Annotation
In 1894, at the beginning of the 3rd pandemic in Hong Kong, A. Yersin and Sh. Kitasato
discovered the causative agent of plague, but it took almost 100 years more to unveil the first secrets of
the origin of plague. In 1980 H. Bercovier, with co-authors, discovered that the homology between the
genomes of Yersinia pestis and Y. pseudotuberculosis was more than 90%. This pioneer observation
motivated further molecular genetic studies of the genus Yersinia. In 1999, M. Achtman, with co-authors,
showed that these bacteria diverged between 20–1.5 thousand years ago, in the late Pleistocene –
Holocene, thus providing further support for the theory of the recent origin of plague.
Considering all current hypotheses, only those of Dijatlov (1989) and Achtman et al., (1999) deal
with the place and circumstances of the recent origin of plague. The first hypothesis is not evolutionary.
The second hypothesis suggests that the plague microbe originated in Africa within populations of the
Nile grass mouse (Arvicanthis niloticus) and its specific flea parasite, Xenopsylla cheopis, along with the
expansion of ancient agriculture in the Nile valley. This hypothesis, however, has poor ecological
support, as it does not pay attention to the psychrophylic-dependent propagation of the
pseudotuberculosis microbe. It is well known that this microbe, unlike most bacteria, should be incubated
in a refrigerator at 4–8°C rather than in warm conditions. Vaschenok (1988) demonstrated that the
pseudotuberculosis microbe could be transmitted to laboratory animals by fleas only at temperatures of 6–
8°C. Therefore, events leading to divergence of pseudotuberculosis and plague microbes, and to worldwide distribution of the latter, likely occurred in the cold environment of Eurasia in the late PleistoceneHolocene.
By ecological approach we show that plague originated in populations of the Mongolian
marmot (Marmota sibirica) and its specific flea parasite, Oropsylla silantiewi, in Central Asia.
Unlike other marmots, the Mongolian marmot lives under psychroarid conditions. It is generally
accepted that M.sibirica speciated in the arid regions of Central Asia where low soil moisture is a
result of low precipitation and high intensity of solar radiation. All marmots plug the burrow
entrance with soil. However, dry soil makes an inadequate plug and encourages the unique
plugging behaviour of the Mongolian marmot. Unlike other species of American and Eurasian
marmots, the Mongolian marmot plugs the entrance of the burrow with a mixture of pebbles
cemented by feces, which accumulate in special “toilet” chambers of the burrows. Marmots
move this mixture using their mouths and feet, thus providing favourable conditions for the
pseudotuberculosis microbe to travel from feces to mouth and enabling its continuous circulation
in marmot populations.
Marmot hibernation consists of alternating short euthermic periods and long periods of deep
torpor. Body temperature in the torpid phase decreases to 1–5°C and reaches normal 37°C in the
euthermic phase. Marmots arouse 11 to 15 times during the winter. Body temperature in marmots differs
between individuals. For instance, adult males enter torpor later and become euthermic earlier than
females and young marmots do. Therefore, individuals in a population of marmots at a given time during
winter may have any body temperature from 5 to 37°C.
The specific parasitic flea O. silantiewi inhabits burrows of marmots; its imago can be found in
burrows throughout the year. Larvae of O. silantiewi are common on marmots in south Siberia and
Mongolia. The parasitic behaviour of O. silantiewi larvae is facilitated by their positive thermotaxis in the
temperature gradient present in the nests of hibernating marmots. Despite the similar seasonal
fluctuations of O. silantiewi on different species of marmots, only fleas infecting Mongolian marmots
display unique the ecological adaptation of larval hemophagy. During hibernation some of the larvae
move from the fur to the mouth of the marmot to feed on blood.
