Organisms Diversity & Evolution

, Volume 17, Issue 2, pp 323–349 | Cite as

Against all odds: reconstructing the evolutionary history of Scrophularia (Scrophulariaceae) despite high levels of incongruence and reticulate evolution

  • Agnes Scheunert
  • Günther Heubl
Original Article


The figwort genus Scrophularia (Scrophulariaceae), widespread across the temperate zone of the Northern Hemisphere, comprises about 250 species and is a taxonomically challenging lineage displaying large morphological and chromosomal diversity. Scrophularia has never been examined in a large-scale phylogenetic and biogeographic context and represents a useful model for studying evolutionary history in the context of reticulation. A comprehensively sampled phylogeny of Scrophularia was constructed, based on nuclear ribosomal (ITS) and plastid DNA sequences (trnQ-rps16 intergenic spacer, trnL-trnF region) of 147 species, using Bayesian inference and maximum likelihood approaches. Selected individuals were cloned. A combination of coding plastid indels and ITS intra-individual site polymorphisms, and applying Neighbor-Net and consensus network methods for adequate examination of within-dataset uncertainty as well as among-dataset incongruence, was used to disentangle phylogenetic relationships. Furthermore, divergence time estimation and ancestral area reconstruction were performed to infer the biogeographic history of the genus. The analyses reveal significant plastid-nuclear marker incongruence and considerable amounts of intra-individual nucleotide polymorphism in the ITS dataset. This is due to a combination of processes including reticulation and incomplete lineage sorting, possibly complicated by inter-array heterogeneity and pseudogenization in ITS in the presence of incomplete concerted evolution. Divergence time estimates indicate that Scrophularia originated during the Miocene in Southwestern Asia, its primary center of diversity. From there, the genus spread to Eastern Asia, the New World, Europe, Northern Africa, and other regions. Hybridization and polyploidy played a key role in the diversification history of Scrophularia, which was shaped by allopatric speciation in mountainous habitats during different climatic periods.


Scrophularia Incongruence Reticulate evolution Intra-individual polymorphism 2ISP Allopatric speciation 



The authors wish to thank the herbaria and curators of A, B, E, GH, HAL, KUN, M, MA, MSB, W, and WU, for providing loans, for access to the specimens for study and for help in obtaining leaf material. Dirk Albach, Cheng-Xin Fu, Mark Mayfield, Søren Rosendal Jensen, Andrej Sytin, and Lang-Ran Xu are acknowledged for sending plant material from specimens deposited in GOET, HU/HZU, KSC, HSNU, LE, and WUK. Christian Bräuchler, Matthias Erben, and the Botanical Garden Munich kindly contributed seeds or plants required for study. We are grateful to Dirk Albach for sending photos and specimens and for continued support and helpful suggestions; to Guido Grimm for the generous time given for help with and discussion of the ITS data; to Susanne Renner and Lars Nauheimer for advice in divergence dating and BEAST; and to Ingo Michalak for help with RAxML and substitution model details. Alastair Potts and three anonymous reviewers are acknowledged for helpful comments which improved the manuscript. We thank Tanja Ernst for invaluable help in the lab and Wei Jie for providing translations from Chinese language.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

13127_2016_316_MOESM1_ESM.pdf (116 kb)
Online Resource 1 (PDF 116 kb)
13127_2016_316_MOESM2_ESM.pdf (183 kb)
Online Resource 2 (PDF 183 kb)
13127_2016_316_MOESM3_ESM.pdf (75 kb)
Online Resource 3 (PDF 74 kb)
13127_2016_316_MOESM4_ESM.pdf (206 kb)
Online Resource 4 (PDF 205 kb)
13127_2016_316_MOESM5_ESM.pdf (72 kb)
Online Resource 5 (PDF 72 kb)
13127_2016_316_MOESM6_ESM.pdf (106 kb)
Online Resource 6 (PDF 105 kb)
13127_2016_316_MOESM7_ESM.pdf (121 kb)
Online Resource 7 (PDF 120 kb)


  1. Abbott, R., Albach, D., Ansell, S., Arntzen, J. W., Baird, S. J. E., Bierne, N., et al. (2013). Hybridization and speciation. Journal of Evolutionary Biology, 26, 229–246.PubMedCrossRefGoogle Scholar
  2. Abdrakhmatov, K. Y., Aldazhanov, S. A., Hager, B. H., Hamburger, M. W., Herring, T. A., Kalabaev, K. B., et al. (1996). Relatively recent construction of the Tien Shan inferred from GPS measurements of present-day crustal deformation rates. Nature, 384, 450–453.CrossRefGoogle Scholar
  3. Albach, D. C., Meudt, H. M., & Oxelman, B. (2005). Piecing together the “new” Plantaginaceae. American Journal of Botany, 92(2), 297–315.PubMedCrossRefGoogle Scholar
  4. Albaladejo, R. G., Fuertes Aguilar, J., Aparicio, A., & Nieto Feliner, G. (2005). Contrasting nuclear-plastidial phylogenetic patterns in the recently diverged Iberian Phlomis crinita and P. lychnitis lineages (Lamiaceae). Taxon, 54, 987–998.CrossRefGoogle Scholar
  5. Álvarez, I., & Wendel, J. F. (2003). Ribosomal ITS sequences and plant phylogenetic inference. Molecular Phylogenetics and Evolution, 29, 417–434.PubMedCrossRefGoogle Scholar
  6. An, Z.-S., Kutzbach, J. E., Prell, W. L., & Porter, S. C. (2001). Evolution of Asian monsoons and phased uplift of the Himalaya-Tibetan plateau since Late Miocene times. Nature, 411, 62–66.CrossRefGoogle Scholar
  7. Andreasen, K., & Baldwin, B. G. (2001). Unequal evolutionary rates between annual and perennial lineages of checker mallows (Sidalcea, Malvaceae): evidence from 18S–26S rDNA internal and external transcribed spacers. Molecular Biology and Evolution, 18(6), 936–944.PubMedCrossRefGoogle Scholar
  8. Arnheim, N., Krystal, M., Schmickel, R., Wilson, G., Ryder, O., & Zimmer, E. (1980). Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes. Proceedings of the National Academy of Sciences of the United States of America, 77(12), 7323–7327.PubMedPubMedCentralCrossRefGoogle Scholar
  9. Attar, F., Riahi, M., Daemi, F., & Aghabeigi, F. (2011). Preliminary molecular phylogeny of Eurasian Scrophularia (Scrophulariaceae) based on DNA sequence data from trnS-trnG and ITS regions. Plant Biosystems, 145(4), 857–865.CrossRefGoogle Scholar
