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Phylogeny and biogeography of the genus Stevia (Asteraceae: Eupatorieae): an example of diversification in the Asteraceae in the new world

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Abstract

The genus Stevia comprises approximately 200 species, which are distributed in North and South America, and are representative of the species diversity of the Asteraceae in the New World. We reconstructed the phylogenetic relationships using sequences of ITS and cpDNA and estimated the divergence times of the major clade of this genus. Our results suggested that Stevia originated in Mexico 7.0–7.3 million years ago (Mya). Two large clades, one with shrub species and another with herb species, were separated at about 6.6 Mya. The phylogenetic reconstruction suggested that an ancestor of Stevia was a small shrub in temperate pine–oak forests and the evolutionary change from a shrub state to a herb state occurred only once. A Brazilian clade was nested in a Mexican herb clade, and its origin was estimated to be 5.2 Mya, suggesting that the migration from North America to South America occurred after the formation of the Isthmus of Panama. The species diversity in Mexico appears to reflect the habitat diversity within the temperate pine–oak forest zone. The presence of many conspecific diploid–polyploid clades in the phylogenetic tree reflects the high frequency of polyploidization among the perennial Stevia species.

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  • 17 July 2017

    An erratum to this article has been published.

References

  • Axelrod DI (1958) Evolution of the Madro-Tertiary geoflora. Bot Rev 24:433–509

    Article  Google Scholar 

  • Bacon CD, Silvestro D, Jaramillo C, Smith BT, Chakrabarty P (2015) Biological evidence supports and early and complex emergence of the Isthmus of Panama. Proc Natl Acad Sci USA 112:6110–6115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baldwin BG (1992) Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: an example from the Compositae. Mol Phylogenet Evol 1:3–16

    Article  CAS  PubMed  Google Scholar 

  • Baldwin BG, Sanderson MJ (1998) Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proc Natl Acad Sci USA 95:9402–9406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Becerra JX (2005) Timing the origin and expansion of the Mexican tropical dry forest. Proc Natl Acad Sci USA 102:10919–10923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bremer K (1994) Asteraceae—cladistics and classification. Timber Press, Portland

    Google Scholar 

  • Bush MB, Piperno DR, Colinvaux PA, De Oliveris PE, Krissek LA, Miller MA, Rowe WE (1992) A 14,300 year paleoecological profile of a lowland tropical lake in Panama. Ecol Monogr 62:251–275

    Article  Google Scholar 

  • Crawford DJ, Tadesse M, Kimball R, Carrillo-Reyes P, Sánchez-Vega I, Mort ME (2014) Coreopsis sect. Pseudoagarista (Asteraceae: Coreopsideae): molecular phylogeny, chromosome numbers, and comments on taxonomy and distribution. Taxon 63:1092–1102

    Article  Google Scholar 

  • Demesure B, Sodzi N, Petit RJ (1995) A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Mol Ecol 4:129–131

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid isolation procedure from small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF (2008) Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet 42:443–461

    Article  CAS  PubMed  Google Scholar 

  • Farris JS, Källersjö M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10:315–319

    Article  Google Scholar 

  • Ferrari L, Lopez-Martinez M, Aguirre-Diaz G, Carrasco-Nunez G (1999) Space-time patterns of Cenozoic arc volcanism in central Mexico: from the Sierra Madre occidental to the Mexican volcanic belt. Geology 27:303–306

    Article  Google Scholar 

  • Ferrari L, Conticelli S, Vaggelli G, Petrone CM, Manetti P (2000) Late Miocene volcanism and intra-arc tectonics during the early development of the Trans-Mexican volcanic belt. Tectonophysics 318:161–185

    Article  CAS  Google Scholar 

  • Fofana B, Harvengt L, Baudoin JP, Du Jardin P (1997) New primers for the polymerase chain amplification of cpDNA intergenic spacers in Phaseolus phylogeny. Belg J Bot 129:118–122

    Google Scholar 

  • Funk VA, Bayer RJ, Keeley S, Chan R, Watson L, Gemeinholzer B, Schilling E, Panero JL, Baldwin BG, Garcia-Jacas N, Susanna A, Jansen RK (2005) Everywhere but Antarctica: using a supertree to understand the diversity and distribution of the Compositae. Biologiske Skrifter 55:343–374

    Google Scholar 

  • Funk VA, Susanna A, Stuessy TF, Robinson H (2009a) Classification of Compositae. In: Funk V, Susanna A, Stuessy TF, Bayer RJ (eds) Systematics, evolution and biogeography of Compositae. International Association for Plant Taxonomy, Institute of Botany, University of Vienna, Vienna, pp 171–189

