Cretaceous and Paleogene Fagaceae from North America and Greenland: evidence for a Late Cretaceous split between Fagus and the remaining Fagaceae

Open access


Modern lineages of the beech family, Fagaceae, one of the most important north-temperate families of woody flowering plants, have been traced back to the early Eocene. In contrast, molecular differentiation patterns indicate that the Fagus lineage, Fagoideae, with a single modern genus, evolved much earlier than the remaining lineages within Fagaceae (Trigonobalanoideae, Castaneoideae, Quercoideae). The minimum age for this primary split in the Fagaceae has been estimated as 80 ± 20 Ma (i.e. Late Cretaceous) in recently published, time-calibrated phylogenetic trees including all Fagales. Here, we report fagaceous fossils from the Campanian of Wyoming (82-81 Ma; Eagle Formation [Fm]), the Danian of western Greenland (64-62 Ma; Agatdal Fm), and the middle Eocene of British Columbia (ca 48 Ma; Princeton Chert), and compare them to the Fagaceae diversity of the recently studied middle Eocene Hareøen Fm of western Greenland (42-40 Ma). The studied assemblages confirm that the Fagus lineage (= Fagoideae) and the remainder of modern Fagaceae were diverged by the middle Late Cretaceous, together with the extinct Fagaceae lineage(s) of Eotrigonobalanus and the newly recognised genus Paraquercus, a unique pollen morph with similarities to both Eotrigonobalanus and Quercus. The new records push back the origin of (modern) Fagus by 10 Ma and that of the earliest Fagoideae by 30 Ma. The earliest Fagoideae pollen from the Campanian of North America differs from its single modern genus Fagus by its markedly thicker pollen wall, a feature also seen in fossil and extant Castaneoideae. This suggests that a thick type 1 foot layer is also the plesiomorphic feature in Fagoideae although not seen in any of its living representatives. The Danian Fagus pollen of Greenland differs in size from those of modern species but is highly similar to that of the western North American early Eocene F. langevinii, the oldest known beech so far. Together with the Quercus pollen record, absent in the Campanian and Danian formations but represented by several types by the middle Eocene, this confirms recent dating estimates focussing on the genera Fagus and Quercus, while rejecting estimates from all-Fagales-dated trees as too young. The basic Castaneoideae pollen type, still found in species of all five extant genera of this putatively paraphyletic subfamily, represents the ancestral pollen type of most (modern) Fagaceae (Trigonobalanoideae, Castaneoideae, Quercoideae).

ACOSTA M.C. & PREMOLI A.C. 2010. Evidence of chloroplast capture in South American Nothofagus (subgenus Nothofagus, Nothofagaceae). Mol. Phylogenet. Evol., 54: 235-242.

APG III 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc., 161: 105-121.

BOUCHAL J., ZETTER R., GRÍMSSON F. & DENK T. 2014. Evolutionary trends and ecological differentiation in early Cenozoic Fagaceae of western North America. Am. J. Bot., 101: 1332-1349.

BOULTER M.C. & KVAČEK Z. 1989. The Palaeocene flora of the Isle of Mull. Palaeont. Assoc. London Spec. Pap. Palaeont., 42: 1-149.

BROWN R.W. 1962. Paleocene floras of the Rocky Mountains and Great Plains. U.S. Geol. Surv. Prof. Paper, 375: 1-119.

COHEN K.M., FINNEY S., GIBBARD P.L. & FAN J.-X. 2013, updated. The ICS international Chronostratigraphic Chart. Episodes, 36: 199-204.

CREPET W.L. & NIXON K.C. 1989. Earliest megafossil evidence of Fagaceae: phylogenetic and biogeographic implications. Am. J. Bot., 76: 842-855.

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 South Western Asia and its phylogenetic implications. Doc. Nat., 150: 1-72.

DENK T. & DILLHOFF R.M. 2005. Ulmus leaves and fruits from the Early-Middle Eocene of northwestern North America: Systematics and implications of characters evolution within Ulmaceae. Can. J. Bot., 83: 1663-1681.

