Abstract
Goniolimon species are mainly components of the Eurasian steppe or steppe-like rocky vegetation, with some taxa occurring also in south-eastern Europe and northern Africa. We analysed the variability of: (i) two maternally inherited plastid loci (rpl32-trnL and 3′rps16-5′trnK) in 110 individuals of six currently accepted species from the Balkans and one species from the Apennines, to provide new insights into their origin and evolutionary history; and (ii) quantitative morphological characters (14 independent characters and one ratio character) in 641 individuals of three species of which two are morphologically and ecologically similar (G. italicum and G. tataricum) and the third, G. dalmaticum, was frequently misidentified as G. tataricum in the past, to provide new taxonomic treatment for proposed G. tataricum subspecies. We delineated several quantitative and five qualitative characters studied in a more limited sample as diagnostic for the identification of four subspecies (three newly described and one in a new rank) of G. tataricum. The history of westward peripheral populations of this species in the Balkans and the Apennines was rather complex and driven by local geo-historic events. These events facilitated multiple waves of east–west expansion of lineages originating from sources outside of the Balkan Peninsula which periodically diversified and occupied localised areas in the Balkans during the Pleistocene. An initial spread of an ancient G. tataricum lineage throughout south-eastern Europe probably occurred during the Messinian Salinity Crisis. Inter- and intraspecific hybridisation/introgression, as well as retention of ancestral polymorphisms, was common in G. tataricum and related taxa over time.
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References
Aleksić JM, Geburek T (2014) Quaternary population dynamics of an endemic conifer, Picea omorika, and their conservation implications. Conservation Genet 15:87–107. https://doi.org/10.1007/s10592-013-0523-6
Aleksić JM, Stojanović D, Banović B, Jančić R (2012) A simple and efficient DNA isolation method for Salvia officinalis. Biochem Genet 50:881–892. https://doi.org/10.1007/s10528-012-9528-y
Aleksić JM, Piotti A, Geburek T, Vendramin GG (2017) Exploring and conserving a “microcosm”: whole-population genetic characterization within a refugial area of the endemic, relict conifer Picea omorika. Conservation Genet 18:777–788. https://doi.org/10.1007/s10592-017-0926-x
Aleksić J, Škondrić S, Lakušić D (2018) Comparative phylogeography of capitulate Campanula species from the Balkans, with description of a new species, C. daucoides. Pl Syst Evol 304:549–575. https://doi.org/10.1007/s00606-018-1490-7
Ančev M (1982) Plumbaginaceae Lindl. In: Velčev V, Kožuharov S (eds) Flora Reipublicae Popularis Bulgaricae 8. Bulgarian Academy of Sciences, Sofia, pp 342–364 (In Bulgarian)
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge
Baker HG (1966) The evolution, functioning, and breakdown of heteromorphic incompatibility systems. I. The Plumbaginaceae. Evolution 20:349–368. https://doi.org/10.1111/j.1558-5646.1966.tb03371.x
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molec Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Barina Z, Caković D, Pifko D, Schönswetter P, Somogyi G, Frajman B (2017) Phylogenetic relationships, biogeography and taxonomic revision of Gymnospermium (Berberidaceae). Bot J Linn Soc 184:298–311. https://doi.org/10.1093/botlinnean/box028
Barina Z, Somogyi G, Pifkó D, Rakaj M (2018) Checklist of vascular plants of Albania. Phytotaxa 378:1–339. https://doi.org/10.11646/phytotaxa.378.1.1
