**3. Conclusion**

It is usually assumed that a certain level of genetic diversity is necessary for the long-term prosperity of a species. Indeed, different genotypes confer different levels of resistance to various environmental stresses, and consequently, the greater the diversity of the genotypes in a population, the more effective its ability to withstand unfavorable conditions will be. Therefore, the existence of a low level of genetic diversity is often considered to represent a crucial stage for the survival of a species or even a sign of its extinction. However, despite several attempts to determine the average levels of genetic variation in different categories of plants (e.g., Gitzendanner & Soltis, 2000; Nybom, 2004), it is still unknown what level of polymorphism should be considered critical for the existence of a certain species. Thus, some rare endemic species exhibit higher levels of genetic diversity than the average values found for this category of plants, such as *Oxytropis chankaensis* (Table). At the same time, very low levels, or even an absence of genetic variability has been found in other narrowly endemic plants (e.g., *Bensoniella oregona*, Soltis et al., 1992). It is impossible to predict the fate of a species on the basis of its genetic diversity alone. Here, we have attempted to address some species existing under extreme conditions in the context of a variety of environmental, biological, evolutionary and other influences.

All of the species described above are represented by small, fragmented, marginal populations. Each of these species is characterized by a particular level of genetic diversity, ranging from very low (*Panax ginseng*) to high (*Oxytropis chankaensis*). Despite these differences, all of these plants exhibit weak competitiveness, and none of them can be considered prosperous. These species are not dominant in their respective plant communities, and they inhabit specific (often quite narrow) ecological niches where their existence is maintained more or less successfully for a long period. Without the effects of human activity, these species could probably exist in this state indefinitely. What are the mechanisms that ensure the long-term existence of these species in small, isolated populations at the limit of their climatic and environmental tolerance?

term persistence. In contrast, the populations of *I. vorobievii* and *I. mandshurica* contain 13 and 6 haplotypes, respectively, which may result from historical gene flow, retention of ancestral polymorphisms that accumulated over a long period in more continuous ancient populations, or a putative origin from several founders. Based on cpDNA haplotypes, demographic event analyses show that populations of both species have undergone

Apparently, the main reason for the rarity of *I. mandshurica* and especially of *I. vorobievii* is the scarcity of suitable habitats for these psammirises in Primorye. As *I. vorobievii* and *I. mandshurica* represent components of steppe vegetation and grow in specific edaphic conditions, they are members of several steppe communities that are likely remnants of previously more widespread steppe vegetation (Krestov & Verkholat, 2003). The contractions of such relic communities result from climate and natural community changes (natural succession) and, in recent years, from anthropogenic habitat destruction. Their isolation from the main part of the species' ranges, limited seed dispersal and poor vegetative reproduction make these psammirises particularly vulnerable and may lead the

It is usually assumed that a certain level of genetic diversity is necessary for the long-term prosperity of a species. Indeed, different genotypes confer different levels of resistance to various environmental stresses, and consequently, the greater the diversity of the genotypes in a population, the more effective its ability to withstand unfavorable conditions will be. Therefore, the existence of a low level of genetic diversity is often considered to represent a crucial stage for the survival of a species or even a sign of its extinction. However, despite several attempts to determine the average levels of genetic variation in different categories of plants (e.g., Gitzendanner & Soltis, 2000; Nybom, 2004), it is still unknown what level of polymorphism should be considered critical for the existence of a certain species. Thus, some rare endemic species exhibit higher levels of genetic diversity than the average values found for this category of plants, such as *Oxytropis chankaensis* (Table). At the same time, very low levels, or even an absence of genetic variability has been found in other narrowly endemic plants (e.g., *Bensoniella oregona*, Soltis et al., 1992). It is impossible to predict the fate of a species on the basis of its genetic diversity alone. Here, we have attempted to address some species existing under extreme conditions in the context of a variety of environmental,

All of the species described above are represented by small, fragmented, marginal populations. Each of these species is characterized by a particular level of genetic diversity, ranging from very low (*Panax ginseng*) to high (*Oxytropis chankaensis*). Despite these differences, all of these plants exhibit weak competitiveness, and none of them can be considered prosperous. These species are not dominant in their respective plant communities, and they inhabit specific (often quite narrow) ecological niches where their existence is maintained more or less successfully for a long period. Without the effects of human activity, these species could probably exist in this state indefinitely. What are the mechanisms that ensure the long-term existence of these species in small, isolated

populations at the limit of their climatic and environmental tolerance?

bottleneck events and expansion in the past (Kozyrenko et al., 2009).

species to extinction.

biological, evolutionary and other influences.