    Google Scholar 

  • Funk VA et al (2009b) Compositae metatrees: the next generation. In: Funk V, Susanna A, Stuessy TF, Bayer RJ (eds) Systematics, evolution and biogeography of Compositae. International Association for Plant Taxonomy, Institute of Botany, University of Vienna, Vienna, pp 747–777

    Google Scholar 

  • Gentry AH (1982) Neotropical floristic diversity: phytogeographical connections between Central and South America, Pleistocene climatic fluctuation, or an accident of the Andean orogeny? Ann Missouri Bot Gard 69:557–593

    Article  Google Scholar 

  • Gottlieb LD (1981) Gene number in species of Astereae that have different chromosome numbers. Proc Natl Acad Sci USA 78:3726–3729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gottlieb LD (2004) Rethinking classic examples of recent speciation in plants. New Phytol 161:71–82

    Article  Google Scholar 

  • Graham A (1989) Paleofloristic and paleoclimatic changes in the Tertiary of northern Latin America. Rev Paleobot Palynol 60:283–293

    Article  Google Scholar 

  • Graham A (1996) A contribution to the geologic history of the Compositae. In: Hind DJN, Beentje HJ (eds) Proceedings of the International Compositae Conference, Kew, 1994, vol. 1, Compositae: Systematics. Royal Bot Gardens, Kew, pp 123–140

  • Graham A (1999) The tertiary history of the northern temperate element in the northern Latin American biota. Am J Bot 86:32–38

    Article  CAS  PubMed  Google Scholar 

  • Grashoff JL (1972) A Systematic Study of the North and Central American species of Stevia. Ph.D. dissertation, Univ. of Texas, Austin

  • Gutiérrez DG, Muñoz-Schick M, Grossi MA, Rodríguez-Cravero JF, Morales V, Moreira-Muñoz A (2016) The genus Stevia (Eupatorieae, Asteraceae) in Chile: a taxonomical and morphological analysis. Phytotaxa 282:1–18

    Article  Google Scholar 

  • Heywood VH (2009) The recent history of Compositae systematics: from daisies to deep achenes, sister groups and metatrees. In: Funk V, Susanna A, Stuessy TF, Bayer RJ (eds) Systematics, evolution and biogeography of Compositae. International Association for Plant Taxonomy, Institute of Botany, University of Vienna, Vienna, pp 39–44

    Google Scholar 

  • Hind DJN, Robinson H (2007) Eupatorieae. In: Kubitzki K (ed) The families and genera of vascular plants, vol 8. Springer, Berlin, pp 510–574

    Google Scholar 

  • Inoue J, dos Reis M, Yang Z (2011) A step-by-step tutorial: Divergence time estimation with approximate likelihood calculation using MCMCTREE in PAML. http://abacus.gene.ucl.ac.uk/software/paml.html

  • Ito M, Yahara T, King RM, Watanabe K, Oshita S, Yokoyama J, Crawford DJ (2000) Molecular phylogeny of Eupatorieae (Asteraceae) estimated from cpDNA RFLP and its implication for the polyploid origin hypothesis of the tribe. J Plant Res 113:91–96

    Article  CAS  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keigwyn LDJr (1978) Pliocene closing of the Isthmus of Panama, based on biostratigraphic evidence from nearby Pacific Ocean and Caribbean Sea cores. Geology 6:630–634

    Article  Google Scholar 

  • King RM, Robinson H (1987) The Genera of the Eupatorieae (Asteraceae). Monographs in systematic botany from the Missouri botanical garden 22. Allen Press, Inc., Lawrence

    Google Scholar 

  • Leigh EG, O’Dea A, Vermeij GJ (2014) Historical biogeography of teh isthmus of Panama. Biol Rev 89:148–172

    Article  PubMed  Google Scholar 

  • Liu JQ, Wang YJ, Wang AL, Ohba H, Abbott RJ (2006) Radiation and diversification within the Ligularia–Cremanthodium–Parasenecio complex (Asteraceae) triggered by uplift of the Qinghai–Tibetan Plateau. Mol Phylogenetics Evol 38:31–49

    Article  CAS  Google Scholar 

  • Lozano-García S, Sosa-Nájera S, Sugiura Y, Caballero M (2005) 23,000 year of vegetation history of the Upper Lerma, a tropical high-altitude basin in Central Mexico. Quatern Res 64:70–82

    Article  Google Scholar 

  • Mastretta-Yanes A, Moreno-Letelier A, Piñero D, Jorgensen TH, Emerson BC (2015) Biodiversity in the Mexican highlands and the interaction of geology, geography and climate within the Trans-Mexican Volcanic Belt. J Biogeogr 42:1586–1600

