ISSN 1062-3590, Biology Bulletin, 2009, Vol. 36, No. 6, pp. 547–554. © Pleiades Publishing, Inc., 2009. Original Russian Text © V.V. Suntsov, N.I. Suntsova, 2009, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2009, No. 6, pp. 645–653.

THEORETICAL BIOLOGY

Principles of Speciation of the Plague Causative Agent Versinia pestis: Gradualism or Saltation? V. V. Suntsova, c and N. I. Suntsovab, c aSevertsov

Institute of Problems of Ecology and Evolution, Russian Academy of Sciences, Leninskii pr. 33, Moscow, 117077 Russia bMoscow State University, Ecological Center, Moscow, 119899 cRussian and Vietnam Tropical Center, No. 3 Street 3/2, 10 Distr., Ho Chi Minh City, Vietnam e-mail: [email protected] Received January 19, 2009

Abstract—The saltation origin of the causative agent of the plague Yersinia pestis from the pseudotuberculosis microbe Y. pseudotuberculosis O:1b has been proclaimed in recent investigations on molecular genetics. The speciation process in this case is proposed to be connected with horizontal transfer of exogenous genetic structures (such as specific plasmids pFra and pPst) into the genome of the ancestral form. The alternative “Darwinian” model of the gradual origin of the plague agent is proposed based on ecological factors. The comparison of two evolutionary scenarios, saltation and gradual, is performed; the latter seems more likely. DOI: 10.1134/S1062359009060016

Gradualism or saltation? This problematic question on the principles of the origin and development of living beings remains one of the most important in modern evolutionary theory (Nazarov, 1991; Iordanskii, 2001; Kolchinskii, 2002; Yablokov, Yusufov, 2006). Gradual evolution is interpreted as continual (although not always uninterrupted) formation of new features of living things; saltation is viewed as a one-act origin of evolutionary novelties leading to the appearance of a new life form. Saltation evolution could be better referred to as genetic revolution. The gradualistic interpretation of the evolution of organic life has its roots in the ancient past and was revived by followers of classic evolutionary theory, Darwinism. Its contemporary interpretation (synthetic theory of evolution, STE) includes the population approach and factors common for all species of living organisms, i.e., inheritable variability, isolation, waves of life, struggle for existence, and natural selection. The local population is considered to be the elementary unit of the evolutionary process, with population and genetic transformations and natural selection; individual organisms are not considered as objects of evolution (Mayr, 1974). Scientifically explained ideas of saltation are relatively recent and have been around for just about a century. They are now widely supported by the young biological discipline, molecular genetics (MG). In most orthodox saltation theories, the question on the reasons for transformation of a population into new species is out of bounds, as the population approach itself is rejected in consideration of all evolutionary events; saltation to a new form occurs in individual organisms

simultaneously or in a few generations which give rise to new taxon of species (or higher) level. In the past two decades, the discussion on saltation or the gradual origin of new forms of causative agents has garnered special interest in medical microbiology and infectology. This is connected with the emergence and reemergence of new infectious diseases, the tragically known plague being one of them. Theories of the saltation type prevail here and proclaim the paradigm of horizontal (lateral) gene transfer (LGT) (Zavarzin, 1974; Prozorov, 2000; Koonin et al., 2001; Kunin et al., 2005). It is proposed that gene interchange between individuals of different species via transformation, transduction, and conjugation is regularly realized in prokaryotes. However, such data were obtained in laboratory conditions in pure cultures of microorganisms, on rich nutritive mediums, and with high concentrations of both donors and recipients. Data on gene transfer in natural associations of prokaryotic organisms are comparatively poor. Hence, the question on peculiarities of natural gene transfer remains under discussion. In general, the data obtained by MG are of poor biological content and give the opportunity to construct “trees” of genes only, not taxa (Pavlinov, 2005; Konstantinidis et al., 2006). If we evaluate the state of problem of gradations and saltations in evolutionary theory, it should confirm that contemporary orthodox Darwinists and saltationists stand on diametrically opposed positions of either uninterrupted or punctuated process of evolution (Kurland et al., 2003). Other than these, there do exist some inter-