  10. Bailey, C. D., Carr, T. G., Harris, S. A., & Hughes, C. E. (2003). Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes. Molecular Phylogenetics and Evolution, 29, 435–455.PubMedCrossRefGoogle Scholar
  11. Baldwin, B. G., Sanderson, M. J., Porter, J. M., Wojciechowski, M. F., Campbell, C. S., & Donoghue, M. J. (1995). The its region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Annals of the Missouri Botanical Garden, 82(2), 247–277.CrossRefGoogle Scholar
  12. Ballato, P., Mulch, A., Landgraf, A., Strecker, M. R., Dalconi, M. C., Friedrich, A., et al. (2010). Middle to late Miocene Middle Eastern climate from stable oxygen and carbon isotope data, southern Alborz mountains, N Iran. Earth and Planetary Science Letters, 300, 125–138.CrossRefGoogle Scholar
  13. Baumel, A., Ainouche, M. L., Bayer, R. J., Ainouche, A. K., & Misset, M. T. (2002). Molecular phylogeny of hybridizing species from the genus Spartina Schreb. (Poaceae). Molecular Phylogenetics and Evolution, 22(2), 303–314.PubMedCrossRefGoogle Scholar
  14. Beiko, R. G., Doolittle, W. F., & Charlebois, R. L. (2008). The impact of reticulate evolution on genome phylogeny. Systematic Biology, 57(6), 844–856.PubMedCrossRefGoogle Scholar
  15. Berberian, M., & King, G. C. P. (1981). Towards a paleogeography and tectonic evolution of Iran. Canadian Journal of Earth Sciences, 18, 210–265.CrossRefGoogle Scholar
  16. Blanco-Pastor, J. L., Vargas, P., & Pfeil, B. E. (2012). Coalescent simulations reveal hybridization and incomplete lineage sorting in Mediterranean Linaria. PloS One, 7(6), e39089.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Boissier, P. E. (1879). Flora orientalis, sive enumeratio plantarum in Oriente a Graecia et Aegypto ad Indiae fines hucusque observatarum, 4, 2. Geneva: H. Georg.Google Scholar
  18. Boufford, D. E., & Spongberg, S. A. (1983). Eastern Asian – Eastern North American phytogeographical relationships - a history from the time of Linnaeus to the twentieth century. Annals of the Missouri Botanical Garden, 70, 423–439.CrossRefGoogle Scholar
  19. Brigham-Grette, J. (2001). New perspectives on Beringian Quaternary paleogeography, stratigraphy, and glacial history. Quaternary Science Reviews, 20, 15–24.CrossRefGoogle Scholar
  20. Brown, D. D., Wensink, P. C., & Jordan, E. (1972). A comparison of the ribosomal DNA’s of Xenopus laevis and Xenopus mulleri: the evolution of tandem genes. Journal of Molecular Biology, 63, 57–73.PubMedCrossRefGoogle Scholar
  21. Bryant, D., & Moulton, V. (2004). Neighbor-Net: an agglomerative method for the construction of phylogenetic networks. Molecular Biology and Evolution, 21(2), 255–265.PubMedCrossRefGoogle Scholar
  22. Campbell, C. S., Wojciechowski, M. F., Baldwin, B. G., Alice, L. A., & Donoghue, M. J. (1997). Persistent nuclear ribosomal DNA sequence polymorphism in the Amelanchier agamic complex (Rosaceae). Molecular Biology and Evolution, 14, 81–90.PubMedCrossRefGoogle Scholar
  23. Carlbom, C. G. (1964). An experimental taxonomic study of a Northwest American polyploid species, Scrophularia lanceolata Pursh. Corvallis: Oregon State University.Google Scholar
  24. Carlbom, C. G. (1969). Evolutionary relationships in the genus Scrophularia L. Hereditas, 61, 287–301.CrossRefGoogle Scholar
  25. Chen, L.-Y., Zhao, S.-Y., Mao, K.-S., Les, D. H., Wang, Q.-F., & Moody, M. L. (2014). Historical biogeography of Haloragaceae: an out-of-Australia hypothesis with multiple intercontinental dispersals. Molecular Phylogenetics and Evolution, 78, 87–95.PubMedCrossRefGoogle Scholar
  26. Chen, S.-T., Guan, K.-Y., Zhou, Z.-K., Olmstead, R., & Cronk, Q. (2005). Molecular phylogeny of Incarvillea (Bignoniaceae) based on ITS and trnL-F sequences. American Journal of Botany, 92, 625–633.PubMedCrossRefGoogle Scholar
  27. Chen, S.-Y., Wu, G.-L., Zhang, D.-J., Gao, Q.-B., Duan, Y.-Z., Zhang, F.-Q., et al. (2008). Potential refugium on the Qinghai–Tibet Plateau revealed by the chloroplast DNA phylogeography of the alpine species Metagentiana striata (Gentianaceae). Botanical Journal of the Linnean Society, 157, 125–140.CrossRefGoogle Scholar
  28. Clay, D. L., Novak, S. J., Serpe, M. D., & Tank, D. C. (2012). Homoploid hybrid speciation in a rare endemic Castilleja from Idaho (Castilleja christii, Orobanchaceae). American Journal of Botany, 99(12), 1976–1990.PubMedCrossRefGoogle Scholar
  29. Comes, H. P. (2004). The Mediterranean region - a hotspot for plant biogeographic research. New Phytologist, 164, 11–14.CrossRefGoogle Scholar
  30. Dalgaard, V. (1979). Biosystematics of the Macaronesian species of Scrophularia. Opera Botanica, 51, 1–64.Google Scholar
  31. Datson, P. M., Murray, B. G., & Hammett, K. R. W. (2006). Pollination systems, hybridization barriers and meiotic chromosome behaviour in Nemesia hybrids. Euphytica, 151, 173–185.CrossRefGoogle Scholar
  32. Datson, P. M., Murray, B. G., & Steiner, K. E. (2008). Climate and the evolution of annual/perennial life-histories in Nemesia (Scrophulariaceae). Plant Systematics and Evolution, 270, 39–57.CrossRefGoogle Scholar
  33. Davis, P. H., Mill, R. R., & Tan, K. (1988). Flora of Turkey and the East Aegean Islands, 10 (Suppl. 1). Edinburgh: Edinburgh University Press.Google Scholar
  34. Degnan, J. H., & Rosenberg, N. A. (2009). Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends in Ecology and Evolution, 24(6), 332–340.PubMedCrossRefGoogle Scholar
  35. Denk, T., Grimsson, F., Zetter, R., & Simonarson, L. A. (2011). Late Cainozoic floras of Iceland: 15 million years of vegetation and climate history in the northern North Atlantic. Dordrecht: Springer.CrossRefGoogle Scholar
  36. Dercourt, J., Zonenshain, L. P., Ricou, L.-E., Kazmin, V. G., Le Pichon, X., Knipper, A. L., et al. (1986). Geological evolution of the Tethys belt from the Atlantic to the Pamirs since the Lias. Tectonophysics, 123, 241–315.CrossRefGoogle Scholar
  37. Djamali, M., Baumel, A., Brewer, S., Jackson, S. T., Kadereit, J. W., López-Vinyallonga, S., et al. (2012a). Ecological implications of Cousinia Cass. (Asteraceae) persistence through the last two glacial–interglacial cycles in the continental Middle East for the Irano-Turanian flora. Review of Palaeobotany and Palynology, 172, 10–20.CrossRefGoogle Scholar
