Phylogeny of beech in western Eurasia as inferred by approximate Bayesian computation

Dušan Gömöry, Ladislav Paule, Vladimír Mačejovský

Abstract


The Fagus sylvatica L. species complex in Europe and Western Asia comprises two commonly recognized subspecies, F. sylvatica subsp. sylvatica [= F. sylvatica sensu stricto (s. str.)] and F. sylvatica subsp. orientalis (= F. orientalis), and two putatively hybridogenous or intermediate taxa, “F. moesiaca” and “F. taurica”. The present study aimed to examine the demographic history of this species complex using 12 allelic loci of nine allozymes scored in 279 beech populations in western Eurasia. Three sets of phylogenetic scenarios were tested by approximate Bayesian computation: one dealing with the divergence of subspecies and/or regional populations within the whole taxonomical complex, and two others focusing on the potential hybrid origin of “F. moesiaca” and “F. taurica”. The best-supported scenario within the first set placed the time of divergence of regional populations of F. orientalis in the Early Pleistocene (1.18–1.87 My BP). According to this scenario, the Iranian population was the ancestral lineage, whereas F. sylvatica s. str. was the lineage that diverged most recently. “Fagus taurica” was found to have originated from hybridization between the Caucasian population of F. orientalis and F. sylvatica s. str. at 144 ky BP. In contrast, there was no evidence of a hybrid origin of “F. moesiaca”. The best-supported scenario suggested that the Balkan lineage is a part of F. sylvatica s. str., which diverged early from F. orientalis in Asia Minor (817 ky BP), while both the Italian and Central-European lineages diverged from the Balkan one later, at the beginning of the last (Weichselian) glacial period.

Keywords


Fagus sylvatica L.; Fagus orientalis Lipsky; phylogenetic scenario; allozymes

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References


Tutin TG, Heywood VH, Burges NA, Valentine, DH, Moore DM, editors. Flora Europaea. Volume 1, Psilotaceae to Platanaceae. Cambridge: Cambridge University Press; 1993.

Denk T. The taxonomy of Fagus in western Eurasia, 1: Fagus sylvatica subsp. orientalis (= F. orientalis). Feddes Repert. 1999;110:177–200. https://doi.org/10.1002/fedr.19991100305

Denk T. The taxonomy of Fagus in western Eurasia, 2: Fagus sylvatica subsp. sylvatica. Feddes Repert. 1999;110:381–412. https://doi.org/10.1002/fedr.19991100510

Wulff EV. The beech in Crimea, its systematic position and origin. In: Rübel E, editor. Die Buchenwälder Europas. Bern: Hans Huber; 1932. p. 223–261.

Гулисашвили [Gulisashvili] ВЗ [VZ], Махатадзе [Mahatadze] ЛБ [LB], Прилипко [Prilipko] ЛИ [LI]. Растительность Кавказа [Rastitel’nost’ Kavkaza]. Москва [Moskva]: Наука [Nauka]; 1975.

Mobayen S, Tregubov V. La carte de la végétation naturelle de l’Iran. Tehran: Université de Tehran; 1970.

Mayer H, Aksoy H. Wälder der Türkei. Stuttgart: Gustav Fischer; 1986.

Czeczott H. Distribution of Fagus orientalis Lipsky. In: Rübel E, editor. Die Buchenwälder Europas. Bern: Hans Huber; 1932. p. 362–387.

Greuter W, Raus T. Med-checklist notulae, 4. Willdenowia. 1981;11:271–280.

Poplavskaja GI. Contribution to experimental studies of the systematics of Crimean beech. Trudy Leningradskogo Obshchestva Estestvoispytatelej. 1936;3:353–371.

Czeczott H. Studium nad zmiennością liści buków: F. orientalis Lipsky, F. sylvatica L. i form pośrednich. Cz. I. Rocznik Dendrologiczny. 1933;5:45–121.

Mišić V. Varijabilitet i ekologija bukve u Jugoslaviji. Beograd: Biološki Institut N. R. Srbije; 1957.

Borza A. Le genre Fagus dans la République Populaire Roumaine. Biológia. 1965;20:367–373.

von Wühlisch G. EUFORGEN technical guidelines for genetic conservation and use for European beech (Fagus sylvatica). Rome: Bioversity International; 2008.

