Skip to main content

Advertisement

SpringerLink
Log in

Spatial patterns and intraspecific diversity of the glacial relict legume species Vavilovia formosa (Stev.) Fed. in Eurasia

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

Vavilovia formosa is one of five genera in tribe Fabeae, (Fabaceae, Leguminosae) with close phylogenetic relationships to Pisum. It grows in subalpine and alpine levels in Armenia, Azerbaijan, Georgia, Iran, Iraq, Lebanon, Russia and Turkey and is recognized as an endangered and protected plant. This study was conducted to reveal its intraspecific variability, as well as to predict the past, extant and future species distribution range. We analysed 51 accessions with common phylogenetic markers (trnF-trnL, trnS-trnG, matK, rbcL, psbA-trnH and ITS). These represent in total up to 2551 bp of chloroplast and 664 bp of nuclear sequences per sample. Two populations from Turkey and Armenia were analysed for genetic diversity by AFLP. Leaf morphometry was conducted on 1457 leaflets from 43 specimens. Extracted bioclimatic parameters were used for niche-modelling approach. Analysis of cpDNA revealed two haplotypes, 12 samples from Armenia, Daghestan, Nakhichevan and Iran belonged to H1 group, while 39 samples of all Turkish and part of Armenian were in H2 group. The mean intrapopulation diversity based on AFLP was low (H E = 0.088) indicating limited outcrossing rate. A significantly positive correlation between geographical latitude and leaf area (\(\rho\) = 0.527, p < 0.05) was found. Niche modelling has shown temporal variation of predicted occurrence across the projected time periods. Vavilovia formosa has suffered a range reduction following climate warming after last glacial maximum, which classify this species as cold-adapted among the Fabeae species as well as a glacial relict.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Molec Ecol 17:5177–5188. doi:10.1111/j.1365-294X.2008.03971

    Article  Google Scholar 

  • Akopian J, Sarukhanyan N, Gabrielyan I, Vanyan A, Mikić A, Smýkal P, Kenicer G, Vishnyakova M, Sinjushin A, Demidenko N, Ambrose M (2010) Reports on establishing an ex situ site for ‘beautiful’ Vavilovia (Vavilovia formosa) in Armenia. Genet Resources Crop Evol 57:1127–1134. doi:10.1007/s10722-010-9606-0

    Article  Google Scholar 

  • Akopian JA, Gabrielyan IG (2008) On high-mountain pea Vavilovia formosa (Stev.) Fed. (Fabaceae) in Armenia. Crop Wild Relatives Newslett 6:26–27.

    Google Scholar 

  • Alefeld F (1861) Pisum formosum. Bonplandia 9:327

    Google Scholar 

  • Alsos IG, Alm T, Normand S, Brochmann C (2009) Past and future range shifts and loss of diversity in dwarf willow (Salix herbacea L.) inferred from genetics, fossils and modelling. Glob Ecol Biogeogr 18:223–239. doi:10.1111/j.1466-8238.2008.00439.x

    Article  Google Scholar 

  • Alsos IG, Ehrich D, Thuiller W et al (2012) Genetic consequences of climate change for northern plants. Proc Roy Soc Biol Sci Ser B 279:2042–2051. doi:10.1098/rspb.2011.2363

    Article  Google Scholar 

  • Atalay I (1996) Palaeosoils as indicators of the climatic changes during Quaternary period in S. Anatolia. J Arid Environ 32:23–35

    Article  Google Scholar 

  • Baloyan SA (2004) List of the species of alpine flora of the Central Armenian volcanic highland. Takhtajania, 15:97–107

  • Boissier E (1856) Diagnoses Plantarum Orientalium novarum, ser. 2, vol. 5. B. Herrmann, Lipsiae

  • Boissier E (1872) Flora Orientalis, vol. 2. H. Georg, Genevae, Basileae

  • Bonin A, Bellemain E, Eidesen PB, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Molec Ecol 13:3261–3273. doi:10.1111/j.1365-294X.2004.02346.x