  38. Djamali, M., Brewer, S., Breckle, S. W., & Jackson, S. T. (2012b). Climatic determinism in phytogeographic regionalization: a test from the Irano-Turanian region, SW and Central Asia. Flora, 207, 237–249.CrossRefGoogle Scholar
  39. Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Eidesen, P. B., Alsos, I. G., Popp, M., Stensrud, O., Suda, J., & Brochmann, C. (2007). Nuclear vs. plastid data: complex Pleistocene history of a circumpolar key species. Molecular Ecology, 16, 3902–3925.PubMedCrossRefGoogle Scholar
  41. Eig, A. (1944). Revision of the oriental Scrophularia species of the herbarium of the Hebrew University. Palestine. Journal of Botany, 3, 79–93.Google Scholar
  42. Ellstrand, N. C., & Schierenbeck, K. A. (2000). Hybridization as a stimulus for the evolution of invasiveness in plants? Proceedings of the National Academy of Sciences of the United States of America, 97(13), 7043–7050.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Estep, M. C., McKain, M. R., Vela Diaz, D., Zhong, J.-S., Hodge, J. G., Hodkinson, T. R., et al. (2014). Allopolyploidy, diversification, and the Miocene grassland expansion. Proceedings of the National Academy of Sciences of the United States of America, 111(42), 15149–15154.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Farris, J. S., Källersjö, M., Kluge, A. G., & Bult, C. (1995). Testing significance of incongruence. Cladistics, 10, 315–319.CrossRefGoogle Scholar
  45. Fehrer, J., Gemeinholzer, B., Chrtek Jr., J., & Bräutigam, S. (2007). Incongruent plastid and nuclear DNA phylogenies reveal ancient intergeneric hybridization in Pilosella hawkweeds (Hieracium, Cichorieae, Asteraceae). Molecular Phylogenetics and Evolution, 42, 347–361.PubMedCrossRefGoogle Scholar
  46. Fehrer, J., Krak, K., & Chrtek Jr., J. (2009). Intra-individual polymorphism in diploid and apomictic polyploid hawkweeds (Hieracium, Lactuceae, Asteraceae): disentangling phylogenetic signal, reticulation, and noise. BMC Evolutionary Biology, 9, 239.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Feng, T., Downie, S. R., Yu, Y., Zhang, X.-M., Chen, W.-W., He, X.-J., et al. (2009). Molecular systematics of Angelica and allied genera (Apiaceae) from the Hengduan Mountains of China based on nrDNA ITS sequences: phylogenetic affinities and biogeographic implications. Journal of Plant Research, 122(4), 403–414.PubMedCrossRefGoogle Scholar
  48. Fischer, E. (2004). Scrophulariaceae. In J. W. Kadereit (Ed.), The families and genera of vascular plants, vol. 7 (pp. 333–432). Heidelberg: Springer.Google Scholar
  49. Fortelius, M., Eronen, J., Liu, L.-P., Pushkina, D., Tesakov, A., Vislobokova, I., et al. (2006). Late Miocene and Pliocene large land mammals and climatic changes in Eurasia. Palaeogeography, Palaeoclimatology, Palaeoecology, 238, 219–227.CrossRefGoogle Scholar
  50. Fuertes Aguilar, J., & Nieto Feliner, G. (2003). Additive polymorphisms and reticulation in an ITS phylogeny of thrifts (Armeria, Plumbaginaceae). Molecular Phylogenetics and Evolution, 28, 430–447.PubMedCrossRefGoogle Scholar
  51. Gadagkar, S. R., Rosenberg, M. S., & Kumar, S. (2005). Inferring species phylogenies from multiple genes: concatenated sequence tree versus consensus gene tree. Journal of Experimental Zoology, 304B, 64–74.CrossRefGoogle Scholar
  52. Glémin, S., Bazin, E., & Charlesworth, D. (2006). Impact of mating systems on patterns of sequence polymorphism in flowering plants. Proceedings of the Royal Society of London B, 273, 3011–3019.CrossRefGoogle Scholar
  53. Goddijn, W. A., & Goethart, J. W. C. (1913). Ein künstlich erzeugter Bastard. Scrophularia neesii Wirtg. x S. vernalis L. Mededeelingen van’s Rijks Herbarium Leiden, 15, 1–10.Google Scholar
  54. Goldblatt, P., & Johnson, D. E., Eds. (1979). Index to plant chromosome numbers. Missouri Botanical Garden. Accessed 27 November 2015.
  55. Gorschkova, S. G. (1997). Scrophularia. In B. K. Schischkin, & E. G. Bobrov (Eds.), Flora of the USSR, translated from Russian, vol. 22 (pp. 205–274). New Delhi: Amerind.Google Scholar
  56. Gould, K. R., & Donoghue, M. J. (2000). Phylogeny and biogeography of Triosteum (Caprifoliaceae). Harvard Papers in Botany, 5, 157–166.Google Scholar
  57. Grau, J. (1976). Die Cytologie südwestmediterraner Scrophularia-Arten. Mitteilungen der Botanischen Staatssammlung München, 12, 609–654.Google Scholar
  58. Grau, J. (1979). The probable allopolyploid origin of Scrophularia auriculata and S. pseudoauriculata. Webbia, 34, 497–499.CrossRefGoogle Scholar
  59. Grau, J. (1980). Scrophularia. In P. Mouterde (Ed.), Nouvelle flore du Liban et de la Syrie, vol. 3 (pp. 235–241). Beyrouth: Dar el-Machreq Éditeurs.Google Scholar
  60. Grau, J. (1981). Scrophularia. In K. H. Rechinger (Ed.), Flora Iranica, cont. 147 (pp. 213–284). Graz: Akademische Druck- und Verlagsanstalt.Google Scholar
  61. Grimm, G. W., & Denk, T. (2008). ITS evolution in Platanus (Platanaceae): homoeologues, pseudogenes and ancient hybridization. Annals of Botany, 101, 403–419.PubMedCrossRefGoogle Scholar
  62. Grimm, G. W., Denk, T., & Hemleben, V. (2007). Coding of intraspecific nucleotide polymorphisms: a tool to resolve reticulate evolutionary relationships in the ITS of beech trees (Fagus L., Fagaceae). Systematics and Biodiversity, 5(3), 291–309.CrossRefGoogle Scholar
  63. Guest, B., Guest, A., & Axen, G. (2007). Late tertiary tectonic evolution of northern Iran: a case for simple crustal folding. Global and Planetary Change, 58, 435–453.CrossRefGoogle Scholar
  64. Guo, Z.-T., Peng, S.-Z., Hao, Q.-Z., Biscaye, P. E., An, Z.-S., & Liu, T.-S. (2004). Late Miocene–Pliocene development of Asian aridification as recorded in the Red-Earth Formation in northern China. Global and Planetary Change, 41, 135–145.CrossRefGoogle Scholar
  65. Guo, Z.-T., Ruddiman, W. F., Hao, Q.-Z., Wu, H.-B., Qiao, Y.-S., Zhu, R.-X., et al. (2002). Onset of Asian desertification by 22 Myr ago inferred from loess deposits in China. Nature, 416, 159–163.PubMedCrossRefGoogle Scholar
  66. Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.Google Scholar
  67. Hildebrand, P. R., Noble, S. R., Searle, M. P., Waters, D. J., & Parrish, R. R. (2001). Old origin for an active mountain range: geology and geochronology of the eastern Hindu Kush, Pakistan. Geological Society of America Bulletin, 113(5), 625–639.CrossRefGoogle Scholar
