The Colchic region as refuge for relict tree lineages: cryptic speciation in field maples

ITS sequences from isolated populations of Acer in the Colchic region allow direct assumptions about the origin, evolution, and radiation of one of the most abundant West Eurasian tree species, Acer campestre L., the field maple. We inferred the molecular evolution of the internal transcribed spacers ITS1 and ITS2 of the nuclear-encoded 35S rDNA cistron in Acer campestre using a range of methods including sequence- and distance-based phylogenetic networks and motif analyses. The data basis for our inference are 344 sequenced clones from 51 individuals of A. campestre, essentially covering the modern distribution range of the species, and 27 individuals representing other species of Acer section Platanoidea. Our results indicate that Acer campestre comprises 2 cryptic species, 1 of which is confined to North-East Turkey and South-West Georgia (ancient Colchis region). Detailed analysis shows that the Colchic genotype is generally more similar to other species of the section than the main genotype of Acer campestre sampled from North Turkey to the Pyrenees. In the light of the fossil record and general differentiation patterns in West Eurasian Acer, we conclude that the Colchic genotype represents a survivor of the initial radiation within section Platanoidea, predating the formation of modern species.

Anahtar Kelimeler:

Acer campestre, Acer orthocampestre sp. nov., biogeography, Colchis, cryptic speciation, East Asia, genotaxonomy, ITS region, phylogenetic networks, West Eurasia

The Colchic region as refuge for relict tree lineages: cryptic speciation in field maples

Keywords:

Acer campestre, Acer orthocampestre sp. nov., biogeography, Colchis, cryptic speciation, East Asia, genotaxonomy, ITS region, phylogenetic networks, West Eurasia,