Beatty GE, McEvoy PM, Sweeney O, Provan J (2008) Range-edge effects promote clonal growth in peripheral populations of the one-sided wintergreen Orthilia secunda. Diversity Distrib 14:546–555. https://doi.org/10.1111/j.1472-4642.2008.00469.x
Bjelčić Ž (1967) Plumbaginaceae. In: Beck Mannagetta G, Maly K, Bjelčić Ž (eds) Flora Bosnae et Hercegovinae 4. Zemaljski muzej Bosne i Hercegovine, Sarajevo, pp 11–13 (In Bosnian)
Bogdanović S (2015) Goniolimon dalmaticum (C. Presl) Rchb. f. In: Nikolić T, Milović M, Bogdanović S, Jasprica N (eds) Endemi u Hrvatskoj flori. Alfa d.d., Zagreb, pp 271–272 (In Croatian)
Boissier E (1848) Plumbaginaceae. In: de Candolle AP (ed) Prodromus systematis naturalis regni vegetabilis 12. Treuttel et Wurz, Paris, pp 617–696
Bokhari MK, Edmondson JR (1982) Goniolimon Boiss. In: Davis PH (ed) Flora of Turkey and the East Aegean Islands 7. University Press, Edinburgh, p 477
Brown RP, Yang Z (2011) Rate variation and estimation of divergence times using strict and relaxed clocks. BMC Evol Biol 11:271
Buzurović U, Stevanović V, Niketić M, Jakovljević K, Tomović G (2013) On the distribution of Goniolimon tataricum (Plumbaginaceae) in Serbia. Bot Serbica 37:167–172
Buzurović U, Bogdanović S, Niketić M, Tomović G (2016) Goniolimon dalmaticum Rchb. f. and G. tataricum (L.) Boiss. (Plumbaginaceae) in the Croatian flora and their distribution in the Balkan Peninsula. Acta Bot Croat 75:164–172. https://doi.org/10.1515/botcro-2016-0035
Buzurović U, Bogdanović S, Brullo S, Niketić M, Tomović G (2018) Goniolimon africanum (Plumbaginaceae), a new endemic species from North Africa. Phytotaxa 349:287–297. https://doi.org/10.11646/phytotaxa.349.3.10
CBOL Plant Working Group (2009) A DNA barcode for land plants. Proc Natl Acad Sci USA 106:12794–12797. https://doi.org/10.1073/pnas.0905845106
Chiang YC, Hung KH, Moore SJ, Ge XJ, Hung S, Hsu TW, Schaal BA, Chiang TY (2009) Paraphyly of organelle DNAs in Cycas Sect. Asiorientales due to ancient ancestral polymorphisms. BMC Evol Biol 9:161. https://doi.org/10.1186/1471-2148-9-161
Chumova Z, Zaveska E, Mandakova T, Krak K, Travniček P (2017) The Mediterranean: the cradle of Anthoxanthum (Poaceae) diploid diversity. Ann Bot (Oxford) 120:285–302. https://doi.org/10.1093/aob/mcx021
Crow JF (1993) Mutation, mean fitness, and genetic load. In: Futuyma D, Antonovics J (eds) Oxford surveys in evolutionary biology 9. Oxford University Press, Oxford, pp 3–42
Dimopoulos P, Raus Th, Bergmeier E, Constantinidis Th, Iatrou G, Kokkini S, Strid A, Tzanoudakis D (2013) Vascular plants of Greece: an annotated checklist. Botanical Garden and Botanical Museum Berlin-Dahlem, Hellenic Botanical Society, Berlin, Athens
Dobeš C, Rossa J, Paule J, Hülber K (2013) Morphology, DNA-molecular variation, karyology, ecogeography, and phytosociology suggest allopatric differentiation and species rank for Potentilla rigoana (Rosaceae). Taxon 62:733–745. https://doi.org/10.12705/624.8
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molec Biol Evol 29:1969–1973. https://doi.org/10.1093/molbev/mss075
Đurović S, Schönswetter P, Niketić M, Tomović G, Frajman B (2017) Disentangling relationships among the members of the Silene saxifraga alliance (Caryophyllaceae): phylogenetic structure is geographically rather than taxonomically segregated. Taxon 66:343–364. https://doi.org/10.12705/662.4
Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Molec Ecol 17:1170–1188. https://doi.org/10.1111/j.1365-294X.2007.03659.x
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Faraday C, Thomson W (1986) Functional aspects of the salt glands of the Plumbaginaceae. J Exp Bot 37:1129–1135. https://doi.org/10.1093/jxb/37.8.1129
