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Microevolutionary Change in the Human Pathogenic Treponemes: an Alternative Hypothesis DON BROTHWELL Institute of Archaeology, London Wcl, England

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Microevolutionary Change in the Human Pathogenic Treponemes: an Alternative Hypothesis DON BROTHWELL Institute of Archaeology, London Wcl, England INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Jan. 1981, p. 82-87 Vol. 31, No. 1 0020-7713/81/010082-06$02.00 NOTES Microevolutionary Change in the Human Pathogenic Treponemes: an Alternative Hypothesis DON BROTHWELL Institute of Archaeology, London WCl, England Recent evidence from both archaeology and biology suggests that the taxonomy of the human pathogenic treponemes may be more complex than previously thought. An alternative evolutionary tree for the treponematoses is suggested. During the past 50 years there has been grow- dum, is involved. Hackett (9),on the other hand, ing interest in the ecology of the human patho- considers the same range of evidence and as a genic treponemes. Not only have they been clas- result supports the following classification: Tre- sified on clinical evidence into a number of spe- ponema pallidum Schaudinn (1905)-venereal cies, but also theories as to their evolution since and endemic syphilis, Treponema pertenue Cas- Pleistocene times have been put forward. Evi- tellani (1908)-yaws; “Treponema carateum” dence over the past decade, from both archae- Brumpt (1939)-pinta. (Note: Names in quota- ology and biology, now seems to demand a re- tion marks are not on the Approved Lists of consideration of the microevolution of trepo- Bacterial Names [Int. J. Syst. Bacteriol. 30:225- nemes (or “treponemata”) of this kind. 420, 19801.) A variant of the latter classification For perhaps three or four centuries, syphilis is suggested by Hardy (ll),who accepts that the has been a subject of considerable epidemologi- differences between endemic and veneral syph- cal and clinical interest (16). Since 1905 (20), ilis are equally deserving of specific (or subspe- when Treponema pallidum was incriminated as cific) distinction, and therefore he would seem the causative agent of syphilis, the taxonomy to accept “T. endemicurn” (or “T. pallidum of the microorganisms producing the human endemicum”) as the causative agent of endemic treponematoses has slowly attracted attention. syphilis. Whichever side is taken in this debate, As Hudson (13) points out, the generic name of course, most authors accept that the taxon- Spirochaeta was earlier preferred by some med- omy of these pathogens can only be tentative, ical biologists, but after some controversial ex- and perhaps significant steps will be made when changes (19, 23), Treponema was accepted as in vitro cultures of these varieties are eventually properly in accord with taxonomic principles, studied. However, this does not mean that hy- although the American Medical Association did potheses concerned with the microevolution of not seem to give it official recognition in their these treponemes should not be advanced. journal until 1943. Moreover, whether the four treponemal patho- The treponematoses are comprised of four gens considered here are worthy of species, sub- distinct clinical entities: venereal syphilis, en- species, or varietal status, their evolutionary re- demic syphilis, yaws, and pinta (9,13-15). These lationships remain basically the same. But what divisions are made on pathological and clinical is their relationship to space and time? evidence rather than on any taxonomic relation- Previous evolutionary schemes. Although ships of the organisms themselves (Table 1). Hudson (13,14) and others have commented on Even electron microscopy has so far failed to the apparent association between the syphilis, reveal structural differences, although these yaws, and pinta treponemes and climatic-cul- pathogenic treponemes can be distinguished tural factors, Hackett (9) alone has constructed from others by having pointed ends with three a workable evolutionary tree for these microor- flagella inserted subterminally in a row (12). ganisms. Minor alternatives to the same basic Failure so far to demonstrate differences of eco- scheme are shown in Fig. 1, hypothesis A being logical significance in the microorganisms iso- preferred by Hackett on evidence available to lated in these four disease groups has resulted in him in 1963. On this overall medical information, differences of opinion as to whether more than he suggests that the pinta form was the fust one species is involved. Hudson (13), in partic- variant evolving from a basal treponemal stock ular, has argued that only one species, T.pal& (representatives of which do not occur in most 82 VOL. 31,1981 NOTES 83 TABLE1. Clinical characteristics of the four treponematoses (modified from Hackett [9]) Endemic Venereal Yaws Character Pinta s-mhilis smhilis Usual source of treponemes Skin anywhere Skin anywhere Buccal mucosa