Advertisement

Tree Genetics & Genomes

, 13:3 | Cite as

Phylogeographic structuring of plastome diversity in Mediterranean oaks (Quercus Group Ilex, Fagaceae)

  • Martina Vitelli
  • Federico Vessella
  • Simone Cardoni
  • Paola Pollegioni
  • Thomas Denk
  • Guido W. Grimm
  • Marco Cosimo Simeone
Original Article
Part of the following topical collections:
  1. Germplasm Diversity

Abstract

Oaks of Quercus Group Ilex are emblematic components of the Mediterranean landscapes and the full extent of their diversity in a geographic context is still poorly assessed. In order to detail differentiation patterns within Group Ilex and to illuminate causes and circumstances that underlie the distribution of its lineages, we examined plastome differentiation in the four species currently representing this oak group across the Mediterranean Basin (Quercus ilex, Quercus coccifera, Quercus aucheri, Quercus alnifolia). Plastid DNA variation was explored with three markers on 124 individuals and spatial analyses were performed with phylogenetic and landscape genetics approaches. A strong geographic sorting, entirely decoupled from species boundaries, was found. Spatial coincidences with phylogenetic splits highlights the presence of four geographic regions (the Middle East, the Aegean region, the central and the western Mediterranean) characterised by different degrees of isolation. Distinct sub-regional structures were identified. Inter- and intra-lineage divergence patterns appear to reflect the complex orogeny of the Mediterranean region and Pleistocene climatic oscillations, while a few widespread haplotypes might represent the remnants of the ancestral Group Ilex range. Regional differentiation in this group is recognised to be triggered by a number of factors, including disruption of the original range, incomplete lineage sorting, repeated phases of asymmetrical introgression and isolation. The key role played by some Mediterranean regions on the range establishment and dynamics of this oak group is discussed.

Keywords

Chloroplast DNA Quercus Mediterranean Basin Landscape genetics Phylogeographical inference 

Notes

Acknowledgements

We warmly thank all the friends and colleagues that participated in the sample collection: Nisreen Al-Qadi, Farag Bakkar, Fotios Bekris, Laura Genco, Tunçay Güner, Magda Bou Dagher-Kharrat, Fazia Krouchi, Angeliki Laiou, Faouzi Maamouri, Maria Mayol, Karalambos Neophytou, Sergio Ortu, Antonello Salis, Leonardo Scuderi, Avra Schirone, Martina Temunovic, Maria Paola Tomasino, Enara Otaegi Veslin, Valasia Yakovoglou and Petar Zhelev. This work represents part of the PhD thesis of MV granted by Sabina Universitas (P.N. 566). GWG is financed by the Austrian Science Fund (FWF): Grant M-1751-B16. TD acknowledges funding by the Swedish Research Council (VR).

Data archiving statement

All sequence data generated as part of this study are available on GenBank (http://www.ncbi.nlm.nih.gov/genbank/) under accession numbers LM222072–LM222201 and LM222232-LM222296; other relevant data are within the paper and its Supplementary File S1.

Supplementary material

11295_2016_1086_MOESM1_ESM.xlsx (71 kb)
Fig S1 (XLSX 70 kb)
11295_2016_1086_MOESM2_ESM.pptx (571 kb)
Fig S2 (PPTX 570 kb)