    Article  CAS  Google Scholar 

  • Bosque M, Adamogianni MI, Bariotakis M, Fazan L, Stoffel M, Garfi G, Gratzfeld J, Kozlowski G, Pirintsos S (2014) Fine-scale spatial patterns of the Tertiary relict Zelkova abelicea (Ulmaceae) indicate possible processes contributing to its persistence to climate changes. Regional Environm Change 14:835–849. doi:10.1007/s10113-013-0544-1

    Article  Google Scholar 

  • Bystriakova N, Ansell SW, Russell SJ, Grundmann M, Vogel JC, Schneider H (2014) Present, past and future of the European rock fern Asplenium fontanum: combining distribution modelling and population genetics to study the effect of climate change on geographic range and genetic diversity. Ann Bot (Oxford) 113:453–465. doi:10.1093/aob/mct274

    Article  Google Scholar 

  • Çiplak B (2003) Distribution of Tettigoniinae (Orthoptera, Tettigoniidae) bush-crickerts in Turkey: the importance of the Anatolian Taurus Mountains in biodiversity and implications for conservation. Biodivers Conserv 12:47–64

    Article  Google Scholar 

  • Daubenmire RF (1943) Vegetational zonation in the Rocky Mountains. Bot Rev 9:325–393. doi:10.1007/BF02872481

    Article  Google Scholar 

  • Davis PH (1970a) Lathyrus. In: Davis PH (ed) Flora of Turkey, 3rd edn. Edinburgh University Press, Edinburgh, vol. 3, pp 328–369

    Google Scholar 

  • Davis PH (1970b) Vavilovia A. Fed. In: Davis PH (ed) Flora of Turkey and East Aegean Islands, vol 3. Edinburg University Press, UK, pp. 44–45

  • Davis PH (1970c) Pisum L. In: Davis PH (ed) Flora of Turkey and East Aegean Islands. Vol 3. University Press, Edinburg, pp 370–373

  • Deniz UG, Sümbül H (2004) Flora of the Elmali Cedar Research Forest (Antalya/Turkey). Turk J Bot 28:529–555

    Google Scholar 

  • Dolukhanov A (1989) Rastitel’nost’ Gruzii (Vegetation of Georgia). v. 1. Metsniereba, Tbilisi (in Russian)

  • Earl DA, von Holdt BM (2012) Structure Harvester: a website and program for visualizing Structure output and implementing the Evanno method. Conservation Genet Resources 4:359–361. doi:10.1007/s12686-011-9548-7

    Article  Google Scholar 

  • Ehrich D (2006) AFLPdat: a collection of R functions for convenient handling of AFLP data. Molec Ecol Notes 6:603–604. doi:10.1111/j.1471-8286.2006.01380.x

    Article  Google Scholar 

  • Ekim T, Güner A (1986) The Anatolian Diagonal: fact or fiction? Proceedings of the Royal Society of Edinburgh 89B:69–77

  • Eliášová A, Trávníček P, Mandák B, Münzbergová Z (2014) Autotetraploids of Vicia cracca show a higher allelic richness in natural populations and a higher seed set after artificial selfing than diploids. Ann Bot (Oxford) 113:159–170. doi:10.1093/aob/mct252

    Article  Google Scholar 

  • Endo Y, Choi BH, Ohashi H, Delgado-Salinas A (2008) Phylogenetic relationships of New World Vicia (Leguminosae) inferred from nrDNA internal transcribed spacer sequences and floral characters. Syst Bot 33:356–363

    Article  Google Scholar 

  • Eren Ö, Gökçeolu M, Parolly G (2004) The flora and vegetation of Bakirli Dagi (Western Taurus Mts, Turkey), including annotations on critical taxa of the Taurus range. Willdenowia 34:463–502

    Article  Google Scholar 

  • Erinç S (1978) Changes in the physical environment in Turkey since the end of the last glacial. In: Brice WC (ed) The environmental history of the Near and Middle East since the last Ice Age. Academic Press, London, p 87–110