With these facts in mind, it is possible to postulate the ecological events, which led to the
transformation of pseudotuberculosis into plague in populations of the Mongolian marmot. During the
late Pliocene – early Pleistocene, south Siberia and central Asia had a dry, warm climate and were
covered by savanna-like landscapes. Due to the arid climate, M.sibirica originated in mountain regions
and developed the specific burrow-plugging behaviour in winter, thus enabling the favourable conditions
for the circulation of pseudotuberculosis microbe from feces to mouth. Throughout the Pleistocene, the
climate of Siberia and central Asia became more continental. The January isotherm –20° C shifted from
the Polar Regions to the center of Asia as far as Mongolia. About 22–15 thousand years ago, in the late
Pleistocene (Sartan time), the temperature dropped to extremely low levels. In an ecological response to
these conditions, flea larvae shifted to facultative hemophagy and the pseudotuberculosis microbe had the
opportunity to invade the cold blood of the sleeping Mongolian marmot by traumatic means, enabling this
morphogenesis by macroevolutionary way.
Further evolution of the plague microbe and its geographical expansion within Rodentia and
Lagomorpha employed adaptive radiation and adjustment to new ecological niches, leading to the
circulation of 25–30 microbe hostal subspecies in different parasitic systems of the "rodent-flea" type,
without significant changes of morphophysiology and metabolism, i.e., by microevolutionary way. The
natural range of plague has expanded on vast areas of Eurasia from Manchuria to Caucasus and Iranian
Kurdistan, and from southern Siberia, northern Kazakhstan and the northern edge of the Caspian Sea to
the southern part of the Indian Subcontinent, excluding Indochina and South China. In Asia, the natural
foci of plague have expanded southeastward, reaching colonies of Indian gerbils (Tatera indica) in
Indostan, as well as Himalayan marmots (M.himalayana) and dark-bellied voles (Eothenomys
melanogaster) in Yunnan.
Foci of plague in tropical Indochina, with X.cheopis as a vector, are confined to settlements and
surrounding agricultural areas. These foci are fundamentally different from natural plague foci by being
classically synanthropic. Due to human socialization in Indostan, the plague microbe (Yersinia pestis
subsp. orientalis by Devignat, 1951 = Y.pestis subsp. ratti by Toumansky, 1957 = subspecies from
populations of Indian gerbil T.indica) was introduced from populations of the Indian gerbil into
commensal rat populations, creating synanthropic “rat” foci, first within the rural flea – host system of
“Rattus rattus – Xenopsylla astia” and later developing within the anthropogenic system “Rattus rattus –
Xenopsylla cheopis.”. During the third pandemic, people transferred the “rat” plague microbe from such
synanthropic foci to coastal regions of Africa and New World.
The only hypothesis we support that is consistent with the above-presented concept is that of
Pollitzer (1954) concerning East African foci with marmot-specific subspecies of the plague microbe. It
states “the marmot-induced” origin of the second pandemic in Europe and the southern Mediterranean
countries with possible subsequent expansion to East Africa via the Nile valley.
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The main points of our concept are as follows. The natural foci of plague are a relatively recent
phenomenon. The establishment of the plague microbe took place without human participation in central
Asian populations of the Mongolian marmot during the late Pleistocene. The late Pleistocene Sartan
cooling and deep frost penetration of the ground induced the speciation of Y. pestis. Winter burrowplugging behaviour of Mongolian marmots inhabiting central Asia on the one hand, and the facultative
larval hemophagy of O.silantiewi due to deep freezing of the ground, on the other hand, were the main
ecological, or, better, behavioural (ethological) factors, allowing the origin of the plague microbe in the
Mongolian marmot – O. silantiewi system. The obligate blood parasitism acquired by the microbe in the
marmot population enabled its effective adaptive radiation in Eurasian populations of other small
burrowing rodents, including non-hibernating forms. Human social and economic activities facilitated
further transcontinental expansion of plague via synanthropic rats. Thus, the disease was transferred from
its primary foci in Eurasia to the other places, leading to the establishment of secondary natural foci in the
New World, Africa and other tropical zones.