  68. Hildebrand, P. R., Searle, M. P., Shakirullah, K. Z. A., & van Heijst, H. J. (2000). Geological evolution of the Hindu Kush, NW frontier Pakistan: active margin to continent-continent collision zone. In M. A. Khan, P. J. Treloar, M. P. Searle, & M. Q. Jan (Eds.), Tectonics of the Nanga Parbat Syntaxis and the western Himalaya. The Geological Society of London special publications, vol. 170 (pp. 277–293). London: The Geological Society of London.Google Scholar
  69. Hipsley, C. A., & Müller, J. (2014). Beyond fossil calibrations: realities of molecular clock practices in evolutionary biology. Frontiers in Genetics, 5, 138.PubMedPubMedCentralCrossRefGoogle Scholar
  70. Hodač, L., Scheben, A. P., Hojsgaard, D., Paun, O., & Hörandl, E. (2014). ITS polymorphisms shed light on hybrid evolution in apomictic plants: a case study on the Ranunculus auricomus complex. PloS One, 9(7), e103003.PubMedPubMedCentralCrossRefGoogle Scholar
  71. Holland, B. R., Huber, K. T., Moulton, V., & Lockhart, P. J. (2004). Using consensus networks to visualize contradictory evidence for species phylogeny. Molecular Biology and Evolution, 21(7), 1459–1461.PubMedCrossRefGoogle Scholar
  72. Holland, B. R., & Moulton, V. (2003). Consensus networks: a method for visualising incompatibilities in collections of trees. In G. Benson & R. Page (Eds.), Algorithms in bioinformatics, WABI 2003 (pp. 165–176). Berlin: Springer.Google Scholar
  73. Hong, D.-Y. (1983). The distribution of Scrophulariaceae in the Holarctic with special reference to the floristic relationships between eastern Asia and eastern North America. Annals of the Missouri Botanical Garden, 70(4), 701–712.CrossRefGoogle Scholar
  74. Hong, D.-Y. (1993). Eastern Asian-North American disjunctions and their biological significance. Cathaya, 5, 1–39.Google Scholar
  75. Hong, D.-Y., Yang, H.-B., Jin, C.-L., & Holmgren, N. H. (1998). Scrophulariaceae. In Z.-Y. Wu (Ed.), Flora of China, vol. 18 (pp. 1–212). St. Louis: Missouri Botanical Garden.Google Scholar
  76. Hoorn, C., Mosbrugger, V., Mulch, A., & Antonelli, A. (2013). Biodiversity from mountain building. Nature Geoscience, 6, 154.CrossRefGoogle Scholar
  77. Huber-Morath, A. (1978). Verbascum. In P. H. Davis (Ed.), Flora of Turkey and the East Aegean Islands, vol. 6 (pp. 461–603). Edinburgh: Edinburgh University Press.Google Scholar
  78. Huelsenbeck, J. P., Bull, J. J., & Cunningham, C. W. (1996). Combining data in phylogenetic analysis. Trends in Ecology and Evolution, 11, 152–158.PubMedCrossRefGoogle Scholar
  79. Huson, D. H., & Bryant, D. (2006). Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23, 254–267.PubMedCrossRefGoogle Scholar
  80. Jobes, D. V., & Thien, L. B. (1997). A conserved motif in the 5.8S ribosomal RNA (rRNA) gene is a useful diagnostic marker for plant internal transcribed spacer (ITS) sequences. Plant Molecular Biology Reporter, 15, 326–334.CrossRefGoogle Scholar
  81. Joly, S., Starr, J. R., Lewis, W. H., & Bruneau, A. (2006). Polyploid and hybrid evolution in roses east of the Rocky Mountains. American Journal of Botany, 93, 412–425.PubMedCrossRefGoogle Scholar
  82. Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Kearney, T. H., & Peebles, R. H. (1951). Arizona Flora. Berkeley, Los Angeles, London: University of California Press.Google Scholar
  84. Kornhall, P., Heidari, N., & Bremer, B. (2001). Selagineae and Manuleeae, two tribes or one? Phylogenetic studies in the Scrophulariaceae. Plant Systematics and Evolution, 228, 199–218.CrossRefGoogle Scholar
  85. Kubatko, L. S., & Degnan, J. H. (2007). Inconsistency of phylogenetic estimates from concatenated data under coalescence. Systematic Biology, 56(1), 17–24.PubMedCrossRefGoogle Scholar
  86. Lall, S. S., & Mill, R. R. (1978). Scrophularia. In P. H. Davis (Ed.), Flora of Turkey and the East Aegean Islands, vol. 6 (pp. 603–647). Edinburgh: Edinburgh University Press.Google Scholar
  87. Laroche, J., & Bousquet, J. (1999). Evolution of the mitochondrial rps3 intron in perennial and annual angiosperms and homology to nad5 intron 1. Molecular Biology and Evolution, 16(4), 441–452.PubMedCrossRefGoogle Scholar
  88. Lavin, M., Herendeen, P. S., & Wojciechowski, M. F. (2005). Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the Tertiary. Systematic Biology, 54(4), 575–594.PubMedCrossRefGoogle Scholar
  89. Leaché, A. D., Harris, R. B., Rannala, B., & Yang, Z.-H. (2014). The influence of gene flow on species tree estimation: a simulation study. Systematic Biology, 63(1), 17–30.PubMedCrossRefGoogle Scholar
  90. Leitch, I. J., & Bennett, M. D. (1997). Polyploidy in angiosperms. Trends in Plant Science, 2(12), 470–476.CrossRefGoogle Scholar
  91. Li, H.-L. (1972). Eastern Asia-Eastern North America species-pairs in wide ranging genera. In A. Graham (Ed.), Floristics and paleofloristics of Asia and Eastern North America (pp. 65–78). Amsterdam: Elsevier.Google Scholar
  92. Li, J.-J., Zhou, S.-Z., Zhao, Z.-J., & Zhang, J. (2015). The Qingzang Movement: the major uplift of the Qinghai-Tibetan Plateau. Science China Earth Sciences, 58(11), 2113–2122.CrossRefGoogle Scholar
  93. Liao, C.-Y., Downie, S. R., Yu, Y., & He, X.-J. (2012). Historical biogeography of the Angelica group (Apiaceae tribe Selineae) inferred from analyses of nrDNA and cpDNA sequences. Journal of Systematics and Evolution, 50(3), 206–217.CrossRefGoogle Scholar
  94. Linder, C. R., & Rieseberg, L. H. (2004). Reconstructing patterns of reticulate evolution in plants. American Journal of Botany, 91(10), 1700–1708.PubMedCentralCrossRefGoogle Scholar
  95. Liu, J.-Q., Wang, Y.-J., Wang, A.-L., Hideaki, O., & Abbott, R. J. (2006). Radiation and diversification within the LigulariaCremanthodiumParasenecio complex (Asteraceae) triggered by uplift of the Qinghai-Tibetan Plateau. Molecular Phylogenetics and Evolution, 38, 31–49.PubMedCrossRefGoogle Scholar
  96. Liu, J.-S., & Schardl, C. L. (1994). A conserved sequence in internal transcribed spacer 1 of plant nuclear rRNA genes. Plant Molecular Biology, 26, 775–778.PubMedCrossRefGoogle Scholar
  97. Lobo, J. M. (2001). Spatial and environmental determinants of vascular plant species richness distribution in the Iberian Peninsula and Balearic Islands. Biological Journal of the Linnean Society, 73, 233–253.CrossRefGoogle Scholar