References

  1. Acosta MC, Premoli AC (2010) Evidence of chloroplast capture in South American Nothofagus (subgenus Nothofagus, Nothofagaceae). Mol Phylogenet Evol 54:235–242CrossRefPubMedGoogle Scholar
  2. Bagnoli F, Tsuda Y, Fineschi S, Bruschi P, Magri D, Zehlev P, Paule L, Simeone MC, González-Martínez SC, Vendramin GG (2016) Combining molecular and fossil data to infer demographic history of Quercus cerris: insights on European eastern glacial refugia. J Biogeogr 43:679–690CrossRefGoogle Scholar
  3. Balaguer L, Martinez-Ferri E, Valladares F, Perez-Corona ME, Baquedano FJ, Castillo FJ, Manrique E (2001) Population divergence in the plasticity of the response of Quercus coccifera to the light environment. Funct Ecol 15:124–135CrossRefGoogle Scholar
  4. Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefPubMedGoogle Scholar
  5. Bandelt H-J, Forster P, Sykes BC, Richards MB (1995) Mitochondrial portraits of human populations using median networks. Genetics 141:743–753PubMedPubMedCentralGoogle Scholar
  6. Bandelt H-J, Macaulay V, Richards M (2000) Median networks: speedy construction and greedy reduction, one simulation, and two case studies from human mtDNA. Mol Phylogenet Evol 16:8–28CrossRefPubMedGoogle Scholar
  7. Barbero M, Loisel R, Quezel P (1992) Biogeography, ecology and history of Mediterranean Quercus ilex ecosystems. Vegetatio 100:19–34CrossRefGoogle Scholar
  8. Besnard G, Rubio de Casas R, Vargas P (2007) Nuclear and plastid DNA polymorphism reveals large-scale reticulation in the olive tree complex (Olea europaea L.). J Biogeogr 34:736–752CrossRefGoogle Scholar
  9. Bilgin R (2011) Back to the suture: the distribution of intraspecific genetic diversity in and around Anatolia. Int J Mol Sci 12:4080–4103CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bittkau C, Comes HP (2005) Evolutionary processes in a continental island system: Molecular phylogeography of the Aegean Nigella arvensis alliance (Ranunculaceae) inferred from chloroplast DNA. Mol Ecol 14:4065–4083Google Scholar
  11. Blondel J (2006) The ‘design’ of Mediterranean landscapes: a millennial story of humans and ecological systems during the historic period. Hum Ecol 34:713–729CrossRefGoogle Scholar
  12. Blondel J, Aronson J (1999) Biology and wildlife of the Mediterranean region. Oxford University Press, OxfordGoogle Scholar
  13. Blondel J, Aronson J, Bodiou JY, Boeuf G (2010) The Mediterranean region: biological diversity in space and time. Oxford University Press, OxfordGoogle Scholar
  14. Brewer S, Cheddadi R, de Beaulieu JL, Reille M (2002) The spread of deciduous Quercus throughout Europe since the last glacial period. Forest Ecol Manag 156:27–48CrossRefGoogle Scholar
  15. Browicz K (1986) Chorology of trees and shrubs in South-West Asia and adjacent regions. Polish Scientific Publishers, WarsawGoogle Scholar
  16. Bryant D, Moulton V (2004) Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21:255–265CrossRefPubMedGoogle Scholar
  17. Cavender-Bares J, Gonzalez-Rodriguez A, Eaton DAR, Hipp AAL, Beulke A, Manos PS (2015) Phylogeny and biogeography of the American live oaks (Quercus subsection Virentes): a genomic and population genetics approach. Mol Ecol 24:3668–3687CrossRefPubMedGoogle Scholar
  18. Chen C, Qi ZC, Xu XH, Comes HP, Koch MA, Jin XJ, Fu CX, Qiu YX (2014) Understanding the formation of Mediterranean-African-Asian disjunctions: evidence for Miocene climate-driven vicariance and recent long-distance dispersal in the Tertiary relict Smilax aspera (Smilacaceae). New Phytol 204:243–255CrossRefPubMedGoogle Scholar