DENK T. & GRIMM G.W. 2009a. The biogeographic history of beech trees. Rev. Palaeobot. Palynol., 158: 83-100.

DENK T. & GRIMM G.W. 2009b. Significance of pollen characteristics for infrageneric classification and phylogeny in Quercus (Fagaceae). Int. J. Plant Sci., 170: 926-940.

DENK T. & GRIMM G.W. 2010. The oaks of western Eurasia: traditional classifications and evidence from two nuclear markers. Taxon, 59: 351-366.

DENK T. & TEKLEVA M.V. 2014. Pollen morphology and ultrastructure of Quercus with focus on Group Ilex (= Quercus Subgenus Heterobalanus (Oerst.) Menitsky): implications for oak systematics and evolution. Grana, 53: 255-282.

DENK T., GRIMM G.W. & HEMLEBEN V. 2005. Patterns of molecular and morphological differentiation in Fagus: implications for phylogeny. Am. J. Bot., 92: 1006-1016.

DENK T., GRÍMSSON F. & ZETTER R. 2012. Fagaceae from the early Oligocene of Central Europe: persisting New World and emerging Old World biogeographic links. Rev. Palaeobot. Palynol., 169: 7-20.

DENK T., GRÍMSSON F., ZETTER R. & SÍMONARSON L.A. 2011. Late Cainozoic Floras of Iceland: 15 Million Years of Vegetation and Climate History in the Northern North Atlantic. Topics in Geobiology, vol. 35. Springer, Heidelberg, New York.

DILLHOFF R.M., LEOPOLD E.B. & MANCHESTER S.R. 2005. The McAbee flora of British Columbia and its relation to the early-middle Eocene Okanagan Highlands flora of the Pacific Northwest. Can. J. Earth Sci., 42: 151-166.

ELLIS B., DALY D.C., HICKEY L.J., JOHNSON K.R., MITCHELL J.D., WILF P. & WING S.L. 2009. Manual of Leaf Architecture. Cornell University Press, New York.

FUJII N., TOMARU N., OKUYAMA K., KOIKE T., MIKAMI T. & UEDA K. 2002. Chloroplast DNA phylogeography of Fagus crenata (Fagaceae) in Japan. Plant Syst. Evol., 232: 21-33.

GNILOVSKAYA A.A. & GOLOVNEVA L.B. 2016. Fagaceous foliage from the latest Cretaceous of the Koryak Upland (northeastern Russia) and its implications for the evolutionary history of the Fagaceae. Rev. Palaeobot. Palynol., 228: 57-66.

GRIMM G.W. & DENK T. 2010. The reticulate origin of modern plane trees (Platanus, Platanaceae) - a nuclear marker puzzle. Taxon, 59: 134-147.

GRÍMSSOF., DENK T., ZETTER R. 2008. Pollen, fruits, and leaves of Tetracentron (Trochodendraceae) from the Cainozoic of Iceland and western North America and their palaeobiogeographic implications. Grana, 47: 1-14.

GRÍMSSON F., ZETTER R., BAAL C. 2011. Combined LM and SEM study of the Middle Miocene (Sarmatian) palynoflora from the Lavanttal Basin, Austria: Part I. Bryophyta, Lycopodiophyta, Pteridophyta, Ginkgophyta, and Gnetophyta. Grana, 50: 102-128.

GRÍMSSON F., GRIMM G.W., MELLER B., BOUCHAL J.M. & ZETTER R. 2016a. Combined LM and SEM study of the Middle Miocene (Sarmatian) palynoflora from the Lavanttal Basin, Austria: Part IV. Magnoliophyta 2 - Fagales to Rosales. Grana, 55: 101-163.

GRÍMSSON F., PEDERSEN G.K., GRIMM G.W., ZETTER R. 2016b. A revised stratigraphy for the Paleocene Agatdalen flora (Nuussuaq Peninsula, western Greenland): correlating fossiliferous outcrops, macrofossils and palynological samples from phosphoritic nodules. Acta Palaeobot., 56(2): 307-327.

GRÍMSSON F., ZETTER R., LABANDEIRA C.C., ENGEL M.S. & WAPPLER T. 2016c. Taxonomic description of in situ bee pollen from the middle Eocene of Germany. Grana. DOI: 10.1080/00173134.2015.1108997.