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Molec Ecol 14:2611–2620. doi:10.1111/j.1365-294X.2005.02553.x

    Article  CAS  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molec Ecol Resources 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x

    Article  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molec Ecol Notes 7:574–578. doi:10.1111/j.1471-8286.2007.01758.x

    Article  CAS  Google Scholar 

  • Fedorov AA (1939) Wild high-mountain peas of Caucasus. Trans Biol Inst 1:39–79 (in Russian)

    Google Scholar 

  • Fedorov AA (1952) Supplement. In: Grossheim AA (ed) Flora of the Caucasus 5. Academy of Science of the USSR, Petersburg, p 453 (in Russian)

  • Franks SJ, Weber JJ, Aitken SN (2014) Evolutionary and plastic responses to climate change in terrestrial plant populations. Evol Appl 7:123–139. doi:10.1111/eva.12112

    Article  PubMed  Google Scholar 

  • Govorov LI (1937) Pisum. In: Vavilov NI, Wulff EV (eds) Flora of cultivated plants IV: grain leguminosae. State Agricultural Publishing Company, Moscow, pp 231–336

    Google Scholar 

  • Grichuk VP (1984) Late Pleistocene vegetation history. In: Velichko AA, Wright HE, Barnosky CW (eds) Late Quaternary Environments of the Soviet Union. University of Minessota Press. Mineapolis, pp 155–178

  • Grossheim AA (1949) Identification of plants of the Caucasus. Sovetskaya Nauka, Moscow (in Russian)

  • Guisan A, Broennimann O, Engler R, Vust M, Yoccoz NG, Lehmann A, Zimmermann NE (2006) Using niche-based models to improve the sampling of rare species. Conservation Biol 20:501–511. doi:10.1111/j.1523-1739.2006.00354.x

    Article  Google Scholar 

  • Gunn C, Kluve RJ (1976) Androecium and pistil characters for the tribe Vicieae (Fabaceae). Taxon 25:563–575

    Article  Google Scholar 

  • Hampe A, Jump AS (2011) Climate relicts: past, present, future. Annual Rev Ecol Evol Syst 42:313–333. doi:10.1146/annurev-ecolsys-102710-145015

    Article  Google Scholar 

  • Härstedt E (1950) Über die Vererbung der Form von Laub- und Kelchblättern von Pisum sativum. Agric Hort Genet 8:7–32

    Google Scholar 

  • Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112. doi:10.1111/j.1095-8312.1999.tb01160.x

    Article  Google Scholar 

  • Hofer J, Turner L, Hellens R, Ambrose M, Matthews P, Michael A, Ellis N (1997) UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr Biol 7:581–587. doi:10.1016/S0960-9822(06)00257-0

    Article  CAS  PubMed  Google Scholar 

  • Hu JM (2000) Phylogenetic relationships of the tribe Millettieae and allies—the current status. In: Herendeen PS, Bruneau A (eds) Advances in legume systematics. Royal Botanic Garden, Kew, UK, p 299–310

  • Jing R, Ambrose MA, Knox MR, Smykal P, Hybl M, Ramos Á, Caminero C, Burstin J, Duc G, van Soest LJM, Swiecicki WK, Pereira G, Vishnyakova M, Davenport G, Flavell AJ, Ellis THN (2012) Genetic diversity in European pisum germplasm collections. Theor Appl Genet 125:367–380. doi:10.1007/s00122-012-1839-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jing R, Vershinin A, Grzebyta J, Shaw P, Smýkal P, Marshall D, Ambrose MJ, Ellis THN, Flavell AJ (2010) The genetic diversity and evolution of field pea (Pisum) studied by high throughput retrotransposon based insertion polymorphism (RBIP) marker analysis. BMC Evol Biol 10:44. doi:10.1186/1471-2148-10-44