  19. Conord C, Gurevitch J, Fady B (2012) Large-scale longitudinal gradients of genetic diversity: a meta-analysis across six phyla in the Mediterranean basin. Ecol Evol 2:2600–2614CrossRefPubMedPubMedCentralGoogle Scholar
  20. Davis PH (1971) Distribution patterns in Anatolia with particular reference to endemism. In: Davis PH, Harper PC, Hedge IC (eds) Plant Life of South-West Asia. Edinburgh Botanical Society of Edinburgh, Edinburgh, pp. 15–27Google Scholar
  21. Denk T, Grimm GW (2010) The oaks of western Eurasia: traditional classifications and evidence from two nuclear markers. Taxon 59:351–366Google Scholar
  22. 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 169:7–20CrossRefGoogle Scholar
  23. Désamoré A, Laenen B, Devos N, Popp M (2011) Out of Africa: north-westwards Pleistocene expansions of the heather Erica arborea. J Biogeogr 38:164–176CrossRefGoogle Scholar
  24. Eaton DAR, Hipp AL, Gonzalez-Rodriguez A, Cavender-Bares J (2015) Historical introgression among the American live oaks and the comparative nature of tests for introgression. Evolution 69:2587–2601CrossRefPubMedGoogle Scholar
  25. Emberger L (1930) La végétation de la région méditerranéenne: essai d’une classification des groupements végétaux. Rev Gen Bot 42:641–662 et 705–721Google Scholar
  26. Gaudeul M, Véla E, Rouhan G (2016) Eastward colonization of the Mediterranean Basin by two geographically structured clades: the case of Odontites Ludw.(Orobanchaceae). Mol Phylogenet Evol 96:140–149CrossRefPubMedGoogle Scholar
  27. Gavin DG, Fitzpatrick MC, Gugger PF, Heath KD, Rodriguez-Sanchez F et al (2014) Climate refugia: joint inference from fossil records, species distribution models and phylogeography. New Phytol 204:37–54CrossRefPubMedGoogle Scholar
  28. Giorgi F (2006) Climate change hot-spots. Geophys Res Lett 33Google Scholar
  29. Govaerts R, Frodin DG (1998) World checklist and bibliography of Fagales (Betulaceae, Corylaceae, Fagaceae and Ticodendraceae). Kew Royal Botanic Gardens, KewGoogle Scholar
  30. Greuter W, Burdet HM, Long G (1986) Med-Checklist: a critical inventory of vascular plants of the circum-Mediterranean countries, Vol 3, Dicotyledones (Convolvulaceae-Labiatae). Conservatoire et Jardin botaniques, Ville de GenèveGoogle Scholar
  31. Gugger PF, Cavender-Bares J (2013) Molecular and morphological support for a Florida origin of the Cuban oak. J Biogeogr 40:632–645CrossRefGoogle Scholar
  32. Hampe A, Jump AS (2011) Climate relicts: past, present, future. Annl Rev Ecol Evol Syst 42:313–333CrossRefGoogle Scholar
  33. Hampe A, Rodríguez-Sánchez F, Dobrowski S, Hu FS, Gavin DG (2013) Climate refugia: from the last glacial maximum to the twenty-first century. New Phytol 197:16–18CrossRefPubMedGoogle Scholar
  34. Hare MP, Avise JC (1998) Population structure in the American oyster as inferred by nuclear gene genealogies. Mol Biol Evol 15:119–128CrossRefPubMedGoogle Scholar
  35. Herrera C (1992) Historical effects and sorting processes as explanations for contemporary ecological patterns: character syndromes in mediterranean woody plants. Am Nat 140:421–446CrossRefGoogle Scholar
  36. Hewitt GM (2011) Mediterranean peninsulas: the evolution of hotspots. In: Zachos FE, Habel JC (eds) Biodiversity hotspots. Springer, Berlin, Heidelberg, pp. 123–147CrossRefGoogle Scholar