GRÍMSSON F., ZETTER R., GRIMM G.W., PEDERSEN G.K., PEDERSEN A.K. & DENK T. 2015. Fagaceae pollen from the early Cenozoic of West Greenland: revisiting Engler’s and Chaney’s Arcto-Tertiary hypotheses. Plant Syst. Evol., 301: 809-832.

HARADA K., TAMAKI K., KAMIYA K. & TAKECHI Y. 2003. Pollen morphology observed by scanning electron microscopy on Japanese Fagaceae species and molecular phylogeny. Bull. Ehime Univ. For., 42: 1-19.

HEATH T.A., HUELSENBECK J.P. & STADLER T. 2014. The fossilized birth-death process for coherent calibration of divergence-time estimates. Proc. Nat. Acad. Sci., 111: E2957-E2966.

HEENAN P.B. & SMISSEN R.D. 2013. Revised circumscription of Nothofagus and recognition of the segregate genera Fuscospora, Lophozonia, and Trisyngyne (Nothofagaceae). Phytotaxa, 146: 1-31.

HEER O. 1868. Flora fossilis arctica 1. Die Fossile Flora der Polarländer enthaltend die in Nordgrönland, auf der Melville-Insel, im Banksland, am Mackenzie, in Island und in Spitzbergen entdeckten fossilen Pflanzen. F. Schulthess, Zürich.

HEER O. 1868-1883. Flora Fossilis Arctica, vol. 1-7. Kongliga Vetenskaps Akademiens Handlingar, Stockholm.

HEER O. 1883. Flora fossilis arctica 7. Die fossile Flora der Polarländer. Enthaltend: Den zweiten Theil der fossilen Flora Grönlands. J. Wurster & Comp., Zürich.

HESSE M., HALBRITTER H., ZETTER R., WEBER M., BUCHNER R., FROSCH-RADIVO A. & ULRICH S. 2009. Pollen terminology - An illustrated handbook. Springer, Wien, New York.

HICKEY L.J. 1973. Classification of the architecture of dicotyledonous leaves. Amer. J. Bot., 60: 17-33.

HICKS J.F. 1993. Chrono-stratigraphic analysis of the foreland basin sediments of the latest Cretaceous, Western Interior, U.S.A. Ph.D. Thesis. Yale University, New Haven, Connecticut.

HIPP A.L., EATON D.A.R., CAVENDER-BARES J., FITZEK E., NIPPER R. & MANOS P.S. 2014. A framework phylogeny of the American oak clade based on sequenced RAD data. PLoS ONE, 9: e93975.


HOFMANN C.-C. 2010. Microstructure of Fagaceae pollen from Austria (Paleocene/Eocene boundary) and Hainan Island (?middle Eocene). 8th European Palaeobotany-Palynology Conference: 119.

HOFMANN C.-C. & ZETTER R. 2007. Upper Cretaceous pollen flora from the Vilui Basin, Siberia: Circumpolar and endemic Aquilapollenites, Manicorpus, and Azonia. Grana, 46: 227-249.

HOFMANN C.-C. & ZETTER R. 2010. Upper Cretaceous sulcate pollen from the Timerdyakh Formation, Vilui Basin (Siberia). Grana, 49: 170-193.

HOFMANN C.-C., MOHAMED O. & EGGER H. 2011. A new terrestrial palynoflora from the Palaeocene/ Eocene boundary in the northwestern Tethyan realm (St. Pankraz, Austria). Rev. Palaeobot. Palynol., 166: 295-310.

HUBERT F., GRIMM G.W., JOUSSELIN E., BERRY V., FRANC A. & KREMER A. 2014. Multiple nuclear genes stabilize the phylogenetic backbone of the genus Quercus. Syst. Biodivers., 12: 405-423.

KANNO M., YOKOYAMA J., SUYAMA Y., OHYAMA M., ITOH T. & SUZUKI M. 2004. Geographical distribution of two haplotypes of chloroplast DNA in four oak species (Quercus) in Japan. J. Plant Res., 117: 311-317.

