4) the hypothesis that because these species of mosquito are refractory to tropical strains of P. falciparum a long period of evolution would have been required before they could become efficient vectors of the parasites.

It was once widely believed, as a general principle of parasite ecology and epidemiology, that parasites tend to evolve towards symbiosis or commensalism with their hosts, because in the long run it would not be in the interests of a parasite to kill its host.

This is frequently given as a reason why P. falciparum malaria, an extremely virulent disease, must be a human disease of recent origin, which might only have evolved during the last few thousand years. This theory bolstered the conclusions of A. P. Waters and co-workers, who argued on the basis of phylogenetic analyses of 24

Evolution of malaria

0.02

0.044

0.018

Babesia

0.042

0.050

9,998

Theileria

0.069

0.022

Eimeria

0.056

9,998

Toxoplasma

0.048

P. malariae

0.042

7,782

P. ovale

0.012

10,000

9,963

P. vivax

8,802

0.026

P. cynomolgi

0.014

6,120

10,000

P. knowlesi

6,123 0.015

P. fragile

0.029

0.024

P. lophurae

0.064

0.026

0.013

10,000

P. gallinaceum

9,993

0.009

0.034

P. reichenowi

10,000

P. falciparum

0.056

P. berghei

Figure 1. Evolutionary relationships of selected Plasmodium species indicated by neighbour-joining analysis of 18S ribosomal gene A sequences in a ClustalX alignment (Thompson et al. (1997) ), modified manually in the BioEdit sequence editing program (Hall (1999) ). The apicomplexan species Toxoplasma gondii, Eimeria mitis, Babesia bigemina, and Theileria annulata were used as outgroups, with 10,000 bootstrap replications. Bootstrap values are shown below the branches and branch lengths above the branches.

DNA sequences that P. falciparum is closely related to avian malarias, but not to other primate malarias, with the implication that P. falciparum malaria is the result of a lateral transfer of a malaria parasite from birds.¹ It remains controversial whether or not P. falciparum is more closely related to avian malaria species than it is to other primate malaria species. Settling this phylogenetic question is not essential for the purposes of this book, since the evolutionary relationships in question date back to over a hundred million years ago. However, the ecological problem is important for current purposes. Research in ecology in recent years has reached the conclusion that it is not inevitable that a parasite or other pathogen will evolve towards avirulence. It all depends on the precise circumstances, in particular it depends on the factors favouring transmission of the parasite to new hosts, which is what will determine its evolutionary fitness.

¹ Waters et al. (1991), discussed by Brooks and McLennan (1992) and McCutchan et al.

(1996).

Evolution of malaria

25

Since all the species of human malaria depend on Anopheles

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