547

548

SUNTSOV, SUNTSOVA

mediate opinions and solutions that tend to smooth away these opposing points of view. The original work is based on ecological studies and proposes a scenario of the origin and evolution of the plague microbe Y. pestis. This scenario is a simple model that can easily be understood by specialists of different fields and seems to help in resolving the dilemma “gradualism or saltation.” The synthesis of ecology and MG represents a possible way out from theoretical difficulties in reconstruction of phylogenies. This application of ecology (synecology) is theoretically supported by the well-known Godel theorem which states that in every axiomatic system problems may arise, which can be resolved only within another (sometimes more general) system. For example, calibration of the “molecular clock” of higher animals and plants cannot be performed within molecular biology itself, as it depends on paleontological, paleoclimatological, and geochronological data. As for the given work, this theoretical foundation should be interpreted in a way that processes of molecular evolution of the plague causative agent should be reconciled with evolutionary processes on higher levels of life organization (cell, organism, population, biocoenosis). However, the population-specific level remains central in questions of evolution: the population is the elementary unit of the evolutionary process and form of existence of species, while species represents the form of life’s existence (Shvarts, 1980). Ecological descriptions of evolutionary processes help to uncover the general picture of genesis of populations, species, and biocoenoses in real abiotic circumstances, and this picture can serve as a sample for correction of MG scenarios or a Procrustean bed of some kind which can reject MG solutions which go beyond the frames of biological (ecological) logics. Many researchers now confirm the inconsistency of identification of traditional and MG reconstructions of phylogenies. “Taxon” and “gene” trees need to be distinguished, the former corresponding to cladogenetic reconstructions (taxa divergence), while the latter are of semogenetic nature (i.e., they reflect divergence of certain traits). In this work, a comparison of saltation and gradual scenarios of the origin of the causative agent of the plague is undertaken. The saltation model was constructed according to data from MG works of the past decade (Achtman et al., 1999, 2004; Pourcel et al., 2004; Song et al., 2004; Zhou et al., 2004a, b, c; Cui et al., 2008; Li et al., 2008), and the paradigm of LGT serves as the theoretical basis of this model. A gradual model was originally constructed within the context of STE based on ecological observations and zoological and parasitological material obtained from Central Asian (Tuvinian) natural and tropical rat (Vietnam) anthropogenic loci of the plague. The causative agent of the plague is the obligate parasite of wild burrowing rodents and lagomorphs. MG methods indicate that it diverged from a weakly viru-

lent saprozoonosis causative agent of the pseudotuberculosis Y. pseudotuberculosis O:1b, intestinal parasite of numerous animals, not earlier than 20 000 years ago (Achtman et al., 1999, 2004; Skumik et al., 2000). The phylogenetic youth of the causative agent of the plague is also obvious from widely known microbiological, epidemiological, epizootological, and ecological data and facts (Dyatlov, 1989; Suntsov, Suntsova, 2006). Exciting scientific intrigue arose connected with the following questions: what events happened on Earth in the recent past (at the end of the last glacial period and after it) which led to the origin of a dangerous blood parasite from a weakly virulent intestinal microbe and its wide (almost global) distribution; what is the nature of selective factors that provoked the divergence of this microbe; where and how did such events happened? The search for the evolutionary roots of the plague microbe is now carried out mostly by molecular geneticists within the LGT concept, which is out of touch with classical biological sciences, such as zoology, ecology, parasitology, biogeography, physiology, paleontology, paleoclimatology, and many others, and an integral understanding of multilevel evolutionary processes cannot be achieved within the framework of only one chosen approach in biology. By the beginning of 21st century, a multitude of facts had been accumulated by the classical disciplines listed above, thus providing the opportunity to obtain coordinated and convincing pictures of the development dynamics of nature during the last glacial period and in the Holocene of the Palearctic. This information has helped to reconstruct the history of former and contemporary areas of habitat together with the intraspecific structure of many contemporary species of rodents and pikas, the main hosts of the plague microbe; the features of their ecology connected with the beginning and end of the glacial epoch (and hence the history of natural plague burrowing) are also of significant interest. The main reason for the leadership of MG in the problem of the origin and evolution of the plague microbe is the deep contradiction between one of the basic ideas of th classical theory of the natural facility of the plague (i.e. idea of geological antiquity of causative agent) and the results of contemporary MG investigations on the bacteria of genus Yersinia. These results leave no doubts as to the phylogenetic recentness of this microbe. Other reasons also exist. MG data reveal the ancestor of the plague microbe and spurred some proposals on the age of bifurcation of ancestral and affiliated forms and divergence of the main phyletic lines (biovars, subspecies) of Y. pestis species. MG research enabled the construction of “rooted” and “oriented” genealogical trees of genus Yersinia, although disputable but deserving discussion. They also provided a foundation for phylogeographical analysis of intraspecific variation of the plague’s causative agent, which BIOLOGY BULLETIN

Vol. 36

No. 6

2009

PRINCIPLES OF SPECIATION OF THE PLAGUE CAUSATIVE AGENT Yersinia pestis pestoides

549

Yersinia pestis ant med ori

Second phylogenetic event: acquisition of plasmid pPst Synthesis of pesticine First phylogenetic event: acquisition of plasmid pFra1 Synthesis of Fra1 Yersinia pseudotuberculosis O:1b Fig. 1. Scheme of saltation origin and evolution of the causative agent of the plague via “penetrance” of specific plasmids pFra and pPst. Biovars: ant, antiqua; med, medievalis; ori, orientalis.