KOCH B.E. 1963. Fossil plants from the lower Paleocene of the Agatdalen (Angmârtussut) area, central Nûgssuaq Peninsula, northwest Greenland. Medd. Grønl. [Bull. Grønl. Geol. Unders.], 172[38]: 1-120.

KOHLMAN-ADAMSKA A. & ZIEMBIŃSKA-TWORZYDŁO M. 2000. Morphological variability and botanical affinity of some species of the genus Tricolporopollenites Pf. et Thoms. from the Middle Miocene Lignite association at Lubstów (Konin region - Central Poland). Acta Palaeobot., 40: 49-71.

KVAČEK Z. & WALTHER H. 1988. Revision der mitteleuropäischen tertiären Fagaceen nach blattepidermalen Charakteristiken II. Teil - Castanopsis (D.Don) Spach, Trigonobalanopsis Kvaček & Walther. Feddes Repert., 99: 395-418.

KVAČEK Z. & WALTHER H. 1989. Palaeobotanical studies in Fagaceae of the European Tertiary. Plant Syst. Evol., 162: 213-229.

LARSEN L.M., PEDERSEN A.K., TEGNER C., DUNCAN R.A., HALD N. & LARSEN J.G. 2015. The age of Tertiary volcanic rocks on the West Greenland continental margin: volcanic evolution and event correlation to other parts of the North Atlantic Igneous Province. Geol. Mag., 153: 487-511.

LARSON-JOHNSON K. 2016. Phylogenetic investigation of the complex evolutionary history of dispersal mode and diversification rates across living and fossil Fagales. New Phytol., 209: 418-435.

LI R.-Q., CHEN Z.-D., LU A.-M., SOLTIS D.E., SOLTIS P.S. & MANOS P.S. 2004. Phylogenetic relationships in Fagales based on DNA sequences from three genomes. Int. J. Plant Sci., 165: 311-324.

MANCHESTER S.R. 1999. Biogeographical relationships of North American Tertiary floras. Ann. Missouri Bot. Gard., 86: 472-522.

MANCHESTER S.R. & CRANE P.R. 1983. Attached leaves, inflorescences, and fruits of Fagopsis, an extinct genus of fagaceous affinity from the Oligocene Florissant flora of Colorado, U.S.A. Am. J. Bot., 70: 1147-1164.

MANCHESTER S.R. & DILLHOFF R.M. 2004. Fagus (Fagaceae) fruits, foliage, and pollen from the Middle Eocene of Pacific Northwestern North America. Can. J. Bot., 82: 1509-1517.

MANCHESTER S.R., GRÍMSSON F. & ZETTER R. 2015. Assessing the fossil record of asterids in the context of our current phylogenetic framework. Ann. Missouri Bot. Gard., 100: 329-363.

MANOS P.S., ZHOU Z.K. & CANNON C.H. 2001. Systematics of Fagaceae: Phylogenetic tests of reproductive trait evolution. Int. J. Plant Sci., 162: 1361-1379.

MANOS P.S., CANNON C.H. & OH S.-H. 2008. Phylogenetic relationships and taxonomic status of the paleoendemic Fagaceae of Western North America: recognition of a new genus, Notholithocarpus. Madroño 55: 181-190.

MELLER B., KOVAR-EDER J. & ZETTER R. 1999. Lower Miocene diaspore, leaf and palynomorph assemblages from the base of the lignite-bearing sequence in the opencast mine Oberdorf, N Voitsberg (Styria, Austria) as an indication of a “Younger Mastixioid” vegetation. Palaeontogr. B, 252: 123-179.

MIYOSHI N., FUJIKI T. & KIMURA H. 2011. Pollen Flora of Japan. Hokkaido University Press, Sapporo.

MOSS P.T., GREENWOOD D.R. & ARCHIBALD S.B. 2005. Regional and local vegetation community dynamics of the Eocene Okanagan Highlands (British Columbia - Washington State) from palynology. Can. J. Earth Sci., 42: 187-204.