Filipowicz N, Nee MH, Renner SS (2012) Description and molecular diagnosis of a new species of Brunfelsia (Solanaceae) from the Bolivian and Argentinean Andes. PhytoKeys 10:83–94. https://doi.org/10.3897/phytokeys.10.2558
Frajman B, Schneeweiss GM (2009) A campanulaceous fate: the Albanian stenoendemic Asyneuma comosiforme in fact belongs to isophyllous Campanula. Syst Bot 34:595–601. https://doi.org/10.1600/036364409789271173
Frajman B, Schönswetter P (2017) Amphi-Adriatic distributions in plants revisited: pleistocene trans-Adriatic dispersal in the Euphorbia barrelieri group (Euphorbiaceae). Bot J Linn Soc 185:240–252. https://doi.org/10.1093/botlinnean/box055
Frajman B, Eggens F, Oxelman B (2009) Hybrid origins and homoploid reticulate evolution within Heliosperma (Sileneae, Caryophyllaceae)—a multigene phylogenetic approach with relative dating. Syst Biol 58:328–345. https://doi.org/10.1093/sysbio/syp030
Franzke A, Hurka H, Janssen D, Neuffer B, Friesen N, Markov M, Mummenhoff K (2004) Molecular signals for late tertiary/early quaternary range splits of an Eurasian steppe plant: clausia aprica (Brassicaceae). Molec Ecol 13:2789–2795. https://doi.org/10.1111/j.1365-294X.2004.02272.x
Friesen N, German DA, Hurka H, Herden T, Oyuntsetseg B, Neuffer B (2016) Dated phylogenies and historical biogeography of Dontostemon and Clausia (Brassicaceae) mirror the palaeogeographical history of the Eurasian steppe. J Biogeogr 43:738–749. https://doi.org/10.1111/jbi.12658
Gajić M (1972) Plumbaginaceae Lindl. In: Josifović M (ed) Flora SR Srbije 3. Srpska akademija nauka i umetnosti, Beograd, pp 90–98 (In Serbian)
González-Gutiérrez PA, Köhler E, Borsch T (2013) New species of Buxus (Buxaceae) from northeastern Cuba based on morphological and molecular characters, including some comments on molecular diagnosis. Willdenowia 43:125–137. https://doi.org/10.3372/wi.43.43115
Graur D, Li WH (2000) Fundamentals in molecular evolution. Sinauer Associates, Sunderland
Greuter W, Burdet MH, Long G (1989) Med-Checklist 4 Conservatoire et Jardin botaniques de la Ville de Genève. Med-Checklist Trust of OPTIMA, Genève
Grigore MN, Toma C (2016) Structure of salt glands of Plumbaginaceae. Rediscovering old findings of the 19th century: ‘Mettenius’ or ‘Licopoli’ organs? J Pl Developm 23:37–52
Hardion L, Dumas PJ, Abdel-Samad F, Dager Kharrat MB, Surina B, Affre L, Médail F, Bacchetta G, Baumel A (2016) Geographical isolation caused the diversification of the Mediterranean thorny cushion-like Astragalus L. sect. Tragacantha DC. (Fabaceae). Molec Phylogen Evol 97:187–195. https://doi.org/10.1016/j.ympev.2016.01.006
Harzhauser M, Mandić O (2008) Neogene lake systems of central and south-eastern Europe: faunal diversity, gradients and interrelations. Palaeogeogr Palaeoclimatol Palaeoecol 260:417–434. https://doi.org/10.1016/j.palaeo.2007.12.013
Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276. https://doi.org/10.1111/j.1095-8312.1996.tb01434.x
Hurka H, Friesen N, German DA, Franzke A, Neuffer B (2012) ‘Missing link’ species Capsella orientalis and Capsella thracica elucidate evolution of model plant genus Capsella (Brassicaceae). Molec Ecol 21:1223–1238. https://doi.org/10.1111/j.1365-294X.2012.05460.x
Jakovljević K, Lakušić D, Vukojičić S, Tomović G, Šinžar-Sekulić J, Stevanović V (2011) Richness and diversity of Pontic flora on serpentine of Serbia. Cent Eur J Bio 6:260–274. https://doi.org/10.2478/s11535-010-0110-5
Jarvis C (2007) Order out of chaos: Linnaean plant names and their types. The Linnean Society of London in association with the Natural History Museum, London