  98. Lockwood, J. D., Aleksić, J. M., Zou, J.-B., Wang, J., Liu, J.-Q., & Renner, S. S. (2013). A new phylogeny for the genus Picea from plastid, mitochondrial, and nuclear sequences. Molecular Phylogenetics and Evolution, 69, 717–727.PubMedCrossRefGoogle Scholar
  99. Lorenz-Lemke, A. P., Muschner, V. C., Bonatto, S. L., Cervi, A. C., Salzano, F. M., & Freitas, L. B. (2005). Phylogeographic inferences concerning evolution of Brazilian Passiflora actinia and P. elegans (Passifloraceae) based on ITS (nrDNA) variation. Annals of Botany, 95, 799–806.PubMedPubMedCentralCrossRefGoogle Scholar
  100. Mabberley, D. J. (1997). The plant-book, 2nd edn. Cambridge: Cambridge University Press.Google Scholar
  101. Maddison, W. P. (1997). Gene trees in species trees. Systematic Biology, 46, 523–536.CrossRefGoogle Scholar
  102. Mallet, J. (2007). Hybrid speciation. Nature, 446, 279–283.PubMedCrossRefGoogle Scholar
  103. Mansion, G., Rosenbaum, G., Schoenenberger, N., Bacchetta, G., Rosselló, J. A., & Conti, E. (2008). Phylogenetic analysis informed by geological history supports multiple, sequential invasions of the Mediterranean basin by the angiosperm family Araceae. Systematic Biology, 57, 269–285.PubMedCrossRefGoogle Scholar
  104. Marhold, K., & Lihová, J. (2006). Polyploidy, hybridization and reticulate evolution: lessons from the Brassicaceae. Plant Systematics and Evolution, 259, 143–174.CrossRefGoogle Scholar
  105. Mason-Gamer, R. J. (2004). Reticulate evolution, introgression, and intertribal gene capture in an allohexaploid grass. Systematic Biology, 53(1), 25–37.PubMedCrossRefGoogle Scholar
  106. Mason-Gamer, R. J., & Kellogg, E. A. (1996). Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Systematic Biology, 45(4), 524–545.CrossRefGoogle Scholar
  107. Mayol, M., & Rosselló, J. A. (2001). Why nuclear ribosomal DNA spacers (ITS) tell different stories in Quercus. Molecular Phylogenetics and Evolution, 19(2), 167–176.PubMedCrossRefGoogle Scholar
  108. McDade, L. A. (1995). Hybridization and phylogenetics. In P. C. Hoch & A. G. Stephenson (Eds.), Experimental and molecular approaches to plant biosystematics (pp. 305–331). St. Louis: Missouri Botanical Garden.Google Scholar
  109. Menezes, C. A. (1903). Diagnoses d’algumas plantas novas ou pouco conhecidas da ilha da Madeira. In A. Nobre (Ed.), Annaes de Sciencias Naturaes (Porto), vol. 8 (pp. 95–99). Porto: Tipographia Occidental.Google Scholar
  110. Menezes, C. A. (1908). Notice sur les espèces madériennes du genre Scrophularia. Funchal: “Diario Popular”.Google Scholar
  111. Meulenkamp, J. E., & Sissingh, W. (2003). Tertiary palaeogeography and tectonostratigraphic evolution of the northern and southern Peri-Tethys platforms and the intermediate domains of the African-Eurasian convergent plate boundary zone. Palaeogeography, Palaeoclimatology, Palaeoecology, 196, 209–228.CrossRefGoogle Scholar
  112. Miao, Y.-F., Herrmann, M., Wu, F.-L., Yan, X.-L., & Yang, S.-L. (2012). What controlled mid-late Miocene long-term aridification in Central Asia?—global cooling or Tibetan Plateau uplift: a review. Earth-Science Reviews, 112, 155–172.CrossRefGoogle Scholar
  113. Miller, K. G., Kominz, M. A., Browning, J. V., Wright, J. D., Mountain, G. S., Katz, M. E., et al. (2005). The Phanerozoic record of global sea-level change. Science, 310, 1293–1298.PubMedCrossRefGoogle Scholar
  114. Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE 2010) New Orleans, (pp. 1–8).Google Scholar
  115. Ming, Q.-Z. (2007). A study on the neotectonic division and environment evolution of Qing-zang Plateau and three parallel rivers area. Yunnan. Geology, 26(4), 387–396.Google Scholar
  116. Mittermeier, R. A., Gil, R. R., Hoffman, M., Pilgrim, J., Brooks, T., Mittermeier, C. G., Lamoreux, J., & da Fonseca, G. A. B. (Eds.) (2004). Hotspots revisited: Earth’s biologically richest and most threatened terrestrial ecoregions. CEMEX: Mexico D.F.Google Scholar
  117. Morrison, D. A. (2010). Using data-display networks for exploratory data analysis in phylogenetic studies. Molecular Biology and Evolution, 27(5), 1044–1057.PubMedCrossRefGoogle Scholar
  118. Mouthereau, F., Lacombe, O., & Vergés, J. (2012). Building the Zagros collisional orogen: timing, strain distribution and the dynamics of Arabia / Eurasia plate convergence. Tectonophysics, 532-535, 27–60.CrossRefGoogle Scholar
  119. Müller, K. (2005). SeqState - primer design and sequence statistics for phylogenetic DNA data sets. Applied Bioinformatics, 4(1), 65–69.PubMedCrossRefGoogle Scholar
  120. Müller, K., & Albach, D. C. (2010). Evolutionary rates in Veronica L. (Plantaginaceae): disentangling the influence of life history and breeding system. Journal of Molecular Evolution, 70, 44–56.PubMedCrossRefGoogle Scholar
  121. Murbeck, S. (1933). Monographie der Gattung Verbascum. Lund: H. Ohlsson.Google Scholar
  122. Navarro Pérez, M. L., López, J., Fernández Mazuecos, M., Rodríguez Riaño, T., Vargas, P., & Ortega Olivencia, A. (2013). The role of birds and insects in pollination shifts of Scrophularia (Scrophulariaceae). Molecular Phylogenetics and Evolution, 69, 239–254.PubMedCrossRefGoogle Scholar
  123. Nei, M., & Rooney, A. P. (2005). Concerted and birth-and-death evolution of multigene families. Annual Review of Genetics, 39, 121–152.PubMedPubMedCentralCrossRefGoogle Scholar
  124. Nie, Z.-L., Sun, H., Beardsley, P. M., Olmstead, R. G., & Wen, J. (2006). Evolution of biogeographic disjunction between Eastern Asia and Eastern North America in Phryma (Phrymaceae). American Journal of Botany, 93(9), 1343–1356.PubMedCrossRefGoogle Scholar
  125. Nie, Z.-L., Wen, J., Sun, H., & Bartholomew, B. (2005). Monophyly of Kellogia Torrey ex Benth. (Rubiaceae) and evolution of its intercontinental disjunction between Western North America and Eastern Asia. American Journal of Botany, 92(4), 642–652.PubMedCrossRefGoogle Scholar
  126. Nieto Feliner, G., & Rosselló, J. A. (2007). Better the devil you know? Guidelines for insightful utilization of nrDNA ITS in species-level evolutionary studies in plants. Molecular Phylogenetics and Evolution, 44, 911–919.PubMedCrossRefGoogle Scholar