MUSTOE G.E. 2011. Cyclic sedimentation in the Eocene Allenby Formation of south-central British Columbia and the origin of the Princeton Chert fossil beds. Can. J. Earth Sci., 48: 25-43.

NEOPHYTOU C., DOUNAVI A., FINK S. & ARAVANOPOULOS F.A. 2010. Interfertile oaks in an island environment: I. High nuclear genetic differentiation and high degree of chloroplast DNA sharing between Q. alnifolia and Q. coccifera in Cyprus. A multipopulation study. Eur. J. Forest Res., 130: 543-555.

NIXON K.C. & CREPET W.L. 1989. Trigonobalanus (Fagaceae): taxonomic status and phylogenetic relationships. Am. J. Bot., 76: 828-841.

OH S.-H. & MANOS P.S. 2008. Molecular phylogenetics and cupule evolution in Fagaceae as inferred from nuclear CRABS CLAW sequences. Taxon, 57: 434-451.

PALAMAREV E. & MAI D.H. 1998. Die paläogenen Fagaceae in Europa: Artenvielfalt und Leitlinien ihrer Entwicklungsgeschichte. Acta Palaeobot., 38: 227-299.

PRAGLOWSKI J. 1982. Fagaceae L. Fagoideae. World Pollen and Spore Flora, 11: 1-28.

PRAGLOWSKI J. 1984. Fagaceae Dumort. Castaneoideae Oerst. World Pollen and Spore Flora, 13: 1-21.

PREMOLI A.C., MATHIASEN P., ACOSTA M.C. & RAMOS V.A. 2012. Phylogeographically concordant chloroplast DNA divergence in sympatric Nothofagus s.s. How deep can it be? New Phytol., 193: 261-275.

PUNT W., HOEN P., BLACKMORE S. & LE THOMAS A. 2007. Glossary of pollen and spore terminology. Rev. Palaeobot. Palynol., 143: 1-81.

READ P.B. 2000. Geology and industrial minerals of the Tertiary basins, British Columbia. GeoFiles: 110.

RENNER S.S., GRIMM G.W., KAPLI P. & DENK T. 2016. Species relationships and divergence times in beeches: New insights from the inclusion of 53 young and old fossils in a birth-death clock model. Phil. Trans. Roy. Soc. B., 371: 20150135.

SAUQUET H., HO S.Y., GANDOLFO M.A., JORDAN G.J., WILF P., CANTRILL D.J., BAYLY M.J., BROMHAM L., BROWN G.K., CARPENTER R.J., LEE D.M., MURPHY D.J., SNIDERMAN J.M. & UDOVICIC F. 2012. Testing the impact of calibration on molecular divergence times using a fossil- rich group: the case of Nothofagus (Fagales). Syst. Biol., 61: 289-313.

SHEN C.F. 1992. A monograph of the genus Fagus Thurn. ex L. (Fagaceae). Ph. D. Thesis. City University of New York, New York.

SIMEONE M.C., PIREDDA R., PAPINI A., VESSELLA F. & SCHIRONE B. 2013. Application of plastid and nuclear markers to DNA barcoding of Euro-Mediterranean oaks (Quercus, Fagaceae): problems, prospects and phylogenetic implications. Bot. J. Linn. Soc.: 478-499.

SIMEONE M.C., GRIMM G.W., PAPINI A., VESSELLA F., CARDONI S., TORDONI E., PIREDDA R., FRANC A. & DENK T. 2016a. Plastome divergence in Fagales. Supplemental information to: Simeone et al., Plastome data reveal multiple geographic origins of Quercus Group Ilex. PeerJ. DOI: 10.7717/peerj.1897/supp-2.

SIMEONE M.C., GRIMM G.W., PAPINI A., VESSELLA F., CARDONI S., TORDONI E., PIREDDA R., FRANC A. & DENK T. 2016b. Plastome data reveal multiple geographic origins of Quercus Group Ilex. PeerJ, 4: e1897. DOI: 10.7717/peerj.1897.

SIMS H.J., HERENDEEN P.S. & CRANE P.R. 1998. New genus of fossil Fagaceae from the Santonian (Late Cretaceous) of Central Georgia, U.S.A. Int. J. Plant Sci., 159: 391-404.

