Abstract
Key message
This study identified 10 fir populations that may be hybridogenous. The immediate activities on conservation of these polymorphic fir populations should be supported as hybrids may be ecologically and economically superior to the parent species.
Abstract
This is the first report on morpho-anatomical differentiation of both lower-rank and upper-rank needles in Abies alba, A. x borisii-regis, and A. cephalonica, using 18 native populations from almost the entire assumed hybrid zone in the Balkan Peninsula. The 35 morpho-anatomical characteristics were analyzed biometrically, and 18 with the application of multivariate statistical analysis. Clinal pattern in distribution of morpho-anatomical variation over the broader transition zone between the putative parent species was observed. Furthermore, the results of the biometric analyses justify the validity of this method for differentiating between the eastern A. alba lineage and A. cephalonica, for both needle types. Thus, the results of this study show clear differences between A. alba and A. cephalonica, but unstable characteristics of A. x borisii-regis. This finding supports the hypothesis that A. x borisii-regis is an unstabilized taxon produced by recent hybridization and introgression between A. alba and A. cephalonica. Based on the multivariate statistical analysis, 10 of the studied fir populations may be hybridogenous within a wider geographical area (southwestern and southern Bulgaria, southernmost North Macedonia and almost the entire Greece). The obtained results did not indicate a hybrid status for two fir populations from Peloponnese and one from the Cephalonia Island (pure A. cephalonica populations), which partly agrees with the recent molecular data.
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The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Andreev N (1992) Pinophyta. In: Kozuharov S (ed) Field guide to the vascular plants in Bulgaria. Naouka & Izkoustvo, Sofia, pp 81–85 (in Bulgarian)
Bagci E, Babaç MT (2003) A morphometric and chemosystematic study on the Abies Miller (Fir) species in Turkey. Acta Bot Gallica 150:355–367. https://doi.org/10.1080/12538078.2003.10516002
Balao F, Lorenzo MT, Sánchez-Robles JM, Paun O, García-Castaño JL, Terrab A (2020) Early diversification and permeable species boundaries in the Mediterranean firs. Ann Bot 125:495–507. https://doi.org/10.1093/aob/mcz186
Bella E, Liepelt S, Parducci L, Drouzas A (2014) Genetic insights into the hybrid origin of Abies x borisii-regis Mattf. Plant Syst Evol 301:749–759. https://doi.org/10.1007/s00606-014-1113-x
Boratyńska K, Sękiewicz K, Jasińska AK, Tomaszewski D, Iszkuło G, Ok T, BouDagher-Kharrat M, Boratyński A (2015) Effect of geographic range discontinuity on taxonomic differentiation of Abies cilicica. Acta Soc Bot Pol 84:419–430. https://doi.org/10.5586/asbp.2015.027
Campbell DR, Faidiga A, Trujillo G (2018) Clines in traits compared over two decades in a plant hybrid zone. Ann Bot 122:315–324. https://doi.org/10.1093/aob/mcy072
Christensen KI (1997) Abies Miller. In: Strid A, Tan K (eds) Flora Hellenica, vol 1. Koeltz Scientific Books, Königstein, pp 1–3
Drouzas AD (2000) Determination and analysis of variation of Greek fir species (Abies sp.), by using biochemical and molecular markers. Dissertation, Aristotle University of Thessaloniki.
Euro+Med 2006+ [continuously updated]: Euro+Med PlantBase - the information resource for Euro-Mediterranean plant diversity. – Published at http://www.europlusmed.org. Accessed 09 February 2023
Fady B, Arbez M, Marpeau A (1992) Geographic variability of terpene composition in Abies cephalonica Loudon and Abies species around the Aegean: Hypotheses for their possible phylogeny from the Miocene. Silvae Genet 41:273–278. https://doi.org/10.1007/BF00202432
Fady B (1993) Caractéristiques écologiques et sylvicoles des sapins de Grèce dans leur aire naturelle et en plantation dans le Sud de la France. Perspectives pour le reboisement en région méditerranéenne. Rev For Fr 45:119–133. https://hal.science/hal-03444183
Farjon A, Filer D (2013) An atlas of the world’s conifers: an analysis of their distribution, biogeography, diversity and conservation status, 1st edn. Koninklijke Brill NV, Leiden
Farjon A, Rushforth KD (1989) A classification of Abies Miller (Pinaceae). Notes Roy Bot Gard Edinburgh 46:59–77
Jalas J, Suominen J (1973) Atlas Florae Europaeae. 2 Gymnospermae (Pinaceae to Ephedraceae). Helsinki
Jasińska A, Sękiewicz K, Ok T, Romo A, Boratyński A, Boratyńska K (2017) Taxonomic position of Abies equi-trojani on the basis of needle characters by comparison with different fir species. Turk J Bot 41:620–631. https://doi.org/10.3906/bot-1612-1
Kormutak A, Vooková B, Čamek V, Salaj T, Galgóci M, Maňka P, Boleček P, Kuna R, Kobliha J, Lukáčik I, Gömöry D (2013) Artificial hybridization of some Abies species. Plant Syst Evol 299:1175–1184. https://doi.org/10.1007/s00606-013-0787-9
Krajmerová D, Paule L, Zhelev P, Voleková M, Evtimov I, Gagov V, Gömöry D (2015) Natural hybridization in eastern-Mediterranean firs: The case of Abies borisii-regis. Plant Biosyst 150:1189–1199. https://doi.org/10.1080/11263504.2015.1011723