  37. Hipp AL, Eaton DAR, Cavender-Bares J, Fitzek E, Nipper R, Manos PS (2014) A framework phylogeny of the American oak clade based on sequenced RAD data. PLoS One 9:e93975CrossRefPubMedPubMedCentralGoogle Scholar
  38. Holz I, Gradstein RS (2005) Cryptogamic epiphytes in primary and recovering upper montane oak forests of Costa Rica—species richness, community composition and ecology. Plant Ecol 178:89–109CrossRefGoogle Scholar
  39. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267CrossRefPubMedGoogle Scholar
  40. IUCN (2016) The Red List of Threatened Species. Version 2015–4; www.iucnredlist.org. Downloaded on 21 March 2016Google Scholar
  41. Johnson PS, Shifley RS, Rogers R (2002) The ecology and silviculture of oaks. CABI Publishing, New YorkCrossRefGoogle Scholar
  42. Kapli P, Botoni D, Ilgaz Ç, Kumlutas Y, Avcı A, Rastegar-Pouyani N, Fathinia B, Lymberakis P, Ahmadzadeh F, Poulakakis N (2013) Molecular phylogeny and historical biogeography of the Anatolian lizard Apathya (Squamata, Lacertidae). Mol Phylogenet Evol 66:992–1001CrossRefPubMedGoogle Scholar
  43. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMedGoogle Scholar
  44. Klausmeyer KR, Shaw MR (2009) Climate change, habitat loss, protected areas and the climate adaptation potential of species in Mediterranean ecosystems worldwide. PLoS One 4:e6392CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kovar-Eder J, Kvaček Z, Ströbitzer-Hermann M (2004) The Miocene flora of Parschlug (Styria, Austria)—revision and synthesis. Ann Naturhist Mus Wien 105:45–159Google Scholar
  46. Krijgsman W (2002) The Mediterranean: Mare Nostrum of Earth sciences. Earth Planet Sci Lett 205:1–12CrossRefGoogle Scholar
  47. Lefèvre F, Koskela J, Hubert J, Kraigher H, Longauer R, Olrik DC, Schueler S et al (2013) Dynamic conservation of forest genetic resources in 33 European countries. Conserv Biol 27:373–384CrossRefPubMedGoogle Scholar
  48. Lei M, Wang Q, Wu ZJ, Lopez-Pujol J, Li DZ, Zhang ZY (2012) Molecular phylogeography of Fagus engleriana (Fagaceae) in subtropical China: limited admixture among multiple refugia. Tree Genet Genomes 8:1203–1212CrossRefGoogle Scholar
  49. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452Google Scholar
  50. Liepelt S, Cheddadi R, de Beaulieu JL, Fady B, Gömöry D, Hussendörfer E et al (2009) Postglacial range expansion and its genetic imprints in Abies alba (Mill.)—a synthesis from palaeobotanic and genetic data. Rev Palaeobot Palynol 153:139–149CrossRefGoogle Scholar
  51. López de Heredia U, Jiménez P, Collada C, Simeone MC, Bellarosa R, Schirone B, Cervera MT, Gil L (2007) Multi-marker phylogeny of three evergreen oaks reveals vicariant patterns in the Western Mediterranean. Taxon 56:1209–1209CrossRefGoogle Scholar
  52. Lumaret R, Mir C, Michaux H, Raynal V (2002) Phylogeographic variation of chloroplast DNA in holm oak (Q. ilex L.). Mol Ecol 11:2327–2336CrossRefPubMedGoogle Scholar
  53. Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75. http://mesquiteproject.org
  54. Magri D, Fineschi S, Bellarosa R, Buonamici A, Sebastiani F, Schirone B, Simeone MC, Vendramin GG (2007) The distribution of Quercus suber chloroplast haplotypes matches the palaeogeographical history of the western Mediterranean. Mol Ecol 16:5259–5266CrossRefPubMedGoogle Scholar
  55. Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76:173–190CrossRefPubMedGoogle Scholar