    Article  PubMed  PubMed Central  Google Scholar 

  • Joannin S, Cornee J, Munch P et al (2010) Early Pleistocene climate cycles in continental deposits of the Lesser Caucasus of Armenia inferred from palynology, magnetostratigraphy, and 40Ar/39Ar dating. Earth Planet Sci Lett 291:149–158. doi:10.1016/j.epsl.2010.01.007

    Article  CAS  Google Scholar 

  • Kato H, Oginuma K, Gu Z, Hammel B, Tobe H (1998) Phylogenetic relationships of Betulaceae based of matK sequences with particular reference to the position of Ostryopsis. Acta Phytotax. Geobot 49:89–97

    Google Scholar 

  • Kenicer G, Smýkal P, Vishnyakova M, Mikič A (2009) Vavilovia formosa, an intriguing Pisum relative. Grain Legum 51:8–12

    Google Scholar 

  • Kenicer GJ, Kajita T, Pennington RT, Murata J (2005) Systematics and biogeography of Lathyrus (Leguminosae) based on internal transcribed spacer and cpDNA sequence data. Amer J Bot 92:1199–1209. doi:10.3732/ajb.92.7.1199

    Article  CAS  Google Scholar 

  • Kitner M, Lebeda A, Doležalová I, Maras M, Křístková E, Nevo E, Pavlíček T, Meglič V, Beharav A (2008) AFLP analysis of Lactuca saligna germplasm collections from four European and three Middle East countries. Israel J Pl Sci 56:185–193

    Article  CAS  Google Scholar 

  • Kupicha FK (1981) Vicieae (Adans.) DC. (1825) nom conserv prop. In: Polhill RM, Raven PH (eds) Advances in legume systematics. Royal Botanical Garden, Kew

    Google Scholar 

  • Kupicha FK (1983) The infrageneric structure of Lathyrus. Notes Roy Bot Gard Edinburgh 41:209–244

    Google Scholar 

  • Lavin M, Alfonso Delgado SA (1990) Pollen brush of Papilionoideae (Leguminosae): morphological variation and systematic utility. Amer J Botany 10:1294–1312

    Article  Google Scholar 

  • Lehman CO, Blixt S (1984) Artificial intraspecific classification in relation to phenotypic manifestation of certain genes in Pisum. Agric Hort Genet 42:49–74

    Google Scholar 

  • Lock M, Maxted N (2005) Tribe Fabeae. In: Lewis G, Schrire B, Mackinder B, Lock M (eds) Legumes of the World. Royal Botanic Gardens, Kew

    Google Scholar 

  • Loridon K, McPhee KE, Morin J et al (2005) Microsatellite marker polymorphism and mapping in pea (Pisum sativum L.). Theor Appl Genet 111:1022–1031. doi:10.1007/s00122-005-0014-3

    Article  CAS  PubMed  Google Scholar 

  • Lynch M, Milligan BG (1994) Analysis of population genetic structure with RAPD markers. Molec Ecol 3:91–99. doi:10.1111/j.1365-294X.1994.tb00109.x

    Article  CAS  Google Scholar 

  • Makasheva RK (1983) Gorokh (pea). Kolos, Leningrad (in Russian)

  • Makasheva RK, Drozd AM, Adamova OP, Golubev AA (1973) Perennial pea. Bull Appl Bot Genet Pl Breed 51:44–56 (in Russian)

    Google Scholar 

  • Maxted N, Ambrose M (2001) Peas (Pisum L.). In: Maxted N, Bennett SJ (eds) Plant genetic resources of legumes in the Mediterranean. Kluwer, Dordrecht, pp 181–190

    Chapter  Google Scholar 

  • Médail F, Diadema K (2009) Glacial refugia influence plant diversity patterns in the Mediterranean Basin. J Biogeogr 36:1333–1345. doi:10.1111/j.1365-2699.2008.02051.x