**3. Conclusion** 

For ginseng, longevity appears to be most important factor for its survival. Indeed, a lifetime of up to several hundred years is unusual for an herbaceous plant that is incapable of vegetative reproduction. Ginseng maintains the ability to produce seeds throughout its life span, and it appears that as a result of apomixes, its seed production is not particularly dependent on environmental conditions or the availability of pollinators. A large number of fully viable seeds and an extended period of embryo maturation allow revival of populations of this species, even from a small number of individuals over the course of many years.

Similar to ginseng, *Aristolochia manshuriensis* only exhibits seed-based reproduction. The life span of this species is not as long as that of other woody plants and is near the average for woody vines. This species has a very poor ability to reproduce vegetatively, and there are major limitations on its seed reproduction as a result of adaptation to pollination only by certain insects. Though adaptation to specific pollinators prevents inbreeding, pollination decreases if pollinators are absent, and the resulting fruit development is low. In this case, high seed production (a large number of seeds per one fertilization event) and adaptability to seed transfer by wind and water seems to be of primary importance for the survival of the species. Even a single successful fertilization every several years could guarantee population restoration if conditions are suitable for seed germination. Under unfavorable conditions, plantlets of this species can exist in a juvenile state for a long time, which allows a population to survive until the re-establishment of suitable conditions.

The ability for vegetative propagation is a pathway for the survival of some species (*Oplopanax elatus*, irises and *Microbiota decussata*). This pathway also allows for the rehabilitation of a species, even after a significant reduction in its population, and it effectively allows clonal colonies to reoccupy their habitats, where suitable conditions for the species are associated with an absence of competitors. The flexibility of the reproductive system of *O. elatus*, combined with its different modes of reproduction allows it to renew heterozygous genotypes by clonal growth and to contribute additional variability resources through sporadic seed reproduction. At the same time, some features of the biology of this species (the long life of a single clone, overlapping generations and the ability to crosspollinate) also help to maintain a certain level of polymorphism.

For *I. mandshurica* and *I. vorobievii,* vegetative reproduction (even if poor) seems to be the only way to survive under unfavorable conditions. Rare reproduction through seeds allows for the maintenance of a certain level of genetic diversity in its populations. However, the spread of both species beyond the borders of their existing populations is unlikely as a result of the scarcity of suitable habitats. Poor vegetative reproduction and limited seed dispersal as well as isolation from the main part of the species range (*I. mandshurica)* or its occurrence in a single locality (*I. vorobievii)* make populations of both species vulnerable. In the case of *I. vorobievii*, this vulnerability may lead to rapid species extinction.

The pattern of genetic diversity and the structure of populations in the endemic species *M. decussata* are congruent with the leading edge model of colonization. It could be proposed that extant southern populations represent the putative species range center. Populations that expanded southward during dry and cool periods at the Oligocene/Miocene boundary have become completely extirpated following climate changes in the Quaternary. The distribution area of *M. decussata* became fragmented quite some time ago through the displacement of the species toward mountain peaks and the extinction of stands in the adjoining territories. The remnant *M. decussata* populations have the potential for survival under ongoing climate changes and global warming because of this species' physiological and ecological range of tolerance, reproduction by layering and other life history traits.

In the case of endemic or rare species, one must distinguish between relics left by the extinction of related populations and newly evolved taxa. All relics that survived the repeated periods of Pleistocene climate cooling have apparently experienced a severe genetic bottleneck, not only as a result of genetic drift associated with the reduction of populations, but also because of selection acting in a rapidly changing climate. Because of this selection, the fittest individuals have survived. Among the representatives of the ancient tropical floras (*P. ginseng, O. elatus, A. manshuriensis*) only a small number of genotypes are likely to have possessed such fitness. By acquiring a mechanism for survival in harsh environments, these species have lost much of their genetic diversity.

In the case of the narrowly endemic species *O. chankaensis*, the situation is different. This species possesses adaptive mechanisms that enable it not only to successfully renew its populations in the coastal zone, which are exposed to frequent flooding and other adverse factors, but also to maintain the high level of recombination responsible for the survival of the species in a changing environment. This is a relatively young species, and its biological characteristics may promote its prosperity and wide distribution; the only obstacle to this is its high habitat specificity; it only inhabits the sandy shore of a large lake where there is intense insolation and high air humidity. However, there are no such habitats nearby, and the small number of plants in some populations makes this species vulnerable.

The patterns observed for various rare species often do not fully correspond to the general idea of survival at the edge of their range. Plant species exhibit tremendous variation in life history traits that may help them survive in harsh or changeable environments. The cause of a plant's rarity depends on the effects of different historical, biological and genetic factors. In all cases, different compensatory mechanisms, such as increased longevity and fertility, the formation of soil seed banks and vegetative reproduction, are involved. The adaptations of these species are not always successful because the historically established balance between reproduction and dispersal can be disturbed. However, in the absence of destructive human activities, many rare species could exist for an indefinite time.