Joly S, McLenachan PA, Lockhart PJ (2009) A statistical approach for distinguishing hybridization and incomplete lineage sorting. Amer Naturalist 174:E54–E70. https://doi.org/10.1086/600082
Jones K, Korotkova N, Petersen J, Henning T, Borsch T, Kilian N (2017) Dynamic diversification history with rate upshifts in Holarctic bell-flowers (Campanula and allies). Cladistics 33:637–666. https://doi.org/10.1111/cla.12187
Kamelin RV (1998) Materials on the history of the flora of Asia: Altai Mountain Country. Altai University Press, Barnaul (In Russian)
Korotkova N, Borsch T, Quandt D, Taylor NP, Müller KF, Barthlott W (2011) What does it take to resolve relationships and to identify species with molecular markers? An example from the epiphytic Rhipsalideae (Cactaceae). Amer J Bot 98:1549–1572. https://doi.org/10.3732/ajb.1000502
Koutroumpa K, Theodoridis S, Warren BH, Jiménez A, Celep F, Doğan M, Romeiras MM, Santos-Guerra A, Fernández-Palacios JM, Caujapé-Castells J, Moura M, Menezes de Sequeira M, Conti E (2018) An expanded molecular phylogeny of Plumbaginaceae, with emphasis on Limonium (sea lavenders): taxonomic implications and biogeographic considerations. Ecol Evol 8:12397–12424. https://doi.org/10.1002/ece3.4553
Kramer AT, Ison JL, Ashley MV, Howe HF (2008) The paradox of forest fragmentation genetics. Conservation Bio 22:878–885. https://doi.org/10.1111/j.1523-1739.2008.00944.x
Krstić N, Savić L, Jovanović G (2012) The Neogene lakes on the Balkan land. Geol Anali Balkanskoga Poluostrva 73:37–60. https://doi.org/10.2298/GABP1273037K
Kubitzki K (1993) Plumbaginaceae. In: Kubitzki K, Rohwer JR, Bittrich V (eds) The families and genera of vascular plants. Springer, Berlin, pp 523–530
Kučera J, Marhold K, Lihová J (2010) Cardamine maritima group (Brassicaceae) in the amphi-Adriatic area: a hotspot of species diversity revealed by DNA sequences and morphological variation. Taxon 59:148–164
Le Floc’h E, Boulos L, Vela E (2010) Catalogue synonymique commenté de la Flore de Tunisie. Banque Nationale de Gènes, Tunis
Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189. https://doi.org/10.1016/S0169-5347(02)02497-7
Lesica P, Allendorf FW (1995) When peripheral populations valuable for conservation? Conservation Biol 9:753–760. https://doi.org/10.1046/j.1523-1739.1995.09040753.x
Lewis PO, Crawford DJ (1995) Pleistocene refugium endemics exhibit greater allozyme diversity than widespread congeners in the genus Polygonella (Polygonaceae). Amer J Bot 82:141–149. https://doi.org/10.1002/j.1537-2197.1995.tb11483.x
Lewis PO, Holder MT, Holsinger KE (2005) Polytomies and Bayesian phylogenetic inference. Syst Biol 54:241–253. https://doi.org/10.1080/10635150590924208
Linczevski IA (1952) Plumbaginaceae Lindl, except the genera Plumbaginella, Armeria, Psylliostachys. In: Shishkin BK, Bobrov EG (eds) Flora SSSR 18. Botanicheskii institut akademii nauk SSSR, Moskva-Lenjingrad, pp 293–474 (In Russian)
Linné C (1753) Species Plantarum. Laurentius Salvius, Stockholm. https://doi.org/10.5962/bhl.title.669
Lledó MD, Crespo MB, Fay MF, Chase MW (2005) Molecular phylogenetics of Limonium and related genera (Plumbaginaceae): biogeographical and systematic implications. Amer J Bot 92:1189–1198. https://doi.org/10.3732/ajb.92.7.1189
Maddison WP, Knowles LL (2006) Inferring phylogeny despite incomplete lineage sorting. Syst Biol 55:21–30. https://doi.org/10.1080/10635150500354928
Magyar I, Geary DH, Müller P (1999) Paleogeographic evolution of the Late Miocene Lake Pannon in Central Europe. Palaeogeogr Palaeoclimatol Palaeoecol 147:151–167. https://doi.org/10.1016/S0031-0182(98)00155-2