    Article  Google Scholar 

  • Montes C, Cardona A, Jaramillo C, Pardo A, Silva JC, Valencia V, Ayala C, Pérez-Angel LC, Rodriguez-Parra LA, Ramirez V, Niño H (2015) Middle Miocene closure of the Central American Seaway. Science 348:226–229

    Article  CAS  PubMed  Google Scholar 

  • Nakamura I, Kameya N, Kato Y, Yamanaka S, Jomori H, Sato Y (1997) A proposal for identifying the short ID sequence which addresses the plastid subtype of higher plants. Breed Sci 47:385–388

    CAS  Google Scholar 

  • Ooi K, Endo Y, Yokoyama J, Murakami N (1995) Useful primer designs to amplify DNA fragments of the plasmid gene matK from angiosperm plants. J Jpn Bot 70:328–331

    Google Scholar 

  • Panero JL, Crozier BS (2016) Macroevolutionary dynamics in the early diversification of Asteraceae. Mol Phylogenetics Evol 99:116–132

    Article  Google Scholar 

  • Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. http://abacus.gene.ucl.ac.uk/software/paml.html

  • Rannala B, Yang Z (2007) Inferring speciation times under an episodic molecular clock. Syst Biol 56:453–466

    Article  PubMed  Google Scholar 

  • Richardson JE, Pennington, RT, Pennington TD, Hollingsworth PM (2001) Rapid diversification of a species-rich genus of neotropical rain forest trees. Science 293:2242–2245

    Article  CAS  PubMed  Google Scholar 

  • Rieseberg LH, Willis JH (2007) Plant speciation. Science 317:910–914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, Nakazato T, Durphy JL, Schwarzbach AE, Donovan LA, Lexer C (2003) Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301:1211–1216

    Article  CAS  PubMed  Google Scholar 

  • Rivera VL, Panero JL, Schilling EE, Crozier BS, Moraes MD (2016) Origins and recent radiation of Brazilian Eupatorieae (Asteraceae) in the eastern Cerrado and Atlantic Forest. Mol Phylogenet Evol 97:90–100

    Article  PubMed  Google Scholar 

  • Robinson BL (1930) Observations on the genus Stevia. Contrib Gray Herb Harv Univ 90:36–58 (1pl)

    Google Scholar 

  • Robinson H, Schilling E, Paneno JL (2009) Eupatorieae. In: Funk V, Susanna A, Stuessy TF, Bayer RJ (eds) Systematics, evolution and biogeography of Compositae. International Association for Plant Taxonomy, Institute of Botany, University of Vienna, Vienna, pp 731–744

    Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed  PubMed Central  Google Scholar 

  • Rzedowski GC, Rzedowski J (2001) Flora fanerogamia del Valle de Mexico. Instituto de Ecologia, A.C., Patzcuaro

    Google Scholar 

  • Schilling EE, Panero JL, Crozier BS, Scott RW, Dávila P (2015) Bricklebush (Brickellia) phylogeny reveals dimensions of the great Asteraceae radiation in Mexico. Mol Phyl Evol 85:161–170

    Article  Google Scholar 

  • Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464

    Article  Google Scholar 

  • Semple JC, Watanabe K (2009) A review of chromosome numbers in the Asteraceae with hypotheses on chromosome base number ebolution. In: Funk V, Susanna A, Stuessy TF, Bayer RJ (eds) Systematics, evolution, and biogeography of Compositae, IAPT, Vienna, pp 61–72

    Google Scholar 

  • Shimodaira H (2002) An approximately unbiased test of phylogenetic tree selection. Syst Biol 51:492–508

    Article  PubMed  Google Scholar 

  • Shimodaira H, Hasegawa M (2001) CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17:1246–1247

    Article  CAS  PubMed  Google Scholar 

  • Soejima A, Yahara T, Watanabe K (2001a) Distribution and variation of sexual and agamospermous populations of Stevia (Asteraceae: Eupatorieae) in the lower latitudes, Mexico. Plant Species Biol 16:91–105

    Article  Google Scholar 

  • Soejima A, Yahara T, Watanabe K (2001b) Thirteen new species and two new combinations of Stevia (Asteraceae: Eupatorieae) from Mexico. Brittonia 53:377–395

    Article  Google Scholar 

  • Soltis DE, Soltis PS, Pires JC, Kovarik A, Tate JA, Mavrodiv E (2004) Recent and recurrent polyploidy in Tragopogon (Asteraceae): cytohenetic, genomic and genetic comparisons. Biol J Linn Soc 82:485–501