### **4. Acknowledgements**

We are grateful to Dr. E.V. Sundukova and Dr. V.N. Makarkin for help with the manuscript preparation. This work was supported by the Grant "Molecular and Cell Biology" of the Russian Academy of Sciences (No 09-I-P22-03), by the Grant "Biological Diversity" of the Russian Academy of Sciences (No 09-I-P23-06), by the Grant "Biological Resources of Russia: Estimation and Fundamental Basis for Monitoring" (No 09-I-ОBN-02), by the Grant No 11- III-В-06-094 of FEBRAS and by Grant "Leading Schools of Thought" from the President of Russian Federation.

#### **5. References**

Adams, C.A., Baskin, J.M. & Baskin, C.C. (2005). Trait Stasis Versus Adaptation in Disjunct Relict Species: Evolutionary Changes in Seed Dormancy–Breaking and

adjoining territories. The remnant *M. decussata* populations have the potential for survival under ongoing climate changes and global warming because of this species' physiological and ecological range of tolerance, reproduction by layering and other life history traits.

In the case of endemic or rare species, one must distinguish between relics left by the extinction of related populations and newly evolved taxa. All relics that survived the repeated periods of Pleistocene climate cooling have apparently experienced a severe genetic bottleneck, not only as a result of genetic drift associated with the reduction of populations, but also because of selection acting in a rapidly changing climate. Because of this selection, the fittest individuals have survived. Among the representatives of the ancient tropical floras (*P. ginseng, O. elatus, A. manshuriensis*) only a small number of genotypes are likely to have possessed such fitness. By acquiring a mechanism for survival in harsh

In the case of the narrowly endemic species *O. chankaensis*, the situation is different. This species possesses adaptive mechanisms that enable it not only to successfully renew its populations in the coastal zone, which are exposed to frequent flooding and other adverse factors, but also to maintain the high level of recombination responsible for the survival of the species in a changing environment. This is a relatively young species, and its biological characteristics may promote its prosperity and wide distribution; the only obstacle to this is its high habitat specificity; it only inhabits the sandy shore of a large lake where there is intense insolation and high air humidity. However, there are no such habitats nearby, and

The patterns observed for various rare species often do not fully correspond to the general idea of survival at the edge of their range. Plant species exhibit tremendous variation in life history traits that may help them survive in harsh or changeable environments. The cause of a plant's rarity depends on the effects of different historical, biological and genetic factors. In all cases, different compensatory mechanisms, such as increased longevity and fertility, the formation of soil seed banks and vegetative reproduction, are involved. The adaptations of these species are not always successful because the historically established balance between reproduction and dispersal can be disturbed. However, in the absence of destructive human

We are grateful to Dr. E.V. Sundukova and Dr. V.N. Makarkin for help with the manuscript preparation. This work was supported by the Grant "Molecular and Cell Biology" of the Russian Academy of Sciences (No 09-I-P22-03), by the Grant "Biological Diversity" of the Russian Academy of Sciences (No 09-I-P23-06), by the Grant "Biological Resources of Russia: Estimation and Fundamental Basis for Monitoring" (No 09-I-ОBN-02), by the Grant No 11- III-В-06-094 of FEBRAS and by Grant "Leading Schools of Thought" from the President of

Adams, C.A., Baskin, J.M. & Baskin, C.C. (2005). Trait Stasis Versus Adaptation in Disjunct

Relict Species: Evolutionary Changes in Seed Dormancy–Breaking and

environments, these species have lost much of their genetic diversity.

the small number of plants in some populations makes this species vulnerable.

activities, many rare species could exist for an indefinite time.

**4. Acknowledgements** 

Russian Federation.

**5. References** 

Germination Requirements in a Subclade of *Aristolochia* Subgenus *Siphisia*  (Piperales). *Seed Sci. Res.*, Vol.15, No.2, (June 2005), pp. 161–173, ISSN 0960-2585


Bondarenko, O.V. (2006). Fossil Woods from the Pliocene of Southern Primorye. *PhD Thesis*,

Bulgakov, V.P. & Zhuravlev, Yu.N. (1989). Generation of *Aristolochia manshuriensis* Kom.