Malakhova LA (1990) Kariologocheskij analiz prirodnykh populjacij redkich i ischezajushchikh rastenij na juge Tomskoj Oblasti. Byull Glavn Bot Sada 155:60–66
Médail F, Diadema K (2009) Glacial refugia influence plant diversity patterns in the Mediterranean Basin. J Biogeogr 36:1333–1345. https://doi.org/10.1111/j.1365-2699.2008.02051.x
Medrano M, Herrera CM (2008) Geographical structuring of genetic diversity across the whole distribution range of Narcissus longispathus, a habitat-specialist, Mediterranean narrow endemic. Ann Bot (Oxford) 102:183–194. https://doi.org/10.1093/aob/mcn086
Meimberg H, Ditrich P, Bringmann G, Schlauer J, Heubl G (2000) Molecular phylogeny of Caryophllidae s.l. based on matK sequences with special emphasis on carnivorous taxa. Pl Biol 2:218–228. https://doi.org/10.1055/s-2000-9460
Micevski K, Matevski V (1995) Goniolimon Boiss. In: Micevski K (ed) Flora na Republika Makedonija 1. Makedonska akademija na naukite i umetnostite, Skopje, pp 480–482 (In North Macedonian)
Molins A, Bacchetta G, Rosato M, Rossello JA, Mayol M (2011) Molecular phylogeography of Thymus herba-barona (Lamiaceae): Insight into the evolutionary history of the flora of the western Mediterranean islands. Taxon 60:1295–1305
Morretti F, Puppi G, Giuliani C, Conti F (2015) Heterostyly in Goniolimon italicum (Plumbaginaceae), endemic to Abruzzo (central Apennines, Italy). Anales Jardin Bot Madrid 72:e014
Nikolić T (2015) Flora Croatica Database. Faculty of Science, University of Zagreb, Zagreb. Available at: http://hirc.botanic.hr/fcd/. Accessed 21 Oct 2015
Pančić J (1856) Verzeichniss der in Serbien wildwachsenden Phanerogamen. nebst den Diagnosen einiger neuer Arten. Wien. Verh K K Zool-Bot Ges Wien 6:475–598
Peng ZX, Kamelin V (1996) Plumbaginaceae. In: Wu ZY, Raven PH (eds) Flora of China, vol 15. Myrsinaceae through Loganiaceae. Missouri Botanical Garden Press, St. Louis, pp 190–204
Petriccione B, Marrone M (2013) First rapporto sullo stato e sulle azioni di conservazione attiva. Italy (L’ Aquila): Corpo forestale dello stato and Ufficio territorial per la biodiversita ‘Dell’Aquila, Italy. Available at: https://www.academia.edu/26043151/PRIMO_RAPPORTO_SULLO_STATO_E_SULLE_AZIONI_DI_CONSERVAZIONE_ATTIVA_DI_GONIOLIMON_ITALICUM. Accessed 1 Mar 2018
Pignatti S (1972) Goniolimon Boiss. In: Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora Europaea 3. Cambridge University Press, Cambridge, pp 50–51
Popov S, Shcherba IG, Ilyina IB, Nevesskaya AL, Paramonova PN, Khondkarian OS, Magyar I (2006) Late Miocene to Pliocene palaeogeography of the Paratethys and its relation to the Mediterranean. Palaeogeogr Palaeoclimatol Palaeoecol 238:91–106. https://doi.org/10.1016/j.palaeo.2006.03.020
Post GE (1883) Flora of Syria, Palestine, and Sinae, from the Taurus to Ras Muhammad, and from the Mediterranean Sea to the Syrian Desert. Syrian Protestant College, Beirut
Purvis A, Garland T (1993) Polytomies in comparative analyses of continuous characters. Syst Biol 42:569–575. https://doi.org/10.2307/2992489
Quézel P (1978) Analysis of the flora of Mediterranean and Saharan Africa. Ann Missouri Bot Gard 65:479–534. https://doi.org/10.2307/2398860
Quézel P, Santa S (1963) Nouvelle flore de l’Algérie et des regions désertoriques meridionales, Tome 2. Centre de la Recherche Scientifique, Paris
Rambaut A (2006) FigTree v1.1.1: Tree figure drawing tool. Available at: http://tree.bio.ed.ac.uk/software/figtree/. Accessed 1 Mar 2016
Rambaut A, Drummond AJ (2007) Tracer, version 1.4. Available at: http://beast.bio.ed.ac.uk/Tracer. Accessed 1 Mar 2016