  56. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  57. Masta SE, Sullivan B, Lamb T, Routman EJ (2002) Phylogeography, species boundaries, and hybridization among toads of the Bufoamericanus group. Mol Phylogenet Evol 24:302–314CrossRefPubMedGoogle Scholar
  58. Mateu-Andrés I, Ciurana M-J, Aguilella A, Boisset F, Guara M, Laguna E, Currás R, Ferrer P, Vela E, Puche MF, Pedrola-Monfort J (2015) Plastid DNA homogeneity in Celtis australis L. (Cannabaceae) and Nerium oleander L. (Apocynaceae) throughout the Mediterranean Basin. Int J Plant Sci 176:421–432CrossRefGoogle Scholar
  59. McIntyre PJ, Thorne JH, Dolanc CR, Flint AL, Flint LE, Kelly M, Ackerly DD (2015) Twentieth-century shifts in forest structure in California: denser forests, smaller trees, and increased dominance of oaks. Proc Natl Acad Sci U S A 112:1458–1463CrossRefPubMedPubMedCentralGoogle Scholar
  60. Médail F, Diadema K (2009) Glacial refugia influence plant diversity patterns in the Mediterranean Basin. J Biogeogr 36:1333–1345CrossRefGoogle Scholar
  61. Menitsky YL (2005) Oaks of Asia. Science Publishers, Enfield, New HampshireGoogle Scholar
  62. Migliore J, Baumel A, Juin M, Médail F (2012) From Mediterranean shores to central Saharan mountains: key phylogeographical insights from the genus Myrtus. J Biogeogr 39:942–956CrossRefGoogle Scholar
  63. Modesto IS, Miguel C, Pina-Martins F, Glushkova M, Veloso M, Paulo OS, Batista D (2014) Identifying signatures of natural selection in cork oak (Quercus suber L.) genes through SNP analysis. Tree Genet Genomes 10:1645–1660CrossRefGoogle Scholar
  64. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858Google Scholar
  65. Neophytou C, Aravanopoulos FA, Fink S, Dounavi A (2011a) Interfertile oaks in an island environment. II. Limited hybridization between Quercus alnifolia Poech and Q. coccifera L. in a mixed stand. Eur J For Res 130:623–635CrossRefGoogle Scholar
  66. Neophytou C, Dounavi A, Fink S, Aravanopoulos FA (2011b) 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 For Res 130:543–555CrossRefGoogle Scholar
  67. Nieto Feliner G (2014) Patterns and processes in plant phylogeography in the Mediterranean Basin. A review. Perspect Plant Ecol Evol Syst 16:265–278CrossRefGoogle Scholar
  68. Paicheler JC, Blanc C (1981) La flore du bassin lacustre miocène de Bes-Konak (Anatolie septentrionale, Turquie). Géol Médit 8:19–60Google Scholar
  69. Papageorgiou AC, Vidalis A, Gailing O, Tsiripidis I, Hatziskakis S, Boutsios S et al (2008) Genetic variation of beech (Fagus sylvatica L.) in Rodopi (N.E. Greece). Eur J For Res 127:81–88CrossRefGoogle Scholar
  70. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539CrossRefPubMedPubMedCentralGoogle Scholar
  71. Petit RJ, Csaikl UM, Bordács S, Burg K, Coart E, Cottrell J, Van Dam B, Deans JD, Dumolin-Lapègue S, Fineschi S (2002) Chloroplast DNA variation in European white oaks: phylogeography and patterns of diversity based on data from over 2600 populations. Forest Ecol Manag 156:5–26Google Scholar
  72. Petit RJ, Aguinagalde I, de Beaulieu J-L, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563CrossRefPubMedGoogle Scholar
  73. Petit RJ, Hampe A, Cheddadi R (2005) Climate changes and tree phylogeography in the Mediterranean. Taxon 54:877–885CrossRefGoogle Scholar
  74. Popov SV, Rögl F, Rozanov AY, Steininger FF, Shcherba IG, Kovac M (2004) Lithological-Paleogeographic maps of Paratethys. 10 maps. Late Eocene to Pliocene. Courier Forschungsinstitut Senckenberg 250:1–46Google Scholar