  127. Nylander, J. A. A. (2004). MrModeltest version 2. Accessed 23 April 2013.
  128. Okuyama, Y., Fujii, N., Wakabayashi, M., Kawakita, A., Ito, M., Watanabe, M., et al. (2005). Nonuniform concerted evolution and chloroplast capture: heterogeneity of observed introgression patterns in three molecular data partition phylogenies of Asian Mitella (Saxifragaceae). Molecular Biology and Evolution, 22, 285–296.PubMedCrossRefGoogle Scholar
  129. Olteanu, R., & Jipa, D. C. (2006). Dacian basin environmental evolution during upper Neogene within the Paratethys domain. Geo-Eco-Marina, 12, 91–105.Google Scholar
  130. Ortega Olivencia, A. (2009). Scrophularia. In C. Benedí, E. Rico, J. Güemes, & A. Herrero (Eds.), Flora Iberica, vol. 13 (pp. 97–134). Madrid: Real Jardín Botánico, CSIC.Google Scholar
  131. Oxelman, B., Kornhall, P., Olmstead, R. G., & Bremer, B. (2005). Further disintegration of Scrophulariaceae. Taxon, 54, 411–425.CrossRefGoogle Scholar
  132. Payseur, B. A., & Rieseberg, L. H. (2016). A genomic perspective on hybridization and speciation. Molecular Ecology, 25(11), 2337–2360.PubMedPubMedCentralCrossRefGoogle Scholar
  133. Peng, D., & Wang, X.-Q. (2008). Reticulate evolution in Thuja inferred from multiple gene sequences: implications for the study of biogeographical disjunction between eastern Asia and North America. Molecular Phylogenetics and Evolution, 47, 1190–1202.PubMedCrossRefGoogle Scholar
  134. Pennell, F. W. (1943). The Scrophulariaceae of the Western Himalayas: The Academy of Natural Sciences of Philadelphia Monographs number 5. Lancaster, Pennsylvania: Wickersham Printing Company.Google Scholar
  135. Pirie, M. D., Humphreys, A. M., Barker, N. P., & Linder, H. P. (2009). Reticulation, data combination, and inferring evolutionary history: an example from Danthonioideae (Poaceae). Systematic Biology, 58, 612–628.PubMedCrossRefGoogle Scholar
  136. Pirie, M. D., Humphreys, A. M., Galley, C., Barker, N. P., Verboom, G. A., Orlovich, D., et al. (2008). A novel supermatrix approach improves resolution of phylogenetic relationships in a comprehensive sample of danthonioid grasses. Molecular Phylogenetics and Evolution, 48, 1106–1119.PubMedCrossRefGoogle Scholar
  137. Popov, S. V., Rögl, F., Rozanov, A. Y., Steininger, F. F., Shcherba, I. G., Kovac, M. (Eds.) (2004). Lithological-Paleogeographic maps of Paratethys, 10 maps Late Eocene to Pliocene, Courier Forschungsinstitut Senckenberg 250. Stuttgart: E. Schweizerbart.Google Scholar
  138. Potts, A. J., Hedderson, T. A., & Grimm, G. W. (2014). Constructing phylogenies in the presence of intra-individual site polymorphisms (2ISPs) with a focus on the nuclear ribosomal cistron. Systematic Biology, 63(1), 1–16.PubMedCrossRefGoogle Scholar
  139. Qi, Y., & Yang, Y.-H. (1999). Topographic effect on spatial variation of plant diversity in California. Geographic Information Sciences, 5(1), 39–46.Google Scholar
  140. Qian, H., & Ricklefs, R. E. (2000). Large-scale processes and the Asian bias in species diversity of temperate plants. Nature, 407, 180–182.PubMedCrossRefGoogle Scholar
  141. Qiu, Y.-X., Fu, C.-X., & Comes, H. P. (2011). Plant molecular phylogeography in China and adjacent regions: tracing the genetic imprints of Quaternary climate and environmental change in the world’s most diverse temperate flora. Molecular Phylogenetics and Evolution, 59, 225–244.PubMedCrossRefGoogle Scholar
  142. Quézel, P. (1985). Definition of the Mediterranean region and origin of its flora. In C. Gomez-Campo (Ed.), Plant conservation in the Mediterranean area (pp. 9–24). Dordrecht: Kluwer.Google Scholar
  143. 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.CrossRefGoogle Scholar
  144. Richardson, A. O., & Palmer, J. D. (2007). Horizontal gene transfer in plants. Journal of Experimental Botany, 58(1), 1–9.PubMedCrossRefGoogle Scholar
  145. Rieseberg, L. H. (1991). Homoploid reticulate evolution in Helianthus (Asteraceae): evidence from ribosomal genes. American Journal of Botany, 78(9), 1218–1237.CrossRefGoogle Scholar
  146. Rieseberg, L. H., & Wendel, J. F. (1993). Introgression and its consequences in plants. In R. Harrison (Ed.), Hybrid zones and the evolutionary process (pp. 70–109). New York: Oxford University Press.Google Scholar
  147. Rieseberg, L. H., Whitton, J., & Linder, C. R. (1996). Molecular marker incongruence in plant hybrid zones and phylogenetic trees. Acta Botanica Neerlandica, 45(3), 243–262.CrossRefGoogle Scholar
  148. Roe, G. H. (2005). Orographic precipitation. Annual Review of Earth and Planetary Sciences, 33, 645–671.CrossRefGoogle Scholar
  149. Rojas Andrés, B. M., Albach, D. C., & Martínez Ortega, M. M. (2015). Exploring the intricate evolutionary history of the diploid–polyploid complex Veronica subsection Pentasepalae (Plantaginaceae). Botanical Journal of the Linnean Society, 179, 670–692.CrossRefGoogle Scholar
  150. Rokas, A., Williams, B. L., King, N., & Carroll, S. B. (2003). Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature, 425, 798–804.PubMedCrossRefGoogle Scholar
  151. Ronquist, F. (1997). Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology, 46, 195–203.CrossRefGoogle Scholar
  152. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.PubMedPubMedCentralCrossRefGoogle Scholar
  153. Rosselló, J. A., Lázaro, A., Cosín, R., & Molins, A. (2007). A phylogeographic split in Buxus balearica (Buxaceae) as evidenced by nuclear ribosomal markers: when ITS paralogues are welcome. Journal of Molecular Evolution, 64, 143–157.PubMedCrossRefGoogle Scholar
  154. Sanmartín, I. (2003). Dispersal vs. vicariance in the Mediterranean: historical biogeography of the Palearctic Pachydeminae (Coleoptera, Scarabaeoidea). Journal of Biogeography, 30, 1883–1897.CrossRefGoogle Scholar