Kandemir G, Kaya Z. EUFORGEN technical guidelines for genetic conservation and use of oriental beech (Fagus orientalis). Rome: Biodiversity International; 2009.

Denk T, Grimm GW, Hemleben V. Patterns of molecular and morphological differentiation in Fagus (Fagaceae): phylogenetic implications. Am J Bot. 2005;92:1006–1016. https://doi.org/10.3732/ajb.92.6.1006

Denk T, Grimm G, Stögerer K, Langer M, Hembelen V. The evolutionary history of Fagus in western Eurasia: the evidence from genes, morphology and the fossil record. Plant Syst Evol. 2002;232:213–236. https://doi.org/10.1007/s006060200044

Denk T, Grimm GW. The biogeographic history of beech trees. Rev Palaeobot Palynol. 2009;158:83–100. https://doi.org/10.1016/j.revpalbo.2009.08.007

Göker M, Grimm GW. General functions to transform associate data to host data, and their use in phylogenetic inference from sequences with intra-individual variability BMC Evol Biol. 2008;8:86. https://doi.org/10.1186/1471-2148-8-86

Grimm GW, Denk T, Hemleben V. Coding of intraspecific nucleotide polymorphisms: a tool to resolve reticulate evolutionary relationships in the ITS of beech trees (Fagus L., Fagaceae). Syst Biodivers. 2007;5:291–309. https://doi.org/10.1017/S1477200007002459

Renner SS, Grimm GW, Kapli P, Denk T. Species relationships and divergence times in beeches: new insights from the inclusion of 53 young and old fossils in a birth–death clock model. Philos Trans R Soc Lond B Biol Sci. 2016;371:20150135. https://doi.org/10.1098/rstb.2015.0135

Gömöry D, Paule L, Vyšný J. Patterns of allozyme variation in western-Eurasian beeches. Bot J Linn Soc. 2007;154:165–174. https://doi.org/10.1111/j.1095-8339.2007.00666.x

Gömöry D, Paule L, Reticulate evolution patterns in western Eurasian beeches. Botanica Helvetica. 2010;120(1):63–74. https://doi.org/10.1007/s00035-010-0068-y

Pritchard JK, Stephens M, Donnelly P. Inference of population structure from multilocus genotype data. Genetics. 2000;155:945–959.

Corander J, Waldmann P, Sillanpää MJ. Bayesian analysis of genetic differentiation between populations. Genetics. 2003;163:367–374.

Beaumont MA, Zhang WY, Balding DJ. Approximate Bayesian computation in population genetics. Genetics. 2002;162:2025–2035.

Csilléry K, Blum MGB, Gaggiotti OE, Francois O. Approximate Bayesian computation (ABC) in practice. Trends Ecol Evol. 2010;25:410–418. https://doi.org/10.1016/j.tree.2010.04.001

Merzeau D, Di Giusto F, Comps B, Thiébaut B, Letouzey J, Cuguen J. The allozyme variants of beech (Fagus sylvatica L.): inheritance and application to a study of the mating system. Silvae Genet. 1989;38:195–201.

Müller-Starck G, Starke R. Inheritance of isoenzymes in European beech (Fagus sylvatica L.). J Hered. 1993;84:291–296.

Cornuet JM, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois R, et al. DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics. 2014;30:1187–1189. https://doi.org/10.1093/bioinformatics/btt763

Voelker RA, Schaffer HE, Mukai T. Spontaneous allozyme mutations in Drosophila melanogaster: rate of occurrence and nature of the mutants. Genetics. 1980;94:961–968.

Baer CF, Miyamoto MM, Denver DR. Mutation rate variation in multicellular eukaryotes: causes and consequences. Nat Rev Genet. 2007;8:619–631. https://doi.org/10.1038/nrg2158

Houston Durrant T, de Rigo D, Caudullo G. Fagus sylvatica and other beeches in Europe: distribution, habitat, usage and threats. In: San-Miguel-Ayanz J, de Rigo D, Caudullo G, Houston Durrant T, Mauri A, editors. European atlas of forest tree species. Luxembourg: Publications Office of the European Union; 2016. p. e012b90+.

Korpeľ Š. Die Urwälder der Westkarpaten. Jena: Gustav Fischer Verlag; 1995.

Kimura M, Crow J. The number of alleles that can be maintained in a finite population. Genetics. 1964;49:725–738.