  75. Quézel P, Médail F (2003) Ecologie et biogéographie des forêts du basin méditerranéen. Elsevier, Collection Environnement, ParisGoogle Scholar
  76. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100CrossRefPubMedGoogle Scholar
  77. Robertson AH (1998) Mesozoic-Tertiary tectonic evolution of the easternmost Mediterranean area: integration of marine and land evidence. Proceedings of the Ocean Drilling Program, Scientific Results 160Google Scholar
  78. Rodriguez-Sanchez F, Guzman B, Valido A, Vargas P, Arroyo J (2009) Late Neogene history of the laurel tree (Laurus L., Lauraceae) based on phylogeographical analyses of Mediterranean and Macaronesian populations. J Biogeogr 36:1270–1281CrossRefGoogle Scholar
  79. Rechinger KH (1943) Flora Aegaea. Flora der Inseln und Halbinseln des ägäischen Meeres. Österreichische Akademie der Wissenschaften Wien, Mathematisch-Naturwissenschaftliche Klasse, Denkschriften,105/1Google Scholar
  80. Romane F, Terradas J (1992) Quercus ilex ecosystems: function, dynamics and management. Kluver, DordrechtCrossRefGoogle Scholar
  81. Simeone MC, Grimm GW, Papini A, Vessella F, Cardoni S, Tordoni E, Piredda R, Franc A, Denk T (2016) Plastome data reveal multiple geographic origins of Quercus Group Ilex. PeerJ 4:e1897CrossRefPubMedPubMedCentralGoogle Scholar
  82. Simeone MC, 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 172:478–499CrossRefGoogle Scholar
  83. Steininger FF, Rögl F (1984) Paleogeography and palinspastic reconstruction of the Neogene of the Mediterranean and Paratethys. Geol Soc Lond, Spec Publ 17:659–668CrossRefGoogle Scholar
  84. Suc J-P (1984) Origin and evolution of the Mediterranean vegetation and climate in Europe. Nature 307:429–432CrossRefGoogle Scholar
  85. 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. Mol Biol Evol 28:2731–2739Google Scholar
  86. Thompson JD (2005) Plant Evolution in the Mediterranean. Oxford Univ. Press, OxfordGoogle Scholar
  87. Toumi L, Lumaret R (2010) Genetic variation and evolutionary history of holly oak: a circum-Mediterranean species-complex [Quercus coccifera L./Q. calliprinos (Webb) Holmboe, Fagaceae]. Plant Syst Evol 290:159–171CrossRefGoogle Scholar
  88. Tovar-Sanchez E, Oyama K (2004) Natural hybridization and hybrid zones between Quercus crassifolia and Quercus crassipes (Fagaceae) in Mexico: morphological and molecular evidence. Am J Bot 91:1352–1363CrossRefPubMedGoogle Scholar
  89. Vandergast AG, Perry WM, Lugo RV, Hathaway SA (2011) Genetic landscapes GIS toolbox: tools to map patterns of genetic divergence and diversity. Mol Ecol Resour 11:158–161CrossRefPubMedGoogle Scholar
  90. Velitzelos D, Bouchal JM, Denk T (2014) Review of the Cenozoic floras and vegetation of Greece. Rev Palaeobot Palynol 204:56–117CrossRefGoogle Scholar
  91. Vessella F, Simeone MC, Schirone B (2015) Quercus suber range dynamics by ecological niche modelling: from the last interglacial to present time. Quat Sci Rev 119:85–93CrossRefGoogle Scholar
  92. Zohary M (1961) On the oak species of the Middle East. Bull Res Counc Isr 9:161–186Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Dipartimento di Scienze Agrarie e Forestali (DAFNE)Università degli studi della TusciaViterboItaly
  2. 2.National Research CouncilInstitute of Agro-environmental and Forest BiologyPoranoItaly
  3. 3.Department of PalaeobiologySwedish Museum of Natural HistoryStockholmSweden
  4. 4.Department of PalaeontologyUniversity of WienWienAustria

Personalised recommendations