Liepelt S, Bialozyt R, Ziegenhagen B (2002) Wind-dispersed pollen mediates postglacial gene flow among refugia. Proc Natl Acad Sci USA 99:14590–14594. https://doi.org/10.1073/pnas.212285399
Liepelt S, Mayland-Quellhorst E, Lahme M, Ziegenhagen B (2010) Contrasting geographical patterns of ancient and modern genetic lineages in Mediterranean Abies species. Plant Syst Evol 284:141–151. https://doi.org/10.1007/s00606-009-0247-8
Linares JC (2011) Biogeography and evolution of Abies (Pinaceae) in the Mediterranean Basin: the roles of long-term climatic change and glacial refugia. J Biogeogr 38:619–630. https://doi.org/10.1111/j.1365-2699.2010.02458.x
Litkowiec M, Sękiewicz K, Romo A, Ok T, BouDagher-Kharrat M, Jasińska AK, Sobierajska K, Boratyńska K, Boratyński A (2021) Biogeography and relationships of the Abies taxa from the mediterranean and central Europe regions as revealed by nuclear DNA markers and needle structural characters. For Ecol Manag 479:118606. https://doi.org/10.1016/j.foreco.2020.118606
Liu TS (1971) A monograph of the genus Abies. National Taiwan University, Taipei, College of Agriculture
Mattfeld J (1926) Die Europäischen und Mediterranen Abies Arten. Die Pflanzenareale 1:22–29 ((in German))
Mattfeld J (1930) Uber hybridogene Sippen der Tanne. Bibliotheca Botanika 100:1–84 ((in German))
Mitsopoulos DJ, Panetsos CP (1987) Origin of variation in fir forests of Greece. Silvae Genet 36:1–15
Nikolić B, Bojović S, Marin PD (2015) Variability of needle morpho-anatomical characters of Picea omorika from natural populations in Serbia. Plant Biosyst 149:61–67. https://doi.org/10.1080/11263504.2013.810180
Nikolić B, Bojović S, Marin PD (2016) Morpho-anatomical traits of Pinus peuce needles from natural populations in Montenegro and Serbia. Plant Biosyst 150:1038–1045. https://doi.org/10.1080/11263504.2014.1000999
Nikolić JS, Jovanović SČ, Zlatković B, Stojanović GS, Mitić Z (2021a) Variability of headspace volatiles in native population of Abies x borisii-regis from the central Rhodopes. Biol Nyssana 12:23–32. https://doi.org/10.5281/zenodo.5522967
Nikolić JS, Zlatković BK, Jovanović SČ, Stojanović GS, Marin PD, Mitić ZS (2021b) Needle volatiles as chemophenetic markers in differentiation of natural populations of Abies alba, A. x borisii-regis, and A. cephalonica. Phytochemistry 183:112612. https://doi.org/10.1016/j.phytochem.2020.112612
Panetsos KP (1992) Variation in the position of resin canals in the needles of Abies species and provenances. Ann Sci Forest 49:253–260. https://doi.org/10.1051/forest:19920304
Popović V, Nikolić B, Lučić A, Lj R, Šešlija Jovanović D, Miljković D (2022) Morpho-anatomical trait variability of the Norway spruce (Picea abies (L.) Karst.) needles in natural populations along elevational diversity gradient. Trees-Struct Funct 36:1131–1147. https://doi.org/10.1007/s00468-022-02277-1
Scaltsoyiannes A, Tsaktsira M, Drouzas AD (1999) Allozyme differentiation in the Mediterranean firs (Abies, Pinaceae). A first comparative study with phylogenetic implications. Plant Syst Evol 216:289–307. https://doi.org/10.1007/BF01084404
Sękiewicz K, Sękiewicz M, Jasińska AK, Boratyńska K, Iszkuło G, Romo A, Boratyński A (2013) Morphological diversity and structure of West Mediterranean Abies species. Plant Biosyst 147:125–134. https://doi.org/10.1080/11263504.2012.753130
Siskas E, Bella E, Papageorgiou AC, Kappas I, Tsiripidis I, Drouzas AD (2023) DNA-based identification of Abies cephalonica, A. alba and their hybrid (A. x borisii-regis) at the individual-level. Plant Biosyst 157:24–37. https://doi.org/10.1080/11263504.2022.2073396
Stefanović M, Nikolić B, Matić R, Popović Z, Vidaković V, Bojović S (2017) Exploration of sexual dimorphism of Taxus baccata L. needles in natural populations. Trees-Struct Funct 31:1697–1710. https://doi.org/10.1007/s00468-017-1579-6
Turrill WB (1937) XI-On the flora of the near east: XVIII. New species, new records and notes. Kew Bull 2:79–86. https://doi.org/10.2307/4107196
WFO (2023) World Flora Online. Published on the Internet; http://www.worldfloraonline.org. Accessed 09 February 2023
Xiang X-G, Cao M, Zhou Z-K (2007) Fossil history and modern distribution of the genus Abies (Pinaceae). Front Forest China 2:355–365. https://doi.org/10.1007/s11461-007-0058-4
Acknowledgements
This research was supported by Grant No 451-03-47/2023-01/ 200124 by the Ministry of Science, Technological Development and Innovation of Republic of Serbia. We are grateful to Dr. Dimitrija Savić Zdravković who made the original drawing of the arrangement of needles at the two-year old shoot increment in studied Abies taxa.
Funding
This study was funded by the Ministry of Science, Technological Development and Innovation of Republic of Serbia (Grant No 451-03-47/2023-01/ 200124).
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Mitić, Z.S., Nikolić, J.S., Jušković, M.Z. et al. Geographic differentiation of Abies alba, A. x borisii-regis, and A. cephalonica populations at the Balkan Peninsula based on needle morpho-anatomy. Trees 37, 1465–1481 (2023). https://doi.org/10.1007/s00468-023-02436-y
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DOI: https://doi.org/10.1007/s00468-023-02436-y