was out of reach of the classical theory of the natural facility of this disease. The significant shortcoming of application of MG methods in the phylogenetics of the Y. pestis microbe is connected with the fact that the results of analysis based on certain gene structures (MG markers, gene fragments) are directly transferred to the phylogeny and taxonomy of the studied group. This can lead to serious misrepresentations, especially when single individuals or limited samples are used. However, this case is typical almost for all works on phylogenetics and phylogeography, as MG methods are expensive and tedious (Abramson, 2007). One more shortcoming of MG methods is that the topology of the obtained phylogenetic trees is strongly dependent on the choice of molecular marker; adequate selection of the latter represents certain difficulties. In the phylogeny of the plague microbe, methods with different markers lead to obviously different results (Achtman et al., 2004; Pourcel et al., 2004; Gu et al., 2006; Torrea et al., 2006; Vergnaud et al., 2007; Cui et al., 2008; Li et al., 2008). The results of MG investigations on the plague’s causative agent prompted the almost accepted opinion that its virulence and pathogenic capacities result, besides from mutations, recombinations, and deletions, from integration of exogenous genetic structures of different sizes (mobile genes, gene blocks, transposons, plasmids) into the genome of an ancestor from the outer environment and/or from other intestinal microorganisms, sometimes taxonomically distant from the plague microbe. However, no such works indicate a reliable source of integrating genetic structures, nor has a natural process of their penetration into the newly formed BIOLOGY BULLETIN

Vol. 36

No. 6

2009

plague cell been uncovered. For example, no comments on the principle of “penetration” of specific plasmids pPst and pFra are given; specific plasmids are by definition formed endogenously, thus becoming specific. If the kind of their acquisition from unknown precursors is discussed, they cannot be defined as specific. Major one-act changes in the genome of the plague’s causative agent, which abruptly alter metabolic interactions between a singular microbe cell and the environment, reflect the saltation approach to the problem of speciation in prokaryotes (Fig. 1). Microbes of the plague which circulate in populations of Brandt’s vole (Transbaikalia, Manchuria, Mongolia), Pere David’s vole (Yunnan), and the common vole (Dagestan, Caucasus) possess some biochemical features which draw them together with the pseudotuberculosis microbe (Domaradskii, 1998; Zhou et al., 2004a, b). According to certain MG traits, some researchers also tend to bring together the pseudotuberculosis microbe with the plague causative agent from vole populations of the Caucasus, Middle Asia, and China (Filippov, 2000; Kukleva et al., 2002; Motin et al., 2002; Achtman et al., 2004; Song et al., 2004; Zhou et al., 2004a, b, c; Vergnaud et al., 2007; Cui et al., 2008; Li et al., 2008). The similarity in biochemical and molecular features led to a hypothesis on the role of the vole’s biovar as an medial form between the ancestral pseudotuberculosis microbe and the descendent plague microbe; microbes from all vole populations (even geographically distant from each other) are in this case referred to as one biovar or subspecies, vole’s (pestoides, microti, microtus, minor). As a result, the area of habitat of subspecies Y. pestis “pestoides” is spatially disrupted into a few distant “islands.”

550

SUNTSOV, SUNTSOVA

Other scenarios of divergence of pseudotuberculosis and plague microbes are constructed according to the MG approach and in general resemble the one depicted in Fig. 1. The following features of the scenario of saltation origin and evolution of the plague microbe can be listed. (1) Accidental appearance of species-forming mutation (macromutation, system mutation, LGT) somewhere in the world regardless of geographical locality, content, and structure of the environment (biogeocoenosis). (2) Negation of gradual cumulative character of evolutionary novelties in the plague microbe. (3) Isolation of the problem of evolution of a causative agent from the evolution of host and vector. (4) Denial of creative role of natural selection and adaptive character of speciation process; evolutionary process is not interpreted as adaptatiogenesis, no leading role is attributed to natural selection in the origin of the plague: a new mutant appears in facilities and gives a new evolutionary line. (5) Denial of population approach: the basic unit of evolutionary process is the single microbe cell. (6) Correspondence of scenario to the typological conception of the absence of an uninterrupted row of retrospective intermediates. This situation resembles the idea of punctuated equilibrium in a paleontological chronicle, which proclaims a true absence of intermediates, not the incomplete character of the chronicle itself. (7) The widely accepted (in classical evolutionary theories) concept of preadaptation finds no reflection in this scenario. Thus, the speciation of the plague’s causative agent, as interpreted by molecular geneticists, occurred in the organism of some vole species of the genus Microtus (or another genus) from solitary microbe cells of pseudotuberculosis agent via spontaneous major alterations of the genome of, according to sentence of the well-known antidarwinist R. Goldschmidt (Goldschmidt, 1940), hopeful monsters. The conception of saltations via acquisition of major gene blocks, transposons, and plasmids seems to be less than convincing. Integration of structural elements (features) is the inalienable characteristic of any organism (Kurland, 2000). According to the classical point of view, macromutations lack adaptive capacity; macromutants are nonviable in natural habitats because of loss of morphophysiological correlations and coordination of organs (organoids, organelles) and whole organisms. It should be noted that the opinion on the saltation origin of the plague microbe is not completely unquestioned among molecular geneticists. For example, Wren (2003) discusses the “quantum leap in the blink of an eye” of the plague causative agent on the geological scale, thus not leaving the idea of the gradual origin of species.

