Skip to main content
Log in

Phylogeny of Rhododendron subgenus Hymenanthes based on chloroplast DNA markers: between-lineage hybridisation during adaptive radiation?

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

Rhododendron subgenus Hymenanthes comprises >200 highly interfertile species in SE Asia (mainly Himalayas and southern China) plus the 10–11 members of subsection Pontica (excluding R. hyperythrum) distributed outside SE Asia. Parsimony and Bayesian analyses of cpDNA matK and trnL-F sequence data divided Hymenanthes into two clades: clade H, in which two Pontica species and the SE Asian R. adenopodum were sister to a clade of 60 SE Asian species, and clade P comprising eight Pontica species plus R. praevernum, R. calophytum, and R. insigne from SE Asia. If these three species belong in Pontica, they expand its range substantially. However, as they have no morphological links to Pontica, they might descend from clade H species that captured chloroplasts from a now extinct species of Pontica. Either way, their distribution within the Chinese/Himalayan range of Rhododendron indicates an ancestor that came from the north or east to meet the diversifying group of Hymenanthes in the Himalayas, making the SE Asian members of Hymenanthes a polyphyletic group.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Arnold ML, Bouck AC, Cornman RS (2004) Verne grant and Louisiana irises: is there anything new under the sun? New Phytol 161:143–149

    Article  Google Scholar 

  • Baldwin BG (1997) Adaptive radiation of the Hawaiian silversword alliance: congruence and conflict of phylogenetic evidence from molecular and non-molecular investigations. In: Givnish TJ, Sytsma KJ (eds) Molecular evolution and adaptive radiation. Cambridge University Press, Cambridge, pp 103–128

    Google Scholar 

  • Barrier M, Robichaux RH, Purugganan MD (2001) Accelerated regulatory gene evolution in an adaptive radiation. Proc Nat Acad Sci USA 98:10208–10213

    Article  CAS  PubMed  Google Scholar 

  • Brown GK, Craven LA, Udovicic F, Ladiges PY (2006) Phylogeny of Rhododendron section Vireya (Ericaceae) based on two non-coding regions of cpDNA. Plant Syst Evol 257:57–93

    Google Scholar 

  • Chamberlain DF (1982) A revision of Rhododendron II. subgenus Hymenanthes. Notes R Bot Gard Edinb 39:209–486

    Google Scholar 

  • Chamberlain DF, Hyam R, Argent G, Fairweather G, Walter KS (1996) The genus Rhododendron: its classification and synonymy. Royal Botanic Garden Edinburgh, Edinburgh

    Google Scholar 

  • Chung JD, Lin TP, Chen YL, Cheng YP, Hwang SY (2007) Phylogeographic study reveals the origin and evolutionary history of a Rhododendron species complex in Taiwan. Mol Phylogenet Evol 42:14–24

    Article  CAS  PubMed  Google Scholar 

  • Clabaut C, Bunje PME, Salzburger W, Meyer A (2007) Geometric morphometric analyses provide evidence for the adaptive character of the Tanganyikan cichlid fish radiations. Evolution 61:560–578

    Article  PubMed  Google Scholar 

  • Cox PA, Cox KNE (1997) The encyclopaedia of Rhododendron species. Glendoick, Perth

    Google Scholar 

  • Danley PD, Kocher TD (2001) Speciation in rapidly diverging systems: lessons from Lake Malawi. Mol Ecol 10:1075–1086

    Article  CAS  PubMed  Google Scholar 

  • Fang RZ, Min TL (1995) The floristic study on the genus Rhododendron. Acta Bot Yunnanica 17:359–379

    Google Scholar 

  • Francisco-Ortega J, Jansen RK, Santos-Guerra A (1996) Chloroplast DNA evidence of colonization, adaptive radiation, and hybridization in the evolution of the Macaronesian flora. Proc Nat Acad Sci USA 93:4085–4090

    Article  CAS  PubMed  Google Scholar 

  • Goetsch L, Eckert AJ, Hall BD (2005) The molecular systematics of Rhododendron (Ericaceae): a phylogeny based upon RPB2 gene sequences. Syst Bot 30:616–626

    Article  Google Scholar 

  • Grant V (1981) Plant speciation. Columbia University Press, New York

    Google Scholar 

  • Johnson LA, Soltis DE (1995) Phylogenetic inference in Saxifragaceae sensu stricto and Gilia (Polemoniaceae) using matK sequences. Ann Mo Bot Gard 82:149–175