Ranđelović N, Stamenković V (1986) Goniolimon tataricum (L.) Boiss. In: Sarić M, Diklić N (eds) Flora SR Srbije 10. Srpska akademija nauka i umetnosti, Beograd, p 57
Rǎvǎrut M (1960) Plumbaginaceae Lindl. In: Sǎvulescu T (ed) Flora Republicii Populare Romîne 7. Academiei Republicii populare Romîne, Bucuresti, pp 21–40
Reichenbach H.G. filio (1854–1855) Icones florae Germanicae et Helveticae 17. Sumptibus Ambrosii Abel, Lipsiae
Rešetnik I, Frajman B, Schönswetter P (2016) Heteroploid Knautia drymeia includes K. gussonei and cannot be separated into diagnosable subspecies. Amer J Bot 103:1300–1313. https://doi.org/10.3732/ajb.1500506
Richards MB, Macaulay VA, Bandelt HJ, Sykes BC (1998) Phylogeography of mitochondrial DNA in western Europe. Ann Human Genet 62:241–260. https://doi.org/10.1046/j.1469-1809.1998.6230241.x
Rieseberg LH (1995) The role of hybridization in evolution: old wine in new skins. Amer J Bot 82:944–953
Rieseberg LH, Willis JH (2007) Plant speciation. Science 317:910–914. https://doi.org/10.1126/science.1137729
Rouchy JM, Caruso A (2006) The Messinian salinity crisis in the Mediterranean basin: a reassessment of the data and an integrated scenario. Sediment Geol 188–189:35–67. https://doi.org/10.1016/j.sedgeo.2006.02.005
Runemark H (1974) Studies in the Aegean flora. XXIII. Goniolimon Boiss. (Plumbaginaceae). Bot Not 127:540–545
Schaal BA, Hayworth DA, Olsen KM, Rauscher JT, Smith WA (1998) Phylogeographic studies in plants: problems and prospects. Molec Ecol 7:465–474. https://doi.org/10.1046/j.1365-294x.1998.00318.x
Schlötterer C (1998) Microsatellites. In: Hoelzel AR (ed) Molecular genetic analysis of populations. IRL Press at Oxford University Press, Oxford
Seberg O, Petersen G (2009) How many loci does it take to DNA barcode a Crocus? PLoS ONE 4:e4598. https://doi.org/10.1371/journal.pone.0004598
Seregin AP, Anackov G, Friesen N (2015) Molecular and morphological revision of the Allium saxatile group (Amaryllidaceae): geographical isolation as the driving force of underestimated speciation. Bot J Linn Soc 178:67–101. https://doi.org/10.1111/boj.12269
Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Amer J Bot 94:275–288. https://doi.org/10.3732/ajb.94.3.275
Siebert A, Voss A (1896) Vilmorin’s Blumengärtnerei. Dritte Neubearbeite Auflage 1:614
StatSoft (2008) STATISTICA (Data Analysis Software System), Version 7.0. StatSoft Inc., Tulsa. Available at: www.statsoft.com
Stevanović V, Jovanović S, Lakušić D, Niketić M (1995) Diverzitet vaskularne flore Jugoslavije sa pregledom vrsta od međunarodnog značaja. In: Stevanović V, Vasić V (eds) Biodiverzitet Jugoslavije sa pregledom vrsta od međunarodnog značaja. Biološki fakultet & Ecolibri, Beograd, pp 183–217 (In Serbian)
Stojanović D, Aleksić JM, Jančić I, Jančić R (2015) A Mediterranean medicinal plant in the continental Balkans: a plastid DNA-based phylogeographic survey of Salvia officinalis (Lamiaceae) and its conservation implications. Willdenowia 45:103–118. https://doi.org/10.3372/wi.45.45112
Strid A (2015) Reliquiae Runemarkianae. Chromosome numbers of angiosperms from the Aegean Islands. Phytol Balcan 21:245–293
Suc JP (1984) Origin and evolution of the Mediterranean vegetation and climate in Europe. Nature 307:429–432. https://doi.org/10.1038/307429a0
Surina B, Schneeweiss GM, Glasnović P, Schönswetter P (2014) Testing the efficiency of nested barriers to dispersal in the Mediterranean high mountain plant Edraianthus graminifolius (Campanulaceae). Molec Ecol 23:2861–2875. https://doi.org/10.1111/mec.12779
Tammaro F, Pignatti S, Frizzi G (1982) Goniolimon italicum (Plumbaginaceae), una nuova specie rinvenuta nei pressi di L’Aquila (Appennino Centrale). Webbia 36:39–46. https://doi.org/10.1080/00837792.1982.10670238