Recently, an article by authoritative Chinese molecular geneticists was published, in which the authors analyze the model of gradual formation of genetic structures encoding the virulence capacity of the plague microbe after divergence of the initial clone from the population of the pseudotuberculosis microbe (Zhou, Yang, 2009). Notably, despite the eclectic approach in the problem of the origin of the plague (mechanical combination of LGT paradigm and selectogenesis), molecular geneticists themselves begin to feel the necessity to expound their positions in terms of STE (preadaptation, vertical inheritance of traits, gene drift, isolation of clones and intraspecific forms, genotypic and phenotypic structure of population, gene flow, selective advantage, and natural selection). As opposed to the LGT paradigm, formation of the plague microbe from the pseudotuberculosis agent might occur comparatively slowly, gradually but not obligatorily evenly according to STE. To accept the “Darwinian” way of speciation of the plague causative agent, one should demonstrate the existence of the intermediate medium and indicate (or give logic proofs) the existence of intermediate live forms as real or retrospective natural phenomena. The classical methodology of phylogenetics is based on the method of “triple parallelism” and needs to coordinate data from comparative anatomy and morphology, embryology, and paleontology. This approach has a strictly limited potential in reconstruction of the evolutionary process in prokaryotes. Hence, as the adaptation of the plague microbe is directed at its habitat (i.e., parasite system “rodent–flea”), we constructed the scenario of its origin and evolution concentrating on ecological aspects of problem, viz. interaction between causative agent and certain rodent species (Mongolian marmot Marmota sibirica and the specific flea of Eurasian marmots Oropsylla silantiewi, respectively). These objects were chosen basing on the sum of the knowledge on different aspects of Pavlovskii’s (1946) theory of natural facility of transmissive diseases of humans and animals and original ecological observations in Central Asia. The peculiarities of ecology of the Mongolian marmot and flea O. silantiewi gave the opportunity to reconstruct the circumstances in which excrements and blood of animals appeared in contact and intestinal microbe had the opportunity to perform an evolutionary transition to a new environment, i.e., new adaptive zone. This scenario was described in earlier works (Suntsov et al., 1997; Suntsov, Suntsova, 2000, 2006, 2008). It reflects the ecological approach to reconstruction of the phylogeny of genus Yersinia and species Y. pestis based on analysis of the adaptive capacities of hosts, vector of causative agent, and the causative agent itself against the background of global climate changes. The results of field zoological, parasitological, and ecological observations served as a foundation for a new conception of the origin of the plague causative agent. BIOLOGY BULLETIN

Vol. 36

No. 6

2009

PRINCIPLES OF SPECIATION OF THE PLAGUE CAUSATIVE AGENT

Va

lda

i

ci gla

ati

551

Sarta nian cooli in Si ng beria 22 00 Deep 0–15 000 y soil freez ears ago ing

on

43° 1 2

ra Saha

–Gob

i

d ari

zo

ne

3 4 5 Fig. 2. Region of the origin of the plague microbe in Central Asia. (1) contemporary area of permafrost; (2) arid areas of Eastern hemisphere; (3) area of the origin of the plague microbe on the combined territory of the Sahara–Gobi arid zone and area of permafrost rock; (4) distribution of maximum Quaternary (Sartanian) frost up to borders of Northern Gobi (43° North); (5) area of primary natural plague loci in arid and subarid regions of Eurasia. Arrows indicate directions of natural expansion of the microbe from Mongolian marmot populations at the end of the Pleistocene and Holocene.