  155. Schäferhoff, B., Fleischmann, A., Fischer, E., Albach, D. C., Borsch, T., Heubl, G., et al. (2010). Towards resolving Lamiales relationships: insights from rapidly evolving chloroplast sequences. BMC Evolutionary Biology, 10, 352.PubMedPubMedCentralCrossRefGoogle Scholar
  156. Scherson, R. A., Vidal, R., & Sanderson, M. J. (2008). Phylogeny, biogeography, and rates of diversification of New World Astragalus (Leguminosae) with an emphasis on South American radiations. American Journal of Botany, 95, 1030–1039.PubMedCrossRefGoogle Scholar
  157. Scheunert, A., & Heubl, G. (2011). Phylogenetic relationships among New World Scrophularia L. (Scrophulariaceae): new insights inferred from DNA sequence data. Plant Systematics and Evolution, 291, 69–89.CrossRefGoogle Scholar
  158. Scheunert, A., & Heubl, G. (2014). Diversification of Scrophularia (Scrophulariaceae) in the Western Mediterranean and Macaronesia - phylogenetic relationships, reticulate evolution and biogeographic patterns. Molecular Phylogenetics and Evolution, 70, 296–313.PubMedCrossRefGoogle Scholar
  159. Schnabel, A., McDonel, P. E., & Wendel, J. F. (2003). Phylogenetic relationships in Gleditsia (Leguminosae) based on ITS sequences. American Journal of Botany, 90(2), 310–320.PubMedCrossRefGoogle Scholar
  160. Seehausen, O. (2004). Hybridization and adaptive radiation. Trends in Ecology and Evolution, 19, 198–207.PubMedCrossRefGoogle Scholar
  161. Shaw, R. J. (1962). The biosystematics of Scrophularia in Western North America. Aliso, 5, 147–178.Google Scholar
  162. Silvestro, D., & Michalak, I. (2012). RaxmlGUI: a graphical front-end for RAxML. Organisms Diversity & Evolution, 12, 335–337.CrossRefGoogle Scholar
  163. Simmons, M. P., & Ochoterena, H. (2000). Gaps as characters in sequence-based phylogenetic analyses. Systematic Biology, 49(2), 369–381.PubMedCrossRefGoogle Scholar
  164. Sobel, E. R., Chen, J., & Heermance, R. V. (2006). Late Oligocene–Early Miocene initiation of shortening in the Southwestern Chinese Tian Shan: implications for Neogene shortening rate variations. Earth and Planetary Science Letters, 247, 70–81.CrossRefGoogle Scholar
  165. Soltis, P. S., & Soltis, D. E. (2009). The role of hybridization in plant speciation. Annual Review of Plant Biology, 60, 561–588.PubMedCrossRefGoogle Scholar
  166. Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22(21), 2688–2690.PubMedCrossRefGoogle Scholar
  167. Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9), 1312–1313.PubMedPubMedCentralCrossRefGoogle Scholar
  168. Stebbins, G. L. (1959). The role of hybridization in evolution. Proceedings of the American Philosophical Society, 103(2), 231–251.Google Scholar
  169. Steiner, K. E. (1996). Chromosome numbers and relationships in tribe Hemimerideae (Scrophulariaceae). Systematic Botany, 21(1), 63–76.CrossRefGoogle Scholar
  170. Stephens, M., Smith, N. J., & Donnelly, P. (2001). A new statistical method for haplotype reconstruction from population data. The American Journal of Human Genetics, 68(4), 978–989.PubMedCrossRefGoogle Scholar
  171. Stiefelhagen, H. (1910). Systematische und pflanzengeographische Studien zur Kenntnis der Gattung Scrophularia. Engler’s. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie, 44, 406–496.Google Scholar
  172. Sun, B.-N., Wu, J.-Y., Liu, Y.-S. C., Ding, S.-T., Li, X.-C., Xie, S.-P., et al. (2011). Reconstructing Neogene vegetation and climates to infer tectonic uplift in western Yunnan, China. Palaeogeography, Palaeoclimatology, Palaeoecology, 304, 328–336.CrossRefGoogle Scholar
  173. Sun, Y.-S., Wang, A.-L., Wan, D.-S., Wang, Q., & Liu, J.-Q. (2012). Rapid radiation of Rheum (Polygonaceae) and parallel evolution of morphological traits. Molecular Phylogenetics and Evolution, 63, 150–158.PubMedCrossRefGoogle Scholar
  174. Swofford, D. L. (2003). PAUP*: Phylogenetic Analysis Using Parsimony (* and other methods) version 4. Accessed 23 April 2013.
  175. Taberlet, P., Gielly, L., Pautou, G., & Bouvet, J. (1991). Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology, 17, 1105–1109.PubMedCrossRefGoogle Scholar
  176. Takhtajan, A. (1986). Floristic regions of the World. Berkeley: University of California Press.Google Scholar
  177. Tank, D. C., & Olmstead, R. G. (2008). From annuals to perennials: phylogeny of subtribe Castillejinae (Orobanchaceae). American Journal of Botany, 95(5), 608–625.PubMedCrossRefGoogle Scholar
  178. Thompson, J. D. (2005). Plant evolution in the Mediterranean. Oxford: Oxford University Press.CrossRefGoogle Scholar
  179. Tiffney, B. H., & Manchester, S. R. (2001). The use of geological and paleontological evidence in evaluating plant phylogeographic hypotheses in the Northern Hemisphere Tertiary. International Journal of Plant Sciences, 162(S6), S3–S17.CrossRefGoogle Scholar
  180. Vaarama, A., & Hiirsalmi, H. (1967). Chromosome studies on some Old World species of the genus Scrophularia. Hereditas, 58, 333–358.CrossRefGoogle Scholar
  181. Valtueña, F. J., López, J., Álvarez, J., Rodríguez Riaño, T., & Ortega Olivencia, A. (2016). Scrophularia arguta, a widespread annual plant in the Canary Islands: a single recent colonization event or a more complex phylogeographic pattern? Ecology and Evolution, 6(13), 4258–4273.PubMedPubMedCentralCrossRefGoogle Scholar
  182. van der Niet, T., & Linder, H. P. (2008). Dealing with incongruence in the quest for the species tree: a case study from the orchid genus Satyrium. Molecular Phylogenetics and Evolution, 47, 154–174.PubMedCrossRefGoogle Scholar
  183. Vargas, P., Carrió, E., Guzmán, B., Amat, E., & Güemes, J. (2009). A geographical pattern of Antirrhinum (Scrophulariaceae) speciation since the Pliocene based on plastid and nuclear DNA polymorphisms. Journal of Biogeography, 36, 1297–1312.CrossRefGoogle Scholar