    Article  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. doi:10.1093/bioinformatics/btu033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stebbins GL (1950) Variation and evolution in plants. Columbia University Press, New York

    Google Scholar 

  • Swofford DL (2003) PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer, Sunderland

    Google Scholar 

  • Tanabe AS (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proporrional, and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Mol Eco Resour 11:914–921

    Article  Google Scholar 

  • Turner BL (1997) The Comps of Mexico. A systematic account of the family Asteracerae. vol. 1. Eupatorieae. Phytologia Memoirs vol. 11

  • Valiente-Banuet A, Flores-Hernández N, Verdú M, Dávila P (1998) The chaparral vegetation in Mexico under nonmediterranean climate: the convergence and Madrean–Tethyan hypotheses reconsidered. Am J Bot 85:1398–1408

    Article  CAS  PubMed  Google Scholar 

  • Wang XR, Tsumura H, Yoshimaru K, Nagasaka K, Szmidt AE (1999) Phylogenetic relationships of Eurasian pines (Pinus, Pinaceae) based on chloroplast rbcL, matK, rpl20-rps18 spacer, and trnV intron sequences. Am J Bot 86:1742–1753

    Article  CAS  PubMed  Google Scholar 

  • Watanabe K (2008) Index to Chromosome Numbers in Asteraceae. http://www.lib.kobe-u.ac.jp/products/asteraceae/index.html.

  • Watanabe K, King RM, Yahara T, Ito M, Yokoyama J, Suzuki T, Crawford DJ (1995) Chromosomal cytology and evolution in Eupatorieae (Asteraceae). Ann Missouri Bot Gard 82:581–592

    Article  Google Scholar 

  • Watanabe K, Yahara T, Soejima A, Ito M (2001) Mexican species of the genus Stevia (Eupatorieae, Asteraceae): chromosome numbers and geographical distribution. Plant Species Biol 16:49–68

    Article  Google Scholar 

  • Watanabe K, Yahara T, Hashimoto G, Nagatani Y, Soejima A, Kawahara T, Nakazawa M (2007) Chromosome numbers and karyotypes in Asteraceae. Ann Missouri Bot Gard 94:643–654

    Article  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M et al (eds) PCR protocols: a guide to methods and application. Academic, San Diego, pp 315–322

    Google Scholar 

  • Willis KJ, Whittaker RJ (2002) Species diversity—Scale matters. Science 295:1245–1248

    Article  CAS  PubMed  Google Scholar 

  • Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank M. Ito, T. Kajita, S. Kobayashi, T. Miyake, and K. Ooi for their help with fieldwork in Mexico; K. Oyama for logistical support in Mexico; Y. Nagatani and the late G. Hashimoto for their assistance with locating Brazilian populations of Stevia; H. Shibuya, M. Miya, and D. Honda for advice regarding statistical analyses; and E. Kamitani for assistance with DNA sequencing. We would also like to thank the following herbaria for access to herbarium materials: the National Herbarium of Mexico at the UNAM (MEXU), the University of Texas Herbarium (TEX), and the Goro Hashimoto Herbarium (São Paulo, Brazil). The present study was supported in part by a Grant in Aid for Scientific Research (No. 14405014), which was provided by the Ministry of Education, Science, and Culture, Japan.

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Authors and Affiliations

  1. Department of Biological Science, Faculty of Advanced Science and Technology, Kumamoto University, Kumamoto, 860-8555, Japan

    Akiko Soejima

  2. Department of Biology, Graduate School of Science, Kobe University, Kobe, 657-8501, Japan

    Akifumi S. Tanabe & Kuniaki Watanabe

  3. Department of Biology, Graduate School of Science, Kyushu University, Fukuoka, 819-0395, Japan

    Izumi Takayama, Miyuki Nakazawa & Tetsukazu Yahara

  4. Hokkaido Research Center, Forestry and Forest Products Research Institute, Sapporo, 062-8516, Japan

    Takayuki Kawahara

  5. University Museum, Kyushu University, Fukuoka, 812-8581, Japan

    Misako Mishima

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Correspondence to Akiko Soejima.

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An erratum to this article is available at https://doi.org/10.1007/s10265-017-0965-x.

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Soejima, A., Tanabe, A.S., Takayama, I. et al. Phylogeny and biogeography of the genus Stevia (Asteraceae: Eupatorieae): an example of diversification in the Asteraceae in the new world. J Plant Res 130, 953–972 (2017). https://doi.org/10.1007/s10265-017-0955-z

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