The microbe Y. pestis diverged from an intestinal parasite, the pseudotuberculosis microbe of the 1st serotype (O:1b) in the late Pleistocene (during the maximum cold Sartanian age, about 22000–15000 years ago) in Central Asia (Fig. 2) in the parasitic system “Mongolian marmot–flea O. silantiewi.” This system can be interpreted as a distinctive temperature and immunological “evolutionary field” with a temperature range of about 5 to 37°C. Ground freezing to the depth of the wintering chambers of the marmot (2 m and deeper) served as the inductor of speciation, as it provoked unusual behavior in the larvae of the marmot’s flea: they moved from the nest lining to the body of the hibernating marmot, thus accepting facultative hemophagy. Due to such behavioral novelty, “gates” for the traumatic (mechanical) penetration of the pseudotuberculosis microbe appeared in the oral cavity of the marmot; the microbe could move to the blood from fecal particles that entered the mouth during construction of the wintering habitat. Two stages were described in the original ecological scenario of the origin and evolution of the plague causative agent, macro- and microevolutionary. Macroevolution, similarly to microevolution, seems to be a population genetic, not historical (phylogenetic) process (Fig. 3). This process occurred on the brink of life and death of the initiating population of a new species under the extreme influence of the environment, thus differing BIOLOGY BULLETIN

Vol. 36

No. 6

2009

from microevolution. The latter seems to be soft “fitting-in” to concrete “hostal” habitat. The characteristic features of the gradual scenario are listed below. (1) Data from different natural disciplines were used for reconstruction of the scenario, i.e., ecology, biogeography, paleontology, paleoclimatology, microbiology, parasitology, epizootology, molecular genetics etc., thus making the model more reliable and “parsimonious.” (2) The behavior of the marmot inhabiting arid territories of Central Asia is connected with preparation for winter hibernation, while the nutrition regime of the marmot’s flea (capacity to alter saprophagy or detritophagy with parasitism) is characterized with instability. These peculiarities are interpreted as basic ecological (ethological) factors of the environment (biocoenosis) that underlie formation of the epizootic system of the plague. (3) The initial reason for the origin of the plague’s causative agent was connected with changes in the climate in Northern Asia, Siberia, and Central Asia in the late Pleistocene and Holocene. After establishment of a strict ultracontinental climate, the ecosystems of Central Asia were overbalanced; subsequent rapid (or, in some estimations, catastrophic) changes in physical

552

SUNTSOV, SUNTSOVA

8–5 thousands of years ago

Pleistocene

10 thousands of years ago

Ma Mj

22 thousands of years ago

Adaptive radiation, formation of hostal subspecies

Intraspecific divergence and geographical expansion 37°C Yersinia (Yersinia) pestis tarbagani

+26°C 15 thousands of years ago ic ermne nt h t e ero mu Heteroim vironm t n e he +5°C

LBEm AcMf

Microevolution

Heat

Synthesis of Fra1, specialization, stabilization of traits Macroevolution

Holocene

Cold

Synthesis of pesticine, bifurcation of ancestral and descendent forms

Yersinia pestis ssp. Heat

Increase of polymorphism

Isolation of the initial clone, gene drift Abrupt fall of temperature, deep ground freezing, transition of marmot’s flea’s larvae from saprophagy to facultative hemophagy, scarifications on mucous membrane of the mouth of the Mongolian marmot

Yersinia (Pfeifferia) pseudotuberculosis O:1b

Transition to principally new environment, speciation with features of genus and family

Fig. 3. Gradual (Darwinian) model of the origin and evolution of the causative agent of the plague. Certain indirectly connected phyletic lines of subspecies of the plague microbe circulating in populations of different vole species: Lb, Lasiopodomys brandti; Mf, Microtus fuscus; Em, Eothenomys melanogaster; Mj, Microtus juldaschi; Ma, Microtus arvalis; Ac, Apodemus chevrieri.

and climatic circumstances led to significant alterations in the behavior of the marmot flea. It moved up to facultative parasitism; i.e., its populations crossed the bounds of normal behavior. As a result of such a “mechanistic” shift, in marmot coadaptive complex of Central Asian mountains and steppe, the conditions for transition of the intestinal parasite to existence in the lymph and blood of an active host appear. (4) The pseudotuberculosis microbe possesses some peculiarities, such as invasive capacity (possibility to infect endothermal animals after cultivation at low temperatures about 5°C above zero), presence of antiphagocytic factors in cells, possibility to reproduce in macrophages, ability to form biofilms, etc. (Zhou, Yang, 2009). These features can easily be interpreted as preadaptations to survival in the “cold” blood of the hibernating marmot and flea organism and hence to transformation into plague causative agent. The pseudotuberculosis microbe from Siberia, the Far East, and Central Asia, excluding others, possesses two cryptic plasmids in its genome (Eppinger et al., 2007). Possibly they served as precursors for specific plasmids pPst and pFra of the plague microbe.