    Article  Google Scholar 

  • Mikič A, Smýkal P, Kenicer G, Vishnyakova M, Sarukhanyan N, Akopian J, Vanyan A, Gabrielyan I, Smýkalová I, Sherbakova E, Zorić L, Atlagić J, Zeremski-Škorić T, Cupina B, Krstić Ð, Jajić I, Antanasović S, Ðorđević V, Mihailović V, Ivanov A, Ochatt S, Ambrose M (2013) The bicentenary of the research on ‘beautiful’ Vavilovia (Vavilovia formosa), a legume crop wild relative with taxonomic and agronomic potential. Bot J Linn Soc 172:524–531. doi:10.1111/boj.12060

    Article  Google Scholar 

  • Mikič A, Smýkal P, Kenicer G, Vishnyakova M, Sarukhanyan N, Akopian JA, Vanyan A, Gabrielyan I, Smýkalová I, Sherbakova E, Zorić L, Atlagić J, Zeremski-Škorić T, Cupina B, Krstić D, Jajić I, Antanasović S, Dorđević V, Mihailović V, Ivanov A, Ochatt S, Toker C, Zlatković B, Ambrose M (2014) Beauty will save the world, but will the world save beauty? The case of the highly endangered Vavilovia formosa (Stev.) Fed. Planta 240:1139–1146. doi:10.1007/s00425-014-2136-9

    Article  PubMed  Google Scholar 

  • Nakhutsrishvili G (2013) High-mountain vegetation. In: Nakhutsrishvili G (ed) The vegetation of Georgia (South Caucasus). Springer, Berlin, pp 119–208

    Chapter  Google Scholar 

  • Namba T (1984) Competitive co-existence in a seasonally fluctuating environment. J Theor Biol 111:369–386. doi:10.1016/S0022-5193(84)80216-7

    Article  Google Scholar 

  • Nicotra AB, Leigh A, Boyce CK, Jones CS, Niklas KJ, Royer DL, Tsukaya H (2011) The evolution and functional significance of leaf shape in the angiosperms. Funct Pl Biol 38:535–552

    Article  Google Scholar 

  • Ohlemüller R, Anderson BJ, Araújo MB, Butchart SH, Kudrna O, Ridgely RS, Thomas CD (2008) The coincidence of climatic and species rarity: high risk to small-range species from climate change. Biol Lett 4:568–572. doi:10.1098/rsbl.2008.0097

    Article  PubMed  PubMed Central  Google Scholar 

  • Oskoueiyan R, Kazempour OS, Maassoumi AA, Nejadsattari T, Mozaffarian V (2010) Phylogenetic status of Vavilovia formosa (Fabaceae-Fabeae) based on nrDNA ITS and cpDNA sequences. Biochem Syst Ecol 38:313–319. doi:10.1016/j.bse.2010.01.011

    Article  CAS  Google Scholar 

  • Otto-Bliesner BL, Marshall SJ, Overpeck JT, Miller GH, Hu A (2006) Simulating Arctic climate warmth and icefield retreat in the last interglaciation. Science 311:1751–1753. doi:10.1126/science.1120808

    Article  Google Scholar 

  • Pescador DS, de Bello F, Valladares F, Escudero A (2015) Plant trait variation along an altitudinal gradient in mediterranean high mountain grasslands: controlling the species turnover effect. PLoS ONE 10:e0118876. doi:10.1371/journal.pone.0118876

    Article  PubMed  PubMed Central  Google Scholar 

  • Phillips SJ, Anderson RP, Schapired RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259. doi:10.1016/j.ecolmodel.2005.03.026

    Article  Google Scholar 

  • Potokina E, Blattner R, Alexandrova T, Bachmann K (2002) AFLP diversity in the common vetch (Vicia sativa L.) on the world scale. Theor Appl Genet 105:58–67. doi:10.1007/s00122-002-0866-8

    Article  CAS  PubMed  Google Scholar 

  • Prévost D, Drouin P, Antoun H (1999) The potential use of cold-adapted rhizobia to improve symbiotic nitrogen fixation in legumes cultivated in temperate regions. In: Margesin R, Schninner F (eds) Fundamentals and application of cold-adapted organisms. Springer, Heidelberg, pp 161–176