PDF

___

Abdelaziz M, Lorite J, Jesşs MPA, Herrador MB, Perfectti F, Gómez JM (2011). Using complementary techniques to distinguish cryptic species: new Erysimum (Brassicaceae) species from North Africa. Am J Bot 98: 1049–1060.
Anderberg A, Anderberg AL (2010). Den virtuella floran. Naturhistoriska riksmuseet. Website http://linnaeus.nrm.se/ flora/ [last accessed 14/05/2014] (in Swedish).
Bandelt HJ, Forster P, Röhl A (1999). Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16: 37–48.
Bandelt HJ, Forster P, Sykes BC, Richards MB (1995). Mitochondrial portraits of human populations using median networks. Genetics 141: 743–753.
Bandelt HJ, Macaulay V, Richards M (2000). Median Networks: speedy construction and greedy reduction, one simulation, and two case studies from human mtDNA. Mol Phylogenet Evol 16: 8–28.
Borsch T, Ortuño Limarino T, Nee MH (2011). Phylogenetics of the neotropical liana genus Pedersenia (Amaranthaceae: Gomphrenoideae) and discovery of a new species from Bolivia based on molecules and morphology. Willdenowia 41: 5–14.
Browicz K, Zieliński J (1982). Chorology of Trees and Shrubs in South-West Asia and Adjacent Regions. Warsaw, Poznan: Polish Scientific Publishers.
Bryant D, Moulton V (2002). NeighborNet: an agglomerative method for the construction of planar phylogenetic networks. In: Guigó R, Gusfield D, editors. Algorithms in Bioinformatics, Second International Workshop WABI, Rome, Italy. Berlin, Germany: Springer Verlag, pp. 375–391.
Bryant D, Moulton V (2004). Neighbor-Net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21: 255–265.
Christie C, Kozlowski G, Frey D, Bétrisey S, Maharramova E, Garfi G, Pirintsos S, Naciri Y (2014). Footprints of past intensive diversification and structuring in the genus Zelkova (Ulmaceae) in south-western Eurasia. J Biogeogr 41: 1081–1093.
de Jong PC (1976). Flowering and sex expression in Acer L. A biosystematic study. Meded Landb Univ Wageningen 76: 1–201.
de Jong PC (1994). Taxonomy and reproductive biology of maples. In: van Gelderen DM, de Jong PC, Oterdoom HJ, editors. Maples of the World. Portland, OR, USA: Timber Press, pp. 69–104. de Jong PC (2002). Worldwide maple diversity. In: Wiegrefe SJ, Angus H, Otis D, Gregorey P, editors. International Maple Symposion 2002. Gloucestershire, UK: The National Arboretum Westonbirt.
Delendick TJ (1981). A Systematic Review of the Aceraceae. New York, NY, USA: City University of New York.
Denk T (1999a). The taxonomy of Fagus in West Eurasia, 1: Fagus sylvatica subsp. orientalis (= F. orientalis). Feddes Repert 110: 177–200.
Denk T (1999b). The taxonomy of Fagus in West Eurasia, 2: Fagus sylvatica subsp. sylvatica. Feddes Repert 110: 381–412.
Denk T (2003). Phylogeny of Fagus L. (Fagaceae) based on morphological data. Plant Syst Evol 240: 55–81.
Denk T (2004). Revision of Fagus from the Cenozoic of Europe and southwestern Asia and its phylogenetic implications. Doc Nat 150: 1–72.
Denk T, Frotzler N, Davitashvili N (2001). Vegetational patterns and distribution of relict taxa in humid temperate forests and wetlands of Georgia (Transcaucasia). Biol J Linn Soc 72: 287– 332.
Denk T, Grimm GW (2005). Phylogeny and biogeography of Zelkova (Ulmaceae sensu stricto) as inferred from leaf morphology, ITS sequence data and the fossil record. Bot J Linn Soc 147: 129–157.
Denk T, Grimm GW (2009). The biogeographic history of beech trees. Rev Palaeobot Palynol 158: 83–100.
Denk T, Grimm GW (2010). The oaks of western Eurasia: traditional classifications and evidence from two nuclear markers. Taxon 59: 351–366.
Denk T, Grimm GW, Hemleben V (2005). Patterns of molecular and morphological differentiation in Fagus: implications for phylogeny. Am J Bot 92: 1006–1016.
Denk T, Grimm G, Stögerer K, Langer M, Hemleben V (2002). The evolutionary history of Fagus in western Eurasia: Evidence from genes, morphology and the fossil record. Plant Syst Evol 232: 213–236.
Draper I, Hedenäs L, Grimm GW (2007). Molecular and morphological incongruence in European species of Isothecium (Bryophyta). Mol Phylogen Evol 42: 700–716.
Flora of China (2014). eFloras: Flora of China. Cambridge, MA: Missouri Botanical Garden and Harvard University Herbaria.
Gebhardt C, Ritter E, Debener T, Schachtschabel U, Walkemeier B, Uhrig H, Salamini F (1989). RFLP analysis and linkage mapping in Solanum tuberosum. Theor Appl Genet 78: 65–75.
Göker M, García-Blázquez G, Voglmayr H, Tellería MT, Martín MP (2009). Molecular taxonomy of phytopathogenic fungi: a case study in Peronospora. PLoS ONE 4: e6319.
Göker M, Grimm GW (2008). General functions to transform associate data to host data, and their use in phylogenetic inference from sequences with intra-individual variability. BMC Evol Biol 8: 86.
Gömöry D, Paule L (2010). Reticulate evolution patterns in western- Eurasian beeches. Bot Helvet 120: 63–74.
Greuter W, Burdet HM (1981). Fagus sylvatica ssp. orientalis (Lipsky) Greuter & Burdet. In: Greuter W, Raus T, editors. Med- Checklist Notulae, 4. Willdenowia 11: 271–280.
Grimm GW (2003). Tracing the Mode and Speed of Intrageneric Evolution - A Case Study of Genus Acer L. and Fagus L. Tübingen: Eberhard-Karls University. http://nbn-resolving.de/ urn:nbn:de:bsz:21-opus-15744.
Grimm GW, Denk T (2008). ITS evolution in Platanus: homoeologues, pseudogenes, and ancient hybridization. Ann Bot 101: 403–419.
Grimm GW, Denk T, Hemleben V (2007). Evolutionary history and systematic of Acer section Acer - a case study of low-level phylogenetics. Plant Syst Evol 267: 215–253.
Grimm GW, Renner SS, Stamatakis A, Hemleben V (2006). A nuclear ribosomal DNA phylogeny of Acer inferred with maximum likelihood, splits graphs, and motif analyses of 606 sequences. Evol Bioinform 2: 279–294.