Genital and mucosal lesions Size of infectious area Large Large Small Small Duration of Infectiousness of individ- Many years A few months A few months A few months ual lesions Infectiousness of patients, Many years 3-5 yr 3-5 yr 3-5 yr including infectious re- lapses Latency" Absent Characteristic Characteristic Characteristic Lesions: Initial, site Exposed skin Skin of legs Mouth? Genital Generalized skin, extent Extensive Extensive Limited Moderate Genital, occurrence Unusual Scanty Scanty Frequent Buccal mucosal, occur- Absent Scanty or Moderate Scanty rence absent Palmar and plantar hyper- Absent Frequent Scanty Scanty keratoses, occurrence Bone, occurrence Absent Moderate Moaerate Scanty Juxta-articular nodules, Absent Frequent scanty scanty occurrence Heart, brain, and other Absent Absent Scanty and Moderate viscera, occurrence mild, or absent Congenital transmission Absent Absent Absent Present Age group for most infec- Children Children Children Adults tions " Latency in a communicable disease is a stage in its course in which there is evidence of infection such as seroreactivity but no clinically detectable active lesions. modern populations). By further mutation and fit both clinical and archaeological information divergence, yaws organisms evolved in humid, now available. Paleopathological discoveries in warm environments, and then endemic syphilis the last 10 years related to the question of tre- evolved from yaws as a means of adapting to ponemal microevolution and dispersal have been arid, hot climates. Venereal syphilis is seen as a principally as follows. late culmination of microevolutionary change, (i) Osteological evidence in the Marquesas linked with climatic change, decreasing endemic islands, Borneo (3), and Tonga (13) suggesting syphilis, denser settlement, more clothing, and infection by one or more varieties of Treponema perhaps even changing sexual behaviour. Will- confirms the previous claim of a yaws type of cox (24, 25) echoes this view in that he sees disease in the Marianas islands (229, and it now treponemal divergence occurring sequentially as looks certain that early Southeast Asian popu- a result of mutation and the selection of a path- lations had gradually extended the treponeme ological state best suited for the continuing range into the central Pacific. transmission from host to host in the particular (ii) Further studies on Amerindian skeletons environment. from North and Central America have estab- Some years ago, modification of Hackett's lished beyond reasonable doubt that treponeme original changes in the spatial distribution of the varieties in the Pre-Columbian New World (5) treponematoses through time seemed to me (2) included one which produced bone lesions dis- to be essential, as various archaeological discov- tinctive of a treponematosis. As some of these eries were casting some doubt on the interpre- cases are from arid zones in Mexico (4) and tations arrived at purely by extrapolating back Arizona (and also probably Peru) (26), trepone- into time from modern clinical evidence. Further mal differentiation was clearly adapting here to archaeological evidence leads me to suggest that hot and dry as well as to more humid climates the time has arrived for at least a consideration (as experienced by the Illinois and Florida Amer- of alternative hypotheses concerning trepone- indians) (17). Moreover, this also seems to dem- mal evolution, especially if they would seem to onstrate that pinta was not the only early New 84 NOTES INT, J. SYST.BACTERIOL. HYPOTHESIS A HYPOTHESIS B FIG. 1. Hypotheses A and B, as suggested by Hackett (9), to explain the microevolution of human pathogenic treponematoses. World treponeme variety, and from the valley of modification of previous hypotheses is possible, Tehuacan in Mexico (1) there is clear evidence if not desirable. of a bone-changing treponematosis at least 2,200 From clinical evidence, it is established that years ago. To me, this is a very important point four main pathogenic varieties of Treponema which so far has not been considered in relation affect humans today. The probable Pleistocene to treponeme evolution. isolation of populations in such areas as New (iii) Although the Aswan project in Egypt and Guinea and Australia and the development in Nubia has resulted in large numbers of extra these communities of yaws-endemic syphilis dis- skeletons being available for study, there still eases suggest that some form of treponematosis remains no evidence of early treponemal disease has affected humans since at least late Pleisto- in Africa. cene times. If treponemes were carried into the (iv) Large numbers of skeletons continue to Americas by early Paleo-Indian groups (rather be excavated in northern Europe, and there is than having had a trans-Pacific entry into the still no evidence of treponemal disease until late New World), then again a Pleistocene antiquity medieval times (circa A.D. 1200 to
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