Cornman, R.S. & Arnold, M.L. (2007). Phylogeography of *Iris missouriensis* (Iridaceae) Based

Cruzan, M.B., Arnold, M.L., Carney, S.E. & Wollenberg, K.R. (1993). cpDNA Inheritance in

Ellstrand, N.C. & Roose, M.L. (1987). Patterns of Genotypic Diversity in Clonal Plant Species. *Am. J. Bot.*, Vol.74, No.1, (January 1987), pp. 123–131, ISSN 0002-9122 Figueroa-Esquivel, E.M., Puebla-Olivares, F., Eguiarte, L.E. & Núñez-Farfán J. (2010).

Gadek, P.A., Alpers, D.L., Heslewood, M.M. & Quinn, C.J. (2000). Relationships Within

Gitzendanner, M.A. & Soltis, P.S. (2000). Patterns of Genetic Variation in Rare and

Hampe, A. & Petit, R.J. (2005). Conserving Biodiversity under Climate Change: the Rear Edge Matters. *Ecol. Lett.*, Vol.8, No.5, (May 2005), pp. 461–467, ISSN 1461-0248 Hao, B., Li, W., Linchun, M., Li, Y., Rui, Z., Mingxia, T. & Weikai, B. (2006). A Study of

Hewitt, G.M. (2004). Genetic Consequences of Climatic Oscillations in the Quaternary.

Huang, S., Kelly, L.M. & Gilbert, M.G. (2003). *Aristolochia* Linnaeus., In: *Flora of China* 

Huh, M.K., Jung, S.D., Moon, H.K., Kim, S.-H. & Sung J.S. (2005). Comparison of Genetic

Hwang, S.-Y., Lin, H.W., Kuo, Y.S. & Lin, T.P. (2001). RAPD Variation in Relation to

(Eds.), Vol.5, , pp. 258–269, Available from http://www.eoras.org

No.2, (March 2005), pp. 69–74, ISSN 1225-9306

*Am. J. Bot.,* Vol.87, No.7, (July 2000), pp. 1044–1057, ISSN 0002-9122

Grushwitsky, I.V. (1961). *Ginseng: the Aspects of Biology*, Nauka, Leningrad, Russia

Vol.80, No.3, (March 1993), pp. 344–350, ISSN 0002-9122

(November 2010), pp. 789–800, ISSN 1870-3453

Sciences, Vladivostok, Russia

pp. 4585–4598, ISSN 0962-1083

ISSN 0033-9946

ISSN 0002-9122

ISSN 0006-2928

406X

195, ISSN 1471-2970

Institute of Biology and Soil Science, Far Eastern Branch of the Russian Academy of

Callus Tissue Cultures. *Rastitel'nye Resursy*, Vol.25, No.2, (May 1989), pp. 266–270,

on Nuclear and Chloroplast Markers. *Mol. Ecol.*, Vol.16, No.21, (November 2007),

Interspecific Crosses and Evolutionary Inference in Louisiana Irises. *Am. J. Bot.*,

Genetic Sructure of a Bird-Dispersed Tropical Tree (*Dendropanax arboreus*) in a Fragmented Landscape in Mexico. *Revista Mexicana de Biodiversidad,* Vol.81, No.3,

Cupressaceae Sensu Lato: a Combined Morphological and Molecular Approach.

Widespread Plant Cogeners. *Am. J. Bot.*, Vol.87, No.6, (June 2000), pp. 783–792,

Conservation Genetics in *Cupressus* c*hengiana*, an Endangered Endemic of China, Using ISSR Markers. *Biochem. Genet.*, Vol.44, No.1-2, (February 2006), pp. 31–45,

*Philos. Trans. R. Soc. Lond. B. Biol. Sci.,* Vol. 359, No.1442, (February 2004), pp. 183–

*(*Ulmaceae through Basellaceae), 19.12.2003, Z.-Y. Wu, P.H. Raven & D.Y. Hong,

Diversity and Population Structure of *Kalopanax pictus* (Araliaceae) and its Thornless Variant Using RAPD. *Korean Journal of Medicinal Crop Science*, Vol.13,

Population Differentiation of *Chamaecyparis formosensis* and *Chamaecyparis taiwanensis*. *Bot. Bull. Acad. Sin.,* Vol.42, No.3, (July 2001), pp. 173–179, ISSN 1817-


(Iridaceae): Evidence from the Nuclear and Chloroplast Genomes. *Russ. J. Genet.,*  Vol.45, No.11, (November 2009), pp. 1394–1402, ISSN 1022-7954


Krestov, P.V. & Verkholat, V.P. (2003). *Rare Plant Communities of Amur Region.* Institute of

Little, D.P., Schwarzbach, A.E., Adams, R.P. & Hsieh, C.-F. (2004). The Circumscription and