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molec Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121
Thiers B (2019) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available at: http://sweetgum.nybg.org/ih/. Accessed 15 Jan 2019
Tomović G, Niketić M, Lakušić D, Ranđelović V, Stevanović V (2014) Balkan endemic plants in Central Serbia and Kosovo regions: distribution patterns, ecological characteristics and centres of diversity. Bot J Linn Soc 176:173–202. https://doi.org/10.1111/boj.12197
Vangjeli J (2015) Excursion flora of Albania. Koeltz Scientific Books, Königstein
Velichko AA (1999) General features of the landscape and climate of northern Eurasia in the Cenozoic. In: Velichko AA (ed) Climate and environment changes during the last 65 million years. Cenozoic: from Palaeocene to Holocene. GEOS, Moscow, pp 219–233 (In Russian)
Volkova AP, Herden T, Friesen N (2017) Genetic variation in Goniolimon speciosum (Plumbaginaceae) reveals a complex history of steppe vegetation. Bot J Linn Soc 184:113–121. https://doi.org/10.1093/botlinnean/box011
Acknowledgements
The Ministry of Education, Science and Technological Development of the Republic of Serbia supported this research through Grant 173030 “Plant biodiversity of Serbia and the Balkans—assessment, sustainable use and protection”. One of the authors (S. Bogdanović) would like to thank the University of Zagreb through the programme of Academic mobility and Erasmus for partial funding of this research. The authors would like to thank A. Radić for language editing and are grateful to S. Djurović, I. Rešetnik and I. Ljubičić for help in the field.
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Contribution to “Plants of the Balkan Peninsula in Space and Time”
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Online Resource 1. Annotation of rpl32-trnL and 3′rps16-5′trnK plastid intergenic spacers used in the study and delineation of haplotypes detected in studied Goniolimon taxa.
Online Resource 2. Aligned matrix of two plastid intergenic spacers (3′rps16-5′trnK and rpl32-trnL) used in the study.
Online Resource 3. Positions of synapomorphic characters in two plastid regions in studied Goniolimon taxa.
Online Resource 4. a Eigenvalues for two-dimensional PCA by species Goniolimon dalmaticum, G. italicum and G. tataricum s.l. presented in Fig. 5a, b eigenvalues for three-dimensional PCA by species G. italicum and G. tataricum s.l. presented in Fig. 5b, c classification matrix for discriminant analysis by group presented in Fig. 5d, d standardised coefficients for canonical variables of CDA presented in Fig. 5d; characters that mostly contributed to the separation along particular axes are given in bold, e total canonical structure for canonical variables of CDA presented in Fig. 5d.
Online Resource 5. Holotype of Goniolimon tataricum (L.) Boiss. subsp. graecum Buzurović, subsp. nov. deposited in the Herbarium of the University of Belgrade (BEOU).
Online Resource 6. Holotype of Goniolimon tataricum (L.) Boiss. subsp. croaticum Buzurović & Bogdanović, subsp. nov. deposited in the Herbarium of the Natural History Museum in Belgrade (BEO).
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Buzurović, U., Tomović, G., Niketić, M. et al. Phylogeographic and taxonomic considerations on Goniolimon tataricum (Plumbaginaceae) and its relatives from south-eastern Europe and the Apennine Peninsula. Plant Syst Evol 306, 29 (2020). https://doi.org/10.1007/s00606-020-01636-0
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DOI: https://doi.org/10.1007/s00606-020-01636-0