    Article  Google Scholar 

  • Kron K (1997) Phylogenetic relationships of Rhododendroideae (Ericaceae). Am J Bot 84:973–980

    Article  CAS  Google Scholar 

  • Kron KA, Gawen LM, Chase MW (1993) Evidence for introgression in azaleas (Rhododendron; Ericaceae): chloroplast DNA and morphological variation in a hybrid swarm on Stone Mountain, Georgia. Am J Bot 80:1095–1099

    Article  CAS  Google Scholar 

  • Kurashige Y, Mine M, Kobayashi N, Handa T, Takayanagi K, Yukawa T (1998) Sectional relationships of the genus Rhododendron based on matK sequences. J Jpn Bot 73:143–154

    Google Scholar 

  • Kurashige Y, Etoh J-I, Handa T, Takayanai K, Yukawa T (2001) Sectional relationships in the genus Rhododendron (Ericaceae): evidence from matK and trnK intron sequences. Plant Syst Evol 228:1–14

    Article  CAS  Google Scholar 

  • Levin DA (2006a) The spatial sorting of ecological species: ghost of competition or of hybridization past? Syst Bot 31:8–12

    Article  Google Scholar 

  • Levin DA (2006b) Flowering phenology in relation to adaptive radiation. Syst Bot 31:239–246

    Article  Google Scholar 

  • Li C-X, Lu S-Q, Barrington DS (2008) Phylogeny of Chinese Polystichum (Dryopteridaceae) based on chloroplast DNA sequence data (trnL-F and rps4-trnS). J Plant Res 121:19–26

    Article  CAS  PubMed  Google Scholar 

  • MacLean RC (2005) Adaptive radiation in microbial microcosms. J Evol Biol 18:1376–1386

    Article  PubMed  Google Scholar 

  • Masueli RW, Camadro EL, Erazzu LE, Bedogni MC, Marfil CF (2009) Homoploid hybridization in the evolution of wild diploid potato species. Plant Syst Evol 277:143–152

    Article  Google Scholar 

  • Meng Y, Wen J, Nie Z-L, Sun H, Yang Y-P (2008) Phylogeny and biogeographic diversification of Maianthemum (Ruscaceae: Polygonatae). Mol Phylogenet Evol 49:424–434

    Article  PubMed  Google Scholar 

  • Milne RI (2004) Phylogeny and biogeography of Rhododendron subsection Pontica, a group with a Tertiary relict distribution. Mol Phylogenet Evol 33:389–401

    Article  CAS  PubMed  Google Scholar 

  • Milne RI, Abbott RJ (2000) Origin and evolution of invasive naturalized material of Rhododendron ponticum L. in the British isles. Mol Ecol 9:541–556

    Article  CAS  PubMed  Google Scholar 

  • Milne RI, Abbott RJ (2002) The origin and evolution of Tertiary relict floras. Adv Bot Res 38:281–314

    Article  Google Scholar 

  • Milne RI, Abbott RJ (2008) Reproductive isolation among two interfertile Rhododendron species: low frequency of post-F1 hybrid genotypes in alpine hybrid zones. Mol Ecol 17:1108–1121

    Article  CAS  PubMed  Google Scholar 

  • Milne RI, Abbott RJ, Wolff K, Chamberlain DF (1999) Hybridization among sympatric species of Rhododendron: (Ericaceae) in Turkey: morphological and molecular evidence. Am J Bot 86:1776–1785

    Article  CAS  PubMed  Google Scholar 

  • Milne RI, Terzioglu S, Abbott RJ (2003) A hybrid zone dominated by fertile F1s: maintenance of species barriers in Rhododendron. Mol Ecol 12:2719–2729

    Article  CAS  PubMed  Google Scholar 

  • Petit RJ, Bodenes C, Ducousso A, Roussel G, Kremer A (2004) Hybridization as a mechanism of invasion in oaks. New Phytol 161:151–164

    Article  CAS  Google Scholar 

  • Ree RH (2005) Phylogeny and the evolution of floral diversity in Pedicularis (Orobanchaceae). Int J Plant Sci 166:595–613