    Google Scholar 

  • Reshiger KH (1979) Lathyrus. In: Reshinger KH (ed) Flora Iranica, 140th edn. Akademische druck und Verlagsansalt, Graz, Austria

    Google Scholar 

  • Rohlf FJ (1997) NTSYS: numerical taxonomy and multivariate analysis system, version 2.0. Exeter Software, Setauket

  • Rohlf FJ (2010) Tps Series. Department of ecology and evolution, State University of New York, Stony Brook. Available at: http://life.bio.sunysb.edu/morph/

  • Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Molec Ecol Notes 4:137–138. doi:10.1046/j.1471-8286.2003.00566.x

    Article  Google Scholar 

  • Safronova VI, Kimeklis AK, Chizhevskaya EP, Belimov AA, Andronov EE, Pinaev AG, Pukhaev AR, Popov KP, Tikhonovich IA (2014) Genetic diversity of rhizobia isolated from nodules of the relic species Vavilovia formosa (Stev.) Fed. Antonie  van  Leeuwenhoek  J  Microbiol  Serol 105:389–399. doi:10.1007/s10482-013-0089-9

    Article  Google Scholar 

  • Safronova VI, Kuznetsova IG, Sazanova AL, Kimeklis AK, Belimov AA, Andronov EE, Pinaev AG, Chizhevskaya EP, Pukhaev AR, Popov KP, Willems A, Tikhonovich IA (2015) Bosea vaviloviae sp. nov., a new species of slow-growing rhizobia isolated from nodules of the relict species Vavilovia formosa (Stev.) Fed. Antonie  van  Leeuwenhoek  J  Microbiol  Serol 107:911–920. doi:10.1007/s10482-015-0383-9

    Article  CAS  Google Scholar 

  • Sayadyan YV (2006) Upper miocene, pliocene, and quaternary stratigraphic reference sections of large intermontane depressions in Armenia. Doklady Earth Sci 407:217–219

    Article  CAS  Google Scholar 

  • Schaefer H, Hechenleitner P, Santos-Guerra A, Menezes de Sequeira M, Pennington RT, Kenicer G, Carine MA (2012) Systematics, biogeography, and character evolution of the legume tribe Fabeae with special focus on the middle-Atlantic island lineages. BMC Evol Biol 12:250. doi:10.1186/1471-2148-12-250

    Article  PubMed  PubMed Central  Google Scholar 

  • Schlee M, Göker M, Grimm GW, Hemleben V (2011) Genetic patterns in the Lathyrus pannonicus complex (Fabaceae) reflect ecological differentiation rather than biogeography and traditional subspecific division. Bot J Linn Soc 165:402–421. doi:10.1111/j.1095-8339.2011.01125.x

    Article  Google Scholar 

  • Schlüter PM, Harris SA (2006) Analysis of multilocus fingerprinting data sets containing missing data. Molec Ecol Notes 6:569–572. doi:10.1111/j.1471-8286.2006.01225.x

    Article  Google Scholar 

  • Schoener TW (1968) Anolis lizards in Bimini: resource partitioning in a complex fauna. Ecology 49:704–726

    Article  Google Scholar 

  • Sinjushin AA, Akopian JA (2011) On seedling structure in Pisum L., Lathyrus L. and Vavilovia Fed. (Fabeae: Fabaceae). Wulfenia 18:81–93

    Google Scholar 

  • Sinjushin AA, Belyakova AS (2010) On intraspecific variation of Vavilovia formosa (Stev.) Fed. (=Pisum formosum (Stev.) Alef.: Fabeae). Pisum Genet 42:31–34

    Google Scholar 

  • Sinjushin AA, Demidenko NV, Gostimskii SA (2009) Preliminary report on taxonomical position of Vavilovia formosa (Stev.) Fed. evidenced from morphological and molecular data. Pisum Genet 41:15–20