SMITH S.Y. & STOCKEY R.A. 2007. Establishing a fossil record for the perianthless Piperales: Saururus tuckerae sp. nov. (Saururaceae) from the Middle Eocene Princeton Chert. Am. J. Bot., 94: 1643-1657. SOLOMON A.M. 1983a. Pollen morphology and plant taxonomy of red oaks in eastern North America. Am. J. Bot., 70: 495-507.

SOLOMON A.M. 1983b. Pollen morphology and plant taxonomy of white oaks in eastern North America. Am. J. Bot., 70: 481-492.

STEVENS P.F. 2001 onwards. Angiosperm Phylogeny Website. Version 8, June 2007 [and more or less continuously updated since]. Available from: Accessed 19/07/2014.

STUCHLIK L., ZIEMBÍNSKA-TWORZYDŁO M. & KOHLMAN-ADAMSKA A. 2007. Botanical affinity of some Neogene sporomorphs and nomenclatural problems. Acta Palaeobot., 47: 291-311.

TAKAHASHI M., FRIIS E.M., HERENDEEN P.S. & CRANE P.R. 2008. Fossil flowers of Fagales from the Kamikitaba locality (Early Coniacian; Late Cretaceous) of Northeastern Japan. Int. J. Plant Sci., 169: 899-907.

VAN BOSKIRK M.C. 1998. The flora of the Eagle Formation and its significance for Late Cretaceous floristic evolution. Ph.D. Thesis. Yale University, New Haven, Connecticut.

VELITZELOS D., BOUCHAL J.M. & DENK T. 2014. Review of the Cenozoic floras and vegetation of Greece. Rev. Palaeobot. Palynol., 204: 56-117. DOI: 10.1016/j.revpalbo.2014.02.006.

WALTHER H. & ZETTER R. 1993. Zur Entwicklung der paläogenen Fagaceae Mitteleuropas. Palaeontogr. B, 230: 183-194.

WANG P.-L. & CHANG K.-T. 1988. On the pollen morphology and systematic position of Trigonobalanus doichangensis. Acta Phytotax. Sin., 26: 44-46.

WANG P.-L., PU F.-T. & ZHENG Z.-H. 1998. Palynological evidence for taxonomy of Trigonobalanus (Fagaceae). Acta Phytotax. Sin., 36: 238-241.

WANG P. & PU F. 2004. Pollen morphology and biogeography of Fagaceae. Guangdong Science and Technology Press, Guangzhou.

XIANG X.-G., WANG W., LI R.-Q., LIN L., LIU Y., ZHOU Z.-K., LI Z.-Y. & CHEN Z.-D. 2014. Largescale phylogenetic analyses reveal fagalean diversification promoted by the interplay of diaspores and environments in the Paleogene. Perspect. Plant Ecol. Evol. Syst., 16: 101-110.

XING Y., ONSTEIN R.E., CARTER R.J., STADLER T. & LINDER H.P. 2014. Fossils and large molecular phylogeny show that the evolution of species richness, generic diversity, and turnover rates are disconnected. Evolution, 68: 2821-2832.

ZETTER R. 1989. Methodik und Bedeutung einer routinemäßig kombinierten lichtmikroskopischen und rasterelektonenmikroskopischen Untersuchung fossiler Mikrofloren. Cour. Forschungsinst. Senckenberg, 109: 41-50.

ZHANG Z.Y., WU R., WANG Q., ZHANG Z.R., LOPEZPUJOL J., FAN D.M. & LI D.Z. 2013. Comparative phylogeography of two sympatric beeches in subtropical China: Species-specific geographic mosaic of lineages. Ecology and Evolution, 3: 4461-4472. DOI: Doi 10.1002/Ece3.829.

Acta Palaeobotanica

The Journal of W. Szafer Institute of Botany of Polish Academy of Sciences

Journal Information

CiteScore 2017: 1.07

SCImago Journal Rank (SJR) 2017: 0.361
Source Normalized Impact per Paper (SNIP) 2017: 0.917

Cited By


All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 302 302 35
PDF Downloads 114 114 14