    Article  CAS  Google Scholar 

  • Renner SS, Zhang L-B, Murata J (2004) A chloroplast phylogeny of Arisaema (Araceae) illustrates Tertiary floristic links between Asia, North America, and East Africa. Am J Bot 91:881–888

    Article  Google Scholar 

  • Ricklefs RE (2006) Evolutionary diversification and the origin of the diversity-environment relationship. Ecology 87:S3–S13

    Article  PubMed  Google Scholar 

  • Rieseberg LH, Wendel JF (1993) Introgression and its consequences in plants. In: Harrison R (ed) Hybrid zones and the evolutionary process. Oxford University Press, Oxford, pp 70–109

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana, Totowa, pp 365–386

    Google Scholar 

  • Sakai AK, Weller SG, Wagner WL, Nepokroeff M, Cullen TM (2006) Adaptive radiation and evolution of breeding systems in Schiedea (Caryophyllaceae), an endemic Hawaiian genus. Ann Mo Bot Gard 93:49–63

    Article  Google Scholar 

  • Schliewen UK, Klee B (2004) Reticulate sympatric speciation in Cameroonian crater lake cichlids. Front Zool 1:5

    Article  PubMed  Google Scholar 

  • Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207

    Article  PubMed  Google Scholar 

  • Sleumer H (1949) Ein System der Gattung Rhododendron. Bot Jahrb 74:511–533

    Google Scholar 

  • Smissen RD, Breitwieser I, Ward JM (2004) Phylogenetic implications of trans-specific chloroplast DNA sequence polymorphism in New Zealand Gnaphalieae (Asteraceae). Plant Syst Evol 249:37–53

    Article  CAS  Google Scholar 

  • Stevenson JB (ed) (1930) The species of Rhododendron. The Rhododendron Society, London

    Google Scholar 

  • Swofford DL (2002) PAUP* phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109

    Article  CAS  PubMed  Google Scholar 

  • Wang A, Yang M, Liu J (2005) Molecular phylogeny, recent radiation and evolution of gross morphology of the rhubarb genus Rheum. Ann Bot 96:489–498

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Yu WB, Chen JQ, Blackmore S (2009) Pollen morphology in relation to floral types and pollination syndromes in Pedicularis (Orobanchaceae). Plant Syst Evol 277:153–162

    Article  Google Scholar 

  • Wu ZY, Raven PH (2005) Flora of China. Apiaceae through Ericaceae, vol. 14. Missouri Botanical Garden, Science Press, Beijing

  • Xiang QYJ, Zhang WH, Ricklefs RE, Qian H, Chen ZD, Wen J, Li JH (2004) Regional differences in rates of plant speciation and molecular evolution: a comparison between eastern Asia and eastern North America. Evolution 58:2175–2184

    CAS  PubMed  Google Scholar 

  • Zha H-G, Milne RI, Sun H (2008) Morphological and molecular evidence of natural hybridization between two distantly related Rhododendron species from the Sino-Himalaya. Bot J Linn Soc 156:119–129

    Article  Google Scholar 

  • Zha H-G, Milne RI, Sun H (2010) Asymmetric hybridization in Rhododendron agastum: a hybrid taxon comprising mainly F1s in Yunnan, China. Ann Bot 105:89–100

    Article  CAS  PubMed  Google Scholar 

  • Zhang JL, Zhang CQ, Gao LM, Yang JB, Li HT (2007) Natural hybridization origin of Rhododendron agastum (Ericaceae) in Yunnan, China: inferred from morphological and molecular evidence. J Plant Res 120:457–463

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank the keeper and staff of the Royal Botanic Garden, Edinburgh, for access to their live material; K.M. Creasey, S.E. Hinds and T. Marczewski for laboratory assistance; Dr C.M. Moeller for software assistance; and three anonymous reviewers for constructive comments on an earlier draft of the manuscript. Dr R.I. Milne was supported by National Environment Research Council (NERC, UK) fellowship NE/B500658/1 while conducting this work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard I. Milne.

Additional information

R. Prickett and L.H. Inns contributed equally.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Milne, R.I., Davies, C., Prickett, R. et al. Phylogeny of Rhododendron subgenus Hymenanthes based on chloroplast DNA markers: between-lineage hybridisation during adaptive radiation?. Plant Syst Evol 285, 233–244 (2010). https://doi.org/10.1007/s00606-010-0269-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-010-0269-2

Keywords

Navigation