Recent Origin of Plague Microbe Yersinia Pestis: Darwinian Evolutionary Process

The problem of new and reemerging diseases is the highly actual in evolutionary infectology. As to plague, there are two approaches to the problem of the recent origin of the plague microbe Yersinia pestis: molecular-genetic (MG) and ecological one. The paradigm of MG-approach is speciation of plague microbe not more then 20 000 y.a. by mode of genetic saltation (in general, by horizontal gene transfer of specific virulence plasmids pFra and pPst from environment or other bacterial species and by inactivation/deletion of nonfunctional genes) [1-3]. The MG-scenarios of the recent origin of plague assume speciation of Y. pestis from the pseudotuberculosis microbe Y. pseudotuberculosis O:1b in the populations of Microtinae species (voles) in different geographic regions: in Tibet, Caucasus, China Loss plateau or Africa (Nile valley, Angola) [4-9]. The phylogenies constructed by authors who used various MG indices place vole biovar Pestoides (genovars O.PE7, O.PE2, O.PE3, O.PE4) and “archeological” ones in the root of phylogenetic trees [3,9]. Close solidarity of MG-investigators create illusion of truth and indisputable of MG-phylogenies. However together with common consolidation of MG-investigators all MG-phylogenies haven’t support by ecological narrative. MG-approach haven’t ability to answer the trivial questions how, where, when clone of psychrophyle saprozoonose pseudotuberculosis microbe O:1b transform into population of causative agent of systemic plague infection. All MG-reconstructions of plague microbe origin and worldwide distribution on the Earth aren’t ecologically valid. In the same time the event of plague origin is recent enough, and its ecological circumstances may be investigated by actual eco-geographic methods.

Ecological approach has a richer biological and bio-geographic content. It throws a light on biogeocenotic prerequisites and ecological circumstances responsible for speciation of Y. pestis [10-12]. We have found that there is an intermediated environment (transitional medium, or transitional zone) in which diverse population–genetic and molecular processes of the gradual (Darwinian, not saltation) but rapid formation of Y. pestis species were realized between the extra-host environment of the pseudotuberculosis microbe (cold abiotic external organic) and the host environment of the plague microbe (lympho-myeloid complex of warm-blooded rodents and pikas) [10-13]. That intermediated environment became host-parasite system Mongolian marmot-tarbagan–marmot flea (Marmota sibirica–Oropsylla silantiewi). According to ecological scenario, causative agent of plague Y. pestis was formed in the host-parasite system marmot–flea in Last Ice Age, in Sartan cooling 22000 – 15000 y.a. in Central Asia, and after this it spread around the world by natural and anthropogenic ways (Figure 1).

Figure 1: The region of origin of the plague microbe Yersinia pestis in settlements of the Tarbagan marmot (Marmota sibirica) in Central Asia and its natural and anthropogenic expansion beyond the zone of primary natural focus. (I) The first pandemic, Justinian’s plague; (II) the second pandemic, Black Death; (III) the third pandemic, modern; 1, the southern boundary of the permafrost zone; 2, the Sahara– Gobi arid zone; 3, the boundary of the dominant distribution of the pseudotuberculosis microbe of the first serotype; 4, the region of speciation of the plague microbe and directions of its natural expansion in the Late Pleistocene– Holocene; 5, the range of the primary natural plague foci in Asia.

The transformation of the clone of the pseudotuberculosis microbe into the population of the causative agent of plague was predetermined by three main biogeocenotic prerequisites formed in Central Asia at and in Sartan time: 1) the unique behavior of Mongolian marmot in preparation for hibernation, 2) the specific behavior the O. silantiewi flea during of host hibernation, and 3) the physiology of marmots as heterothermic hibernating family–colonial animals [10,14]. We discovered that the main ecological principle initiated speciation process of Y. pestis was inadaptive traumatic infection of primary host – Mongolian marmot – by pseudotuberculosis microbe Y. pseudotuberculosis O:1b due to immediate contact of feces and blood in mouth cavity of hibernating marmots. This contact was initiated by tandem of specific behavior of Mongolian marmot (animals prepare plug in hibernating burrow from mixture of gravel and itself feces, move gravel by teeth and feces introduced in the mouth) and specific behavior of marmot flea larvas (in could months flea larvas due to positive thermotaxis move on to bodies of sleeping marmots, some of them introduce in marmot mouth, make scarifications and feed blood). Heterothermy (and heteroimmunity) of hibernating marmots created favorable conditions for adaptation of to be plague microbe to circulate in populations of homothermal rodents – recent hosts of plague microbe [10].

The description of the evolutionary principle (gradualism) and the ecological–genetic mechanisms (natural selection in the M. sibirica–O. silantiewi host-parasite system) of the plague microbe speciation opens up a way to the synthesis of molecular-genetic and ecological approaches in the problem of plague microbe origin and will be useful for development theory of molecular evolution as a whole.

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