(5) The macroevolutionary gradual character of the transformation of the pseudotuberculosis microbe into the causative agent of the plague is also obvious. The evolving microbe gradually moved from an open parasitic system (digestive system of rodent—outer environment (soil)—rodent) into a closed one (lymphomyeloid complex of rodent—digestive tract of flea—rodent), while metabolic processes of the microbe underwent certain changes. The vector of motive selection was directed at the temperature gradient from 5°C (state of deep marmot’s hibernation, intensive reproduction of psychrophilic pseudotuberculosis microbe) to 37°C (stable equifinal state of the plague microbe in the organism of the endothermal host). (6) Intraspecific evolution of the plague microbe followed the microevolutionary principle of adaptive radiation. (7) The scenario represents an encyclopedic evolutionary model demonstrating numerous questions of evolutionary theory, i.e., the interrelation between micro- and macroevolution, gradualism and saltation, macroevolution and phylogenesis, mono- and polyphyly; coherent, noncoherent and quantum evolution; role of heterobathmy (mosaic evolution) and preadapBIOLOGY BULLETIN

Vol. 36

No. 6

2009

PRINCIPLES OF SPECIATION OF THE PLAGUE CAUSATIVE AGENT

tation in macroevolutionary events; parallelism convergence and homoplasy in formation of new life forms and taxa, etc. (8) The model indicates that the analysis of general problems of evolutionary theory should be better begun from population and genetic macroevolution which results in speciation (in the given model, the new species has features of a new genus and a new family), and then move to microevolution, i.e., transformation of the initial population of a new monotypic species into a polytypic species. Hence, the sequence of stages of evolutionary transformations can differ from the one declared by STE. (9) The gradual model allows logically presentation and characterization of retrospective intermediate forms between causative agents of pseudotuberculosis and plague, which existed in the population of heterothermic Mongolian marmots between synthesis of the pesticine antibiotic by the plague microbe. This substance provided a clear hiatus between species. Hypothetical intermediate forms might satisfy the requirements of wide polymorphism (phenotypic and genotypic dispersion). (10) The scenario obviously demonstrates a real heterothermic (heteroimmune) intermediate environment available for multicomponent investigation, the parasitic system “Mongolian marmot–flea O. silantiewi” in which transformation of the pseudotuberculosis microbe into the plague causative agent occurred. Despite statements of antidarwinists that higher taxa cannot evolve via gradual genetic transformations of the population, this process really exists. This confirms the statement of STE on the unity of macro- and microevolutionary population genetic processes. (11) Finally, the proposed scenario logically enters the more general scenario of changes in the climate and biota of Northern and Central Asia during the last glacial period and after it. The extinction of mammoths and other gigantic animals coincided with the origin of the microscopic causative agent of the plague. When comparing the presented scenarios of the causative agent’s evolution, the second, gradual, seems to be more reliable and natural. From a pragmatic point of view, the “Darwinian” model has a certain significance for problems of public health protection: new diseases arise during abrupt natural and anthropogenic alterations in the environment in some regions under specific physical and climatic, ecological and biocoenotic, and also social economic and demographic (in historical period) conditions. The population of a causative agent passes in an evolutionary way gradually in the heterogenous intermediate environment through polymorphic intermediate forms. In this case, the possibility to foreknow and prevent the appearance of a new causative agent exists. In conclusion, we would like to express our hope that further saturation of the two presented scenarios with facts together with construction of other models BIOLOGY BULLETIN

Vol. 36

No. 6

2009

553

would contribute significantly to solution of one of the most important problems of evolutionary theory: gradualism or saltation, one which would appear to be more incorporated into the general theory of evolution and generate a more detailed investigation program may have more success. While such a program successfully directs the activity of scientists, it would be invulnerable to critics. Mistakes and prejudices are better revealed not comparing certain facts (what is usually practiced in science) but comparing hypotheses and theories as a whole. There are plenty of such hypotheses in the problem of the origin and evolution of the causative agent of the plague, while only one of them can be true. On the other hand, when analyzing Figs. 2 and 3, some similarity in scenarios seems to exist. Moreover, the example of formation of genetic structures of the plague microbe responsible for high virulence and pathogenicity was cited above (Zhou, Yang, 2009), which, although seems eclectic and mechanically combining the ideas of LGT and selectogenesis, appeared to be an intermediate opinion in the dilemma “gradualism/saltation.” It is possible in this case that these scenarios are not mutually exclusive but rather complement: “gene trees” somewhat correspond to “taxa trees.” From such a point of view, the necessity of ecological and genetic synthesis is needed for reconstruction of the phylogeny of the Y. pestis microbe. One should precisely study the reasons for differences and contradictions in scenarios and generate a sensible compromise solution. It cannot be excluded that such a compromise would find its place in the theory of punctuated equilibrium. REFERENCES Abramson, N.I., Phylogeography: Results, Problems, and Prospects, Vestnik VOGIS, 2007, vol. 11, no. 2, pp. 307–331. Achtman, M., Morelli, G., Zhu, P., et al., Microevolution and History of the Plague Bacillus, Yersinia pestis, Proc. Natl. Acad. Sci. USA, 2004, vol. 101, no. 51, pp. 17837–17842. Achtman, M., Zurth, K., Morelli, G., et al., Yersinia pestis, the Cause of Plague, Is a Recently Emerged Clone of Yersinia pseudotuberculosis, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, no. 24, pp. 14043–14048. Cui, Y., Li, Y., Gorge, O., Platonov, M.E., et al., Insight Into Microevolution of Yersinia pestis by Clustered Regularly Interspaced Short Palindromic Repeats, PloS ONE, 2008, vol. 3, no. 3, pp. 1–10. Domaradskii, I.V., Chuma (Plague), Moscow: Meditsina, 1998. Dyatlov, A.I., Evolyutsionnye Aspekty V Prirodnoi Ochagovosti Chumy (Evolutionary Aspects in Plague Natural Nidality), Stavropol: Stavr. Kn. Izd., 1989. Eppinger, M., Rosovitz, M.J., Fricke, F.W., et al., The Complete Genome Sequence of Yersinia pseudotuberculosis IP31758, the Causative Agent of Far East Scarlet-Like Fever, PLoS Genet., 2007, vol. 3, no. 8, p. E142. Filippov, A.A., Transposable Genetic Elements of Pathogenic Yersinia. Probl. Osobo Opasnykh Infekts., 2000, no. 80, pp. 71–88.