Ohta T, Kimura M. A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genet Res. 1973;22:201–204. https://doi.org/10.1017/S0016672300012994

Barbadilla A, King LM, Lewontin RC. What does electrophoretic variation tell us about protein variation? Mol Biol Evol. 1996;13(2):427–432. https://doi.org/10.1093/oxfordjournals.molbev.a025602

Brown AHD, Marshall DR, Weir BS. Current status of the charge state model for protein polymorphism. In: Gibson JB, Oakeshot JG, editors. Genetic studies of Drosophila populations. Canberra: Australian National University Press; 1981. p. 15–43.

Richardson BJ, Baverstock PR, Adams M. Allozyme electrophoresis: a handbook for animal systematics and population studies. Sydney: Academic Press; 1986.

Demesure B, Comps B, Petit R. Phylogeography of the common beech (Fagus sylvatica L.) in Europe inferred by restriction studies of PCR amplified chloroplast DNA fragments. Evolution. 1996;50:2515–2520. https://doi.org/10.1111/j.1558-5646.1996.tb03638.x

Gailing O, von Wühlisch G. Nuclear markers (AFLPs) and chloroplast microsatellites differ between Fagus sylvatica and F. orientalis. Silvae Genet. 2004;53:105–110. https://doi.org/10.1515/sg-2004-0019

Kvaček Z, Walther H. Revision der mitteleuropäischen tertiären Fagaceen nach blattepidermalen Charakteristiken. IV. Teil Fagus Linné. Feddes Repert. 1991;102:471–534. https://doi.org/10.1002/fedr.19911020702

Tralau H. Die spättertiären Fagus-Arten Europas. Botaniska Notiser. 1962;115:147–177.

Denk T. Phylogeny of Fagus L. (Fagaceae) based on morphological data. Plant Syst Evol. 2003;240:55–81. https://doi.org/10.1007/s00606-003-0018-x

Gerasimenko N. Environmental changes in the Crimean mountains during the Last Interglacial–middle pleniglacial as recorded by pollen and lithopedology. Quat Int. 2007;164–165:207–220. https://doi.org/10.1016/j.quaint.2006.12.018

Cordova CE, Gerasimenko NP, Lehman PH, Kliukin AA. Late Pleistocene and Holocene paleoenvironments of Crimea: pollen, soils, geomorphology, and geoarchaeology. In: Buynevich IV, Yanko-Hombach V, Gilbert AS, Martin RE, editors. Geology and geoarchaeology of the Black Sea Region: beyond the flood hypothesis. Boulder, CO: Geological Society of America; 2011. p. 133–164. (Special Papers, Geological Society of America; vol 473). https://doi.org/10.1130/2011.2473(09)

Zubakov VA. Climatostratigraphic scheme of the Black-Sea Pleistocene and its correlation with the oxygen isotope scale and glacial events. Quat Res. 1988;29:1–24. https://doi.org/10.1016/0033-5894(88)90067-1

Dodonov AE, Zhou LP, Markova AK, Tchepalyga AL, Trubikhin VM, Aleksandrovski AL, et al. Middle-Upper Pleistocene bio-climatic and magnetic records of the northern Black Sea coastal area. Quat Int. 2006;149:44–54. https://doi.org/10.1016/j.quaint.2005.11.017

Gömöry D, Paule L, Shvadchak IM, Popescu F, Sulkowska M, Hynek V, et al. Spatial patterns of the genetic differentiation in European beech (Fagus sylvatica L.) at allozyme loci in the Carpathians and the adjacent regions. Silvae Genet. 2003;52:78–83.

Magri D, Vendramin GG, Comps B, Dupanloup I, Geburek T, Gömöry D, et al. Palaeobotanical and genetic data outline the Quaternary history of European beech populations. New Phytol. 2006;171:199–222. https://doi.org/10.1111/j.1469-8137.2006.01740.x

Peters R. Beech forests. Dordrecht: Springer Science & Business Media; 1997. (Geobotany; vol 24). https://doi.org/10.1007/978-94-015-8794-5

Paffetti D, Vettori C, Caramelli D, Vernesi C, Lari M, Paganelli A, et al. Unexpected presence of Fagus orientalis complex in Italy as inferred from 45,000-year-old DNA pollen samples from Venice lagoon. BMC Evol Biol. 2007;7(2 suppl):S6. https://doi.org/10.1186/1471-2148-7-S2-S6