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Australian Systematic Botany Australian Systematic Botany Society
Taxonomy, biogeography and evolution of plants
RESEARCH ARTICLE

Phylogeny and proposed circumscription of Breynia, Sauropus and Synostemon (Phyllanthaceae), based on chloroplast and nuclear DNA sequences

Kanchana Pruesapan A B , Ian R. H. Telford C , Jeremy J. Bruhl C and Peter C. van Welzen A D
+ Author Affiliations
- Author Affiliations

A Netherlands Centre for Biodiversity Naturalis (section NHN), Leiden University, PO Box 9514, 2300 RA Leiden, the Netherlands.

B Plant Varieties Protection Division, Department of Agriculture, 50 Pahonyothin Road, Chatuchak, Bangkok 10900, Thailand.

C Botany & N.C.W. Beadle Herbarium, School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia.

D Corresponding author. Email: welzen@nhn.leidenuniv.nl

Australian Systematic Botany 25(5) 313-330 https://doi.org/10.1071/SB11005
Submitted: 26 January 2011  Accepted: 8 June 2012   Published: 10 October 2012

Abstract

Previous estimates of phylogeny in the Phyllanthaceae, Phyllantheae, have been hampered by undersampling of species from morphologically distinctive groups and using too few gene regions. To increase the phylogenetic resolution, sequences of two nuclear (ITS1–5.8S–ITS2) and Phytochrome C (PHYC)) and two non-coding chloroplast (accD–psaI, trnS–trnG) DNA markers were analysed using maximum parsimony and Bayesian inference with expanded sampling in Breynia, Glochidion, Sauropus and Synostemon. Our results supported reinstatement of Synostemon, previously included in Sauropus s.str., to generic rank, and provided evidence towards its future infrageneric classification. The results also indicated expansion of Breynia to include Sauropus s.str.; this combined monophyletic group consists of two strongly supported clades. Finally, we showed monophyly for Glochidion, which is sister to Phyllanthus subg. Phyllanthodendron, both still remaining undersampled. Morphological features characteristic of Breynia, Sauropus and Synostemon are discussed, as well as the desirability of dividing Phyllanthus into smaller genera.


References

Airy Shaw HK (1969) Notes on Malesian and other Asiatic Euphorbiaceae. CI. New or noteworthy species of Sauropus Bl. Kew Bulletin 23, 42–55.

Airy Shaw HK (1980a) A partial synopsis of the Euphorbiaceae – Platylobeae of Australia (excluding Phyllanthus, Euphorbia and Calycopeplus). Kew Bulletin 35, 577–700.
A partial synopsis of the Euphorbiaceae – Platylobeae of Australia (excluding Phyllanthus, Euphorbia and Calycopeplus).Crossref | GoogleScholarGoogle Scholar |

Airy Shaw HK (1980b) The Euphorbiaceae of New Guinea. Kew Bulletin 8, 38–42.

Andersson L, Chase MW (2001) Phylogeny and classification of Marantaceae. Botanical Journal of the Linnean Society 135, 275–287.
Phylogeny and classification of Marantaceae.Crossref | GoogleScholarGoogle Scholar |

Beille L (1927) Euphorbiaceae. In ‘Flore générale de l’Indo-Chine 5’. (Ed. MH Lecomte) pp. 643–658. (Masson & Cie.: Paris)

Croizat L (1940) New and critical Euphorbiaceae from eastern tropical Asia. Journal of the Arnold Arboretum. Arnold Arboretum 21, 490–510.

Croizat L (1942) On certain Euphorbiaceae from the tropical Far East. Journal of the Arnold Arboretum. Arnold Arboretum 23, 29–54.

Farris JS, Källersjö M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10, 315–319.
Testing significance of incongruence.Crossref | GoogleScholarGoogle Scholar |

Farris JS, Källersjö M, Kluge AG, Bult C (1995) Constructing a significance test for incongruence. Systematic Biology 44, 570–572.

Felsenstein J (1985) Confidence limits on phylogenetics: an approach using the bootstrap. Evolution 39, 783–791.
Confidence limits on phylogenetics: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar |

Fitch WM (1971) Towards defining the course of evolution: minimum change for a specific tree topology. Systematic Zoology 20, 406–416.
Towards defining the course of evolution: minimum change for a specific tree topology.Crossref | GoogleScholarGoogle Scholar |

Govaerts R, Frodin DG, Radcliffe-Smith A (2000) ‘World checklist and bibliography of Euphorbiaceae (and Pandaceae) 1, 2, 4.’ (The Royal Botanic Gardens, Kew: London)

Hamilton MB (1999) Four primer pairs for the application of chloroplast intergenic regions with intraspecific variation. Molecular Ecology 8, 521–523.

Hemsley WB (1898) Phyllanthodendron mirabilis Hemsl. Hooker’s Icones Plantarum 26, 2563–2564.

Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42, 182–192.

Hoffmann P, Kathriarachchi H, Wurdack KJ (2006) A phylogenetic classification of Phyllanthaceae (Malpighiales; Euphorbiaceae sensu lato). Kew Bulletin 61, 37–53.

Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
MrBayes: Bayesian inference of phylogenetic trees.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvotV2isw%3D%3D&md5=36cced4192c095ad0b58c7c43beb4c9bCAS |

Hunter JT, Bruhl JJ (1996) Four new rare species of Sauropus Blume (Euphorbiaceae: Phyllantheae) from north Queensland. Austrobaileya 4, 661–672.

Hunter JT, Bruhl JJ (1997) New Sauropus (Euphorbiaceae: Phyllantheae) taxa for the Northern Territory and Western Australia and notes on other Sauropus occurring in these regions. Nuytsia 11, 165–184.

Johnson LA, Soltis DE (1998) Assessing congruence: empirical examples from molecular data. In ‘Molecular systematics of plants’. (Eds DE Soltis, PS Soltis, JJ Doyle) pp. 297–348. (Kluwer Academic Publisher: Dordrecht, the Netherlands)

Kathriarachchi K, Samuel R, Hoffmann P, Mlinarec J, Wurdack KJ, Ralimanana H, Stuessy TF, Chase MW (2006) Phylogenetics of tribe Phyllantheae (Phyllanthaceae; Euphorbiaceae sensu lato) based on nrITS and plastid matK DNA sequence data. American Journal of Botany 93, 637–655.
Phylogenetics of tribe Phyllantheae (Phyllanthaceae; Euphorbiaceae sensu lato) based on nrITS and plastid matK DNA sequence data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvFWjs7w%3D&md5=5bea0e795840ea3a2e770d8eb392f04eCAS |

Kato M, Takimura A, Kawakita A (2003) An obligate pollination mutualism and reciprocal diversification in the tree genus Glochidion (Euphorbiaceae). Proceedings of the Natural Academy of Sciences of the United States of America – Physical Science 100, 5264–5267.
An obligate pollination mutualism and reciprocal diversification in the tree genus Glochidion (Euphorbiaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjs1yitr0%3D&md5=c5eb030c0eaaa21cdd6c136b63c7c39cCAS |

Kawakita A (2010) Evolution of obligate pollination mutualism in the tribe Phyllantheae (Phyllanthaceae). Plant Species Biology 25, 3–19.
Evolution of obligate pollination mutualism in the tribe Phyllantheae (Phyllanthaceae).Crossref | GoogleScholarGoogle Scholar |

Kawakita A, Kato M (2004a) Evolution of obligate pollination mutualism in New Caledonian Phyllanthus (Euphorbiaceae). American Journal of Botany 91, 410–415.