554

SUNTSOV, SUNTSOVA

Goldschmidt, R., The Material Basis of Evolution, N. Haven; Connecticut: Yale Chiv., 1940, pp. 205–206. Gu, J., Neary, J.L., Sanchez, M., et al., Genome Evolution and Functional Divergence in Yersinia, J. Exp. Zool. (Part B.: Mol. Dev. Evol.), 2006, vol. 308, no. 1, pp. 37–49. Iordanskii, N.N., Evolyutsiya zhizni (Life Evolution), Moscow: Akademiya, 2001. Kolchinskii, E.I., Neokatastrofizm i selektsionizm: vechnaya dilemma ili vozmozhnost' sinteza? Istoriko-kriticheskie ocherki (Neocatastrophism and Selectionism: Everlasting Dilemma or Possibility of Synthesis? (Historical–Critical Studies)), St. Petersburg: Nauka, 2002. Konstantinidis, K.T., Ramette, A., and Tiedje, J.M., The Bacterial Species Definition in the Genomic Era, Phil. Trans. Royal Soc. Br., 2006, vol. 361, pp. 1929–1940. Koonin, E.V., Makarova, K.S., and Aravind, L., Horizontal Gene Transfer in Prokaryotes: Quantification and Classification, An. Rev. Microbiol., 2001, vol. 55, pp. 709–742. Kukleva, L.M., Protsenko, O.A., and Kutyrev, V.V., Modern Concepts of Relationship between the Causative Agents of Plague and Pseudotuberculosis, Mol. Genet. Mikrobiol. Virusol., 2002, no. 1, pp. 3–7. Kunin, V., Goldovsky, L., Darzentas, N., et al., The Net of Life: Reconstructing the Microbial Phylogenetic Network, Genome Res. published online, 2005. Kurland, C.G., Canback, B., and Berg, O.G., Horizontal Gene Transfer: A Critical View, Proc. Natl. Acad. Sci. USA, 2003, vol. 100, no. 17, pp. 9658–9662. Kurland, C.G., Something for Everyone: Horizontal Gene Transfer in Evolution, EMBO Rep., 2000, vol. 15, no. 1(2), pp. 92–95. Li, Y., Dai, E., Cui, Y., et al., Different Region Analysis for Genotyping Yersinia pestis Isolates from China, PLoS ONE, 2008, vol. 3, no. 5. P. E2166. Mayr, E., Populations, Species, and Evolution, Cambridge (Massachusetts): Harvard Univ., 1970. Motin, V.L., Georgescu, A.M., Elliott, J.M., et al., Genetic Variability of Yersinia pestis Isolates As Predicted by PCR-Based IS100 Genotyping and Analysis of Structural Genes Encoding Glycerol-3-Phosphate Dehydrogenase (GlpD), J. Bacteriol., 2002, vol. 184, pp. 1019–1027. Nazarov, V.I., Uchenie o makroevolyutsii. Na puti k novomu sintezu (A Teaching on Macroevolution: On the Way to New Synthesis), Moscow: Nauka, 1991. Pavlinov, I.Ya., Vvedenie v sovremennuyu filogenetiku (Introduction to Modern Phlogenetics), Moscow: KMK, 2005. Pavlovskii, E.N., Principles of the Teaching on Natural Nidality of Human Transmission Diseases, Zhur. Obshch. Biol., 1946, vol. 7, no. 1, pp. 3–33. Pourcel, C., Andre-Mazeaud, F., Neubauer, H., et al., Tandem Repeats Analysis for the High Resolution Phylogenetic Analysis of Yersinia pestis, 2004, http://www.biomedcentral.com/1471–2180/4/22. Prozorov, A.A., Horizontal Gene Transfer in Bacteria, Usp. Sovrem. Biol., 2000, vol. 120, no. 6, pp. 515–528. Shvarts, S.S., Ekologicheskie zakonomernosti evolyutsii (Ecological Consistent Patterns of Evolution), Moscow: Nauka, 1980. Skurnik, M., Peippo, A., and Ervela, E., Characterization of the O-Antigen Gene Cluster of Yersinia pseudotuberculosis