    Google Scholar 

  • Smýkal P, Coyne C, Ambrose M, Maxted N, Schaefer H, Blair MW, Berger J, Greene SL, Nelson MN, Besharat N, Vymyslický T, Toker C, Saxena RK, Roorkiwal M, Pandey MK, Hu J, Li YH, Wang LX, Guo Y, Qiu LJ, Redden RJ, Varshney RK (2015) Legume crops phylogeny and genetic diversity for science and breeding. Crit Rev Pl Sci 34:43–104. doi:10.1080/07352689.2014.897904

    Article  Google Scholar 

  • Smýkal P, Kenicer G, Flavell AJ, Corander J, Kosterin O, Redden RJ, Ford R, Coyne CJ, Maxted N, Ambrose MJ, Ellis THN (2011) Phylogeny, phylogeography and genetic diversity of the Pisum genus. Pl Genet Resources 9:4–18. doi:10.1017/S147926211000033x

    Article  Google Scholar 

  • Soudzilovskaia NA, Elumeeva TG, Onipchenko VG et al (2013) Functional traits predict relationship between plant abundance dynamic and long-term climate warming. Proc Natl Acad Sci USA 110:18180–18184. doi:10.1073/pnas.1310700110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Speed JDM, Austrheim G, Hester AJ, Mysterud A (2012) Elevational advance of alpine plant communities is buffered by herbivory. J Veg Sci 23:617–625. doi:10.1111/j.1654-1103.2012.01391.x

    Article  Google Scholar 

  • Steele KP, Wojciechowski MF (2003) Phylogenetic analyses of tribes Trifolieae and Vicieae, based on sequences of the plastid gene matK (Papilionoideae: Leguminosae). In: Klitgaard BB, Bruneau A (eds) Advances in Legume Systematics, 10th edn. Royal Botanical Garden, Kew, pp 355–370

    Google Scholar 

  • Steven C (1812) Orobus formosus Steven. Mém Soc Imp Naturalistes Moscou 4:50

    Google Scholar 

  • Stewart JR, Lister AM, Barnes I, Dalén L (2010) Refugia revisited: individualistic responses of species in space and time. Proc Roy Soc London Ser B Biol Sci 277:661–671. doi:10.1098/rspb.2009.1272

    Article  Google Scholar 

  • Tarkhnishvili D, Gavashelishvili A, Mumladze L (2012) Palaeoclimatic models help to understand current distribution of Caucasian forest species. Biol J Linn Soc 105:231–248. doi:10.1111/j.1095-8312.2011.01788.x

    Article  Google Scholar 

  • Tarasov PE, Volkova VS, Webb T et al (2000) Last glacial maximum biomes reconstructed from pollen and plant macrofossil data from northern Eurasia. J Biogeogr 27:609–620. doi:10.1046/j.13652699.2000.00429.x

    Article  Google Scholar 

  • Tamanyan K, Fayvush G, Nanagyulyan S, Danielyan T (eds) (2010) The Red Book of plants of Armenian Republic (higher plants and fungi). Zangak, Yerevan

  • Tomooka N, Yoon MS, Doi K, Kaga A, Vaughan D (2002) AFLP analysis of diploid species in the genus Vigna subgenus Ceratotropis. Genet Resources Crop Evol 49:521–530. doi:10.1023/A:1020954800107

    Article  Google Scholar 

  • Townsend CC, Guest E (eds) (1974) Flora of Iraq, vol. 3. Ministry of Agriculture & Agrarian Reform, Baghdad

  • Tzedakis PC, Emerson BC, Hewitt GM (2013) Cryptic or mystic? Glacial tree refugia in northern Europe. Trends Ecol Evol 28:696–704. doi:10.1016/j.tree.2013.09.001

    Article  CAS  PubMed  Google Scholar 

  • van de Wouw M, Maxted N, Chabane K, Ford-Lloyd BV (2001) Molecular taxonomy of Vicia ser. Vicia based on amplified fragment length polymorphisms. Pl Syst Evol 229:95–105. doi:10.1007/s006060170020