  184. Verboom, G. A., Herron, M. L., Moncrieff, G. R., & Slingsby, J. A. (2016). Maintenance of species integrity in the context of a recent radiation: the case of Jamesbrittenia (Scrophulariaceae: Limoselleae) in southern Africa. Botanical Journal of the Linnean Society, 182, 115–139.CrossRefGoogle Scholar
  185. Volkov, R. A., Komarova, N. Y., & Hemleben, V. (2007). Ribosomal DNA in plant hybrids: inheritance, rearrangement, expression. Systematics and Biodiversity, 5(3), 261–276.CrossRefGoogle Scholar
  186. Vriesendorp, B., & Bakker, F. T. (2005). Reconstructing patterns of reticulate evolution in angiosperms: what can we do? Taxon, 54, 593–604.CrossRefGoogle Scholar
  187. Wang, C.-S., Dai, J.-G., Zhao, X.-X., Li, Y.-L., Graham, S. A., He, D.-F., et al. (2014). Outward-growth of the Tibetan Plateau during the Cenozoic: a review. Tectonophysics, 621, 1–43.CrossRefGoogle Scholar
  188. Wang, L., Wu, Z.-Q., Bystriakova, N., Ansell, S. W., Xiang, Q.-P., Heinrichs, J., et al. (2011). Phylogeography of the Sino-Himalayan fern Lepisorus clathratus on “The Roof of the World”. PloS One, 6(9), e25896.PubMedPubMedCentralCrossRefGoogle Scholar
  189. Weisrock, D. W., Smith, S. D., Chan, L. M., Biebouw, K., Kappeler, P. M., & Yoder, A. D. (2012). Concatenation and concordance in the reconstruction of mouse lemur phylogeny: an empirical demonstration of the effect of allele sampling in phylogenetics. Molecular Biology and Evolution, 29(6), 1615–1630.PubMedPubMedCentralCrossRefGoogle Scholar
  190. Wen, J., Ickert-Bond, S. M., Nie, Z.-L., & Li, R. (2010). Timing and modes of evolution of Eastern Asian – North American biogeographic disjunctions in seed plants. In M.-Y. Long, H.-Y. Gu, & Z.-H. Zhou (Eds.), Darwin’s heritage today: proceedings of the Darwin 200 Beijing International Conference (pp. 252–269). Beijing: Higher Education.Google Scholar
  191. Wen, J., Zhang, J.-Q., Nie, Z.-L., Zhong, Y., & Sun, H. (2014). Evolutionary diversifications of plants on the Qinghai-Tibetan Plateau. Frontiers in Genetics, 5, 4.PubMedPubMedCentralGoogle Scholar
  192. Wendel, J. F., & Doyle, J. J. (1998). Phylogenetic incongruence: window into genome history and molecular evolution. In D. E. Soltis, P. S. Soltis, & J. J. Doyle (Eds.), Molecular systematics of plants II: DNA sequencing (pp. 265–296). Dordrecht: Kluwer.CrossRefGoogle Scholar
  193. Whittall, J., Liston, A., Gisler, S., & Meinke, R. J. (2000). Detecting nucleotide additivity from direct sequences is a SNAP: an example from Sidalcea (Malvaceae). Plant Biology, 2, 211–217.CrossRefGoogle Scholar
  194. Willis, J. C. (1973). A dictionary of the flowering plants and ferns, 8th edn. Cambridge: Cambridge University Press.Google Scholar
  195. Wolfe, A. D., & Elisens, W. J. (1994). Nuclear ribosomal DNA restriction-site variation in Penstemon section Peltanthera (Scrophulariaceae): an evaluation of diploid hybrid speciation and evidence for introgression. American Journal of Botany, 81(12), 1627–1635.CrossRefGoogle Scholar
  196. Wright, S. I., Kalisz, S., & Slotte, T. (2013). Evolutionary consequences of self-fertilization in plants. Proceedings of the Royal Society of London B, 280(1760), 20130133.CrossRefGoogle Scholar
  197. Wright, S. I., Lauga, B., & Charlesworth, D. (2002). Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Molecular Biology and Evolution, 19(9), 1407–1420.PubMedCrossRefGoogle Scholar
  198. Xiang, Q.-Y., Soltis, D. E., & Soltis, P. S. (1998). The Eastern Asian and Eastern and Western North American floristic disjunction: congruent phylogenetic patterns in seven diverse genera. Molecular Phylogenetics and Evolution, 10(2), 178–190.PubMedCrossRefGoogle Scholar
  199. Xiao, L.-Q., Möller, M., & Zhu, H. (2010). High nrDNA ITS polymorphism in the ancient extant seed plant Cycas: incomplete concerted evolution and the origin of pseudogenes. Molecular Phylogenetics and Evolution, 55, 168–177.PubMedCrossRefGoogle Scholar
  200. Yang, F.-S., Qin, A.-L., Li, Y.-F., & Wang, X.-Q. (2012). Great genetic differentiation among populations of Meconopsis integrifolia and its implication for plant speciation in the Qinghai-Tibetan Plateau. PloS One, 7(5), e37196.PubMedPubMedCentralCrossRefGoogle Scholar
  201. Yu, Y., Harris, A. J., & He, X.-J. (2010). S-DIVA (statistical dispersal–vicariance analysis): a tool for inferring biogeographic histories. Molecular Phylogenetics and Evolution, 56, 848–850.PubMedCrossRefGoogle Scholar
  202. Yu, Y., Harris, A. J., & He, X.-J. (2014). RASP (Reconstruct Ancestral State in Phylogenies) version 2. Accessed 23 April 2013.
  203. Yuan, D.-Y., Ge, W.-P., Chen, Z.-W., Li, C.-Y., Wang, Z.-C., Zhang, H.-P., et al. (2013). The growth of northeastern Tibet and its relevance to large-scale continental geodynamics: a review of recent studies. Tectonics, 32, 1358–1370.CrossRefGoogle Scholar
  204. Yue, J.-P., Sun, H., Baum, D. A., Li, J.-H., Al-Shehbaz, I. A., & Ree, R. (2009). Molecular phylogeny of Solms-laubachia (Brassicaceae) s.l., based on multiple nuclear and plastid DNA sequences, and its biogeographic implications. Journal of Systematics and Evolution, 47(5), 402–415.CrossRefGoogle Scholar
  205. Yue, J.-X., Li, J.-P., Wang, D., Araki, H., Tian, D.-C., & Yang, S.-H. (2010). Genome-wide investigation reveals high evolutionary rates in annual model plants. BMC Plant Biology, 10, 242.PubMedPubMedCentralCrossRefGoogle Scholar
  206. Zhang, J.-Q., Meng, S.-Y., Allen, G. A., Wen, J., & Rao, G.-Y. (2014). Rapid radiation and dispersal out of the Qinghai-Tibetan Plateau of an alpine plant lineage Rhodiola (Crassulaceae). Molecular Phylogenetics and Evolution, 77, 147–158.PubMedCrossRefGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2017

Authors and Affiliations

  1. 1.Systematic Botany and Mycology, Department Biology I, and GeoBio-Center LMULudwig-Maximilians-University MunichMunichGermany

Personalised recommendations