and the Cryptic O-Antigen Gene Cluster of Yersinia pestis Shows That the Plague Bacillus Is Most Closely Related to and Has Evolved from Y. pseudotuberculosis Serotype O:1b, Mol. Microbiol., 2000, vol. 37, no. 2, pp. 316–330. Song, Y., Tong, Z., Wang, J., et al., Complete Genome Sequence of Yersinia pestis Strain 91001, An Isolate Avirulent to Humans, DNA Research, 2004, vol. 11, no. 3, pp. 179–197. Suntsov, V.V., Suntsova, N.I., and Nguen Ai Phuong, Biocenotic Structure of Plague Foci in Vietnam. 1. Hosts and Vectors, in Sb. rabot k 10-letiyu Trop. tsentra. Kn. 1. Ch. II. Tropicheskaya meditsina (Collected Papers to the Tenth Anniversary of the Tropical Center, Book 1, part II. Tropical Medicine), Korzun, L.P., Krivolutskii, D.A., Naumov, A.V., and Novikov, G.G., Eds., Moscow: Tropcentr, 1997. pp. 455– 479. Suntsov, V.V. and Suntsova, N.I., Chuma. Proiskhozhdenie i evolyutsiya epizooticheskoi sistemy (ekologicheskie, geograficheskie i sotsial’nye aspekty) (Plague. The Origin and Evolution of Epizootic System (Ecological, Geographical, and Social Aspects)), Moscow: KMK, 2006. Suntsov, V.V. and Suntsova, N.I., Ecological Aspects of Evolution of the Plague Microbe Yersinia pestis and the Genesis of Natural Foci, Izv. Akad. Nauk, Ser. Biol., 2000, vol. 27, no. 6, pp. 645–657. Suntsov, V.V. and Suntsova, N.I., Concepts of Macro- and Microevolution as Related to the Problem of Origin and Global Expansion of the Plague Pathogen Yersinia pestis, Izv. Akad. Nauk, Ser. Biol., 2008, vol. 35, no. 4, pp. 645–657. Torrea, G., Chenal-Francisque, V., Leclercq, A., et al., Efficient Tracing of Global Isolates of Yersinia pestis by Restriction Fragment Length Polymorphism Analisis using Three Insertion Sequences as Probes, J. Clinical Microbiol., 2006, vol. 44, no. 6, pp. 2084–2092. Vergnaud, G., Li, Y., Gorge, O., et al., Analysis of the Three Yersinia pestis CRISPR Loci Provides New Tools for Phylogenetic Studies and Possibly for the Investigation of Ancient DNA, Adv. Exp. Med. Biol., 2007, vol. 603, pp. 327–338. Wren, B.W., The Yersinia—A Model Genus to Study the Rapid Evolution of Bacterial Pathogens, Nat. Rev. Microbiol., 2003, vol. 1, no. 1, pp. 55–64. Yablokov, A.V. and Yusufov, A.G., Evolyutsionnoe uchenie (Evolutionary Teaching), Moscow: Vysshaya Shkola, 2006. Zavarzin, G.A., Fenotipicheskaya sistematika bakterii. Prostranstvo logicheskikh vozmozhnostei (Phenotypic Bacterial Taxonomy. The Space of Logical Possibilities), Moscow: Nauka, 1974. Zhou, D. and Yang, R., Molecular Darwinian Evolution of Virulence in Yersinia pestis, Infect. Immun., 2009, http://iai.asm.org/cgi/content/abstract /IAI.01477-08.1. Zhou, D., Han, Y., Song, Y., et al., Comparative and Evolutionary Genomics of Yersinia pestis, Microbes Infect., 2004b, vol. 6, no. 13, pp. 1226–1234. Zhou, D., Han, Y., Song, Y., et al., DNA Microarray Analysis of Genome Dynamics in Yersinia pestis: Insights into Bacterial Genome Microevolution and Niche Adaptation, J. Bacteriol., 2004a, vol. 186, no. 15, pp. 5138–5146. Zhou, D., Tong, Z., Song, Y., et al., Genetics of Metabolic Variations between Yersinia pestis Biovars and the Proposal of a New Biovar, Microtus, J. Bacteriol., 2004c, vol. 186, no. 15, pp. 5147–5152. BIOLOGY BULLETIN

Vol. 36

No. 6

2009