Malyshev, L.I. (2007). Phenetics in the Section Verticillares of the Genus *Oxytropis* DC. (Fabaceae). *Bot. Zhurn.*, Vol.92, No.6, (June 2007), pp. 793–807, ISSN 0006-8136 Malyshev, L.I. (2008). Diversity of the genus *Oxytropis* in Asian Russia. *Turczaninowia*,

Melnikova, A.B. & Machinov, A.N. (2004). On the Record of *Microbiota decussata*

Nakonechnaya, O.V., Koren, O.G., Nesterova, S.V., Sidorenko, V.S., Kholina, A.B., Batygina,

*Resursy*, Vol.41, No.3, (August-September 2008), pp. 14–25, ISSN 0033-9946 Nakonechnaya, O.V., Koren, O.G. & Zhuravlev, Yu.N. (2007). Allozyme Variation of the

Nakonechnaya, O.V., Sidorenko, V.S., Koren, O.G., Nesterova, S.V. & Zhuravlev, Yu.N.

Nybom, H. (2004). Comparison of Different Nuclear DNA Markers for Estimating

Pavlova, N.S. (1987). Family Iridaceae, In: *The vascular plants of the Soviet Far East,* Vol.2, S.S.

Pavlova, N.S. (1989). Family Fabaceae. In: *The vascular plants of the Soviet Far East,* Vol.4, S.S. Kharkevich, (Ed.), pp. 191–339, Nauka, ISBN 5-02-026577-2, Leningrad, Russia Pavlova, N.S. (2006). Family Iridaceae. *Iris* L., In: *Flora of the Russian Far East, Additions and* 

Pavlyutkin, B.I., Petrenko, T.I. & Chekryzhov, I.Y. (2005). The Problems of Stratigraphy of

*Geologiya*, Vol.24, No.6, (November 2005), pp. 59–76, ISSN 0207-4028 Petit, R.J., Duminil, J., Fineschi, S., Hampe, A., Salvini, D. & Vendramin, G.G. (2005).

Vol.45, No.11, (November 2009), pp. 1394–1402, ISSN 1022-7954

Biology and Soil Sciences, ISSN 5744213406, Vladivostok*,* Russia

Kurentsova, G.E. (1968). *Relic Plants of Primorye*, Nauka, Leningrad, Russia

Vol.11, No.3, (December 2008), pp. 5–141, ISSN 1560-7259

Vol.43, No.2, (February 2007), pp. 156–164, ISSN 1022-7954

*Bull.*, Vol.36, No.4, (August 2009), pp. 393–396, ISSN 1062-3590

Kharkevich, (Ed.), pp. 414–426, Nauka, Leningrad, Russia

1872–1881, ISSN 0002-9122

1143–1155, ISSN 0962-1083

1083

2004), pp. 1470–14720, ISSN 0006-8136

(Iridaceae): Evidence from the Nuclear and Chloroplast Genomes. *Russ. J. Genet.,* 

Phylogenetic Relationships of *Callitropsis* and the Newly Described Genus *Xanthocyparis* (Cupressaceae). *Am. J. Bot.*, Vol.91, No.11, (November 2004), pp.

(Cupressaceae) at Unusually Low Altitude. *Bot. Zhurn.*, Vol.89, No.9, (September

T.B. & Zhuravlev, Yu.N. (2005). Elements of Reproductive Biology of *Aristolochia manshuriensis* Kom. (Aristolochiaceae) in the Conditions of Introduction. *Rastitel'nye* 

Relict Plant *Aristolochia manshuriensis* Kom. (Aristolochiaseae). *Russ. J. Genet*.,

(2008). Specific features of pollination in the Manchurian birthwort, *Aristolochia manshuriensis. Biol. Bull.* Vol.35, No.5, (October 2008), pp. 459–465, ISSN 1062-3590 Nechaev, V.A. & Nakonechnaya, O.V. (2009). Structure of Fruits and Seeds and Ways of

Dissemination of Two Species of the Genus *Aristolochia* L. in Primorsky Krai. *Biol.* 

Intraspecic Genetic Diversity in Plants. *Mol. Ecol.,* Vol.13, No.5, (May 2004), pp.

*Modications to "Vascular Plants of the Soviet Far East",* A.E. Kozhevnikov, N.S. Probatova, (Eds.), pp. 277–279, Dal'nauka, ISBN 5-8044-0534-9, Vladivostok, Russia

the Tertiary Deposits of the Pavlovka Coal-eld (Primorye). *Tikhookeanskaya* 

Comparative Organization of Chloroplast, Mitochondrial and Nuclear Diversity in Plant Populations. *Mol. Ecol.,* Vol.14, No.3, (March 2005), pp. 689–701, ISSN 0962-