    Google Scholar 

  • Vos P, Hogers R, Bleeker M et al (1995) AFLP—a new technique for DNA-fingerprinting. Nucleic Acid Res 23:4407–4414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warren DL, Glor RE, Turelli M (2008) Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62:2868–2883. doi:10.1111/j.1558-5646.2008.00482.x

    Article  PubMed  Google Scholar 

  • Warren DL, Glor RE, Turelli M (2010) ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 33:607–611. doi:10.1111/j.1600-0587.2009.06142.x

    Article  Google Scholar 

  • Watanabe S et al (2011) MIROC-ESM 2010: Model description and basic results of CMIP5-20c3m experiments. Geosci Model Dev 4:845–872. doi:10.5194/gmd-4-845-2011

    Article  Google Scholar 

  • Webb T, Bartlein PJ (1992) Global changes during the last 3 million years: climatic controls and biotic responses. Ann Rev Ecol Syst 23:141–173

    Article  Google Scholar 

  • Wu QB, Dong XF, Liu YZ, Jin HJ (2007) Responses of permafrost on the Qinghai–Tibet Plateau, China, to climate change and engineering construction. Arct Antarct Alp Res 39:682–687. doi:10.1029/2006JF000631

    Article  Google Scholar 

  • Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Molec Biol Rev 63:968–989

    CAS  Google Scholar 

Download references

Acknowledgements

The authors thank to A. Mikič for an inspiration of this study and to P.C. Tzedakis for discussions on the concept of the paper. M. Vishnyakova, VIR, Russia are acknowledged for facilitating access to respective herbarium specimens. This work was supported by Royal Society of Edinburgh fellowship (P.S. and G.K.) and Palacky University grant Agency IGA 2013_001, IGA 2014_001, IGA 2015_001 and IGA 2016_001 funding (P.S., M.CH., L.M., M.K.).

Author information

Authors and Affiliations

  1. Department of Botany, Faculty of Sciences, Palacký University in Olomouc, Šlechtitelů 27, 783 71, Olomouc-Holice, Czech Republic

    Petr Smýkal, Michala Chaloupská, Lucie Marečková & Miloslav Kitner

  2. Department of Biology and Botanical Garden, University of Crete, Heraklion, Greece

    Michael Bariotakis & Stergios Pirintsos

  3. Department of Genetics, Lomonosov Moscow State University, Moscow, Russia

    Andrey Sinjushin

  4. National Academy of Sciences, Institute of Botany, Yerevan, Armenia

    Ivan Gabrielyan & Janna Akopian

  5. Akdeniz University, Antalya, Turkey

    Cengiz Toker

  6. Royal Botanical Garden Edinburgh, Edinburgh, UK

    Gregory Kenicer

Authors
  1. Petr Smýkal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michala Chaloupská
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael Bariotakis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lucie Marečková
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrey Sinjushin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ivan Gabrielyan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Janna Akopian
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Cengiz Toker
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Gregory Kenicer
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Miloslav Kitner
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Stergios Pirintsos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Petr Smýkal.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling editor: Andreas Tribsch.

Electronic supplementary material

Information on Electronic Supplementary Material

Information on Electronic Supplementary Material

Online Resource 1. List of samples used in the study, with indicated origin, collector, locality information, GenBank accession numbers and molecular ITS and cpDNA haplotypes.

Online Resource 2. Nucleotide alignment of sequenced part of matK gene.

Online Resource 3. List of species accompanying Vavilovia formosa at studied localities.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Smýkal, P., Chaloupská, M., Bariotakis, M. et al. Spatial patterns and intraspecific diversity of the glacial relict legume species Vavilovia formosa (Stev.) Fed. in Eurasia. Plant Syst Evol 303, 267–282 (2017). https://doi.org/10.1007/s00606-016-1368-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-016-1368-5

Keywords

Search

Navigation