Güner TH, Denk T (2012). The genus Mahonia in the Miocene of Turkey: taxonomy and biogeographic implications. Rev Palaebot Palynol 175: 32–46.
Holland B, Moulton V (2003). Consensus networks: a method for visualising incompatibilities in collections of trees. In: Benson G, Page R, editors. Algorithms in Bioinformatics: Third International Workshop WABI, Budapest, Hungary. Proceedings. Berlin, Germany: Springer Verlag, pp. 165–176.
Huson DH, Bryant D (2006). Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254–267.
Jobst J, King K, Hemleben V (1998). Molecular evolution of the internal transcribed spacers (ITS1 and ITS2) and phylogenetic relationships among species of Cucurbitaceae. Mol Phylogenet Evol 9: 204–219.
Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006). World map of the Köppen-Geiger climate classification updated. Meteorol Z 15: 259–263.
Krüssmann G (1960). Handbuch der Laubgehölze. Band 1. Berlin, Germany: Paul Parey (in German).
Kvaček Z, Erdei B (2001). Putative proteaceous elements of the Lomatites-type reinterpreted as new Berberis of the European Tertiary. Plant Syst Evol 226: 1–12.
Lewis PO (2001). A likelihood approach to estimating phylogeny from discrete morphological character data. Syst Biol 50: 913– 925.
Mai DH (1995). Tertiäre Vegetationsgeschichte Europas. Jena, Germany: Gustav Fischer Verlag (in German).
Mallet J (2007). Hybrid speciation. Nature 446: 279–283.
Manchester SR (1999). Biogeographical relationships of North American Tertiary floras. Ann MO Bot Gard 86: 472–522.
Murray AE (1978). Acer note no. 8. Kalmia 8: 17–20.
Murray AE (1982). Acer notes no. 11. Kalmia 12: 17.
Ogata K (1967). A systematic study of the genus Acer. Bull Tokyo Imp Univ Forest 63: 89–206.
Okuyama Y, Kato M (2009). Unveiling cryptic species diversity of flowering plants: successful biological species identification of Asian Mitella using nuclear ribosomal DNA sequence. BMC Evol Biol 9: 105.
Pattengale ND, Masoud A, Bininda-Emonds ORP, Moret BME, Stamatakis A (2009). How many bootstrap replicates are necessary? In: Batzoglou S, editor. RECOMB 2009. Berlin, Germany: Springer-Verlag, pp. 184–200.
Pax F (1885). Monographie der Gattung Acer. Bot Jahrb 6: 287–347 (in German).
Pax F (1886). Monographie der Gattung Acer. Bot Jahrb 7: 177–263 (in German).
Pfosser MF, Guzy-Wrobelska J, Sun BY, Stuessy TF, Sugawara T, Fujii N (2002). The origin of species of Acer (Sapindaceae) endemic to Ullung island, Korea. Syst Botany 27: 351–367.
Pojárkova AI (1933). Botanico-geographical survey of the maples of the USSR in connection with the history of the whole genus Acer L. Acta Inst Bot Acad Sci USSR Ser 1 1: 225–374.
Potts AJ, Hedderson TA, Grimm GW (2014). Constructing phylogenies in the presence of intra-individual site polymorphisms (2ISPs) with a focus on the nuclear ribosomal cistron. Syst Biol 63: 1–16.
Ramstein G, Fluteau F, Besse J, Joussaume S (1997). Effect of orogeny, plate motion, and land-sea distribution on Eurasian climate change over the past 30 million years. Nature 386: 788–795.
Razafimandimbison SG, Kellogg EA, Bremer B (2004). Recent origin and phylogenetic utility of divergent ITS putative pseudogenes: a case study from Naucleeae (Rubiaceae). Syst Biol 53: 177–192.
Renner SS, Grimm GW, Schneeweiss GM, Stuessy TF, Ricklefs RE (2008). Rooting and dating maples (Acer) with an uncorrelated- rates molecular clock: implications for North American/Asian disjunctions. Syst Biol 57: 795–808.
Rodriguez F, Oliver JL, Marin A, Medina JR (1990). The general stochastic model of nucleotide substitution. J Theor Biol 142: 485–501.
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.
Shen CF (1992). A Monograph of the Genus Fagus Thurn. ex L. (Fagaceae). New York, NY, USA: City University of New York.
Stamatakis A (2006). RAxML-VI-HPC: Maximum-Likelihood- based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.
Stamatakis A, Hoover P, Rougemont J (2008). A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57: 758–771.
Swofford DL (2002). PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods) 4.0 Beta. Sunderland, MA, USA: Sinauer Associates.
Tanai T (1983). Revisions of tertiary Acer from East Asia. J Fac Sci Hokkaido Univ Geol Mineral 20: 291–390.
Torres RA, Ganal M, Hemleben V (1990). GC balance in the internal transcribed spacers ITS1 and ITS2 of nuclear ribosomal DNA. J Mol Evol 30: 170–181.
van Gelderen DM, de Jong PC, Oterdoom HJ (1994). Maples of the World. Portland, OR, USA: Timber Press.
Velitzelos D, Bouchal JM, Denk T (2014). Review of the Cenozoic floras and vegetation of Greece. Rev Palaeobot Palynol 204: 56–117.
Walter H (1973). Vegetation of the Earth in Relation to the Climate and the Eco-physiological Conditions. New York, NY, USA: Springer Verlag.
Walther H (1972). Studien über tertiäre Acer Mitteleuropas. Abh Staatl Mus Mineral Geol Dresden 19: 1–309 (in German).
Weiner AKM, Weinkauf MFG, Kurasawa A, Darling KF, Kučera M, Grimm GW (2014). Biogeography of cryptic species in a marine plankton lineage shaped by niche incumbency and historical contingency. PLoS ONE 9: e92148.
Xu T, Chen Y, de Jong PC, Oterdoom HJ, Chang C-S (2008). Acer Linnaeus, Sp. Pl. 2: 1054. 1753. In: Wu Z, Raven PH, Hong D, editors. Flora of China, Vol. 11: Oxalidaceae through Aceraceae. St. Louis, MO, USA: Missouri Botanical Garden Press, pp. 516–553.
Yaltirik F (1967). Contribution to the taxonomy of woody plants in Turkey. Notes Roy Bot Gard Edinb 28: 9–10.
Yatabe Y, Murakami N (2003). Recognition of cryptic species in the Asplenium nidus complex using molecular data — a progress report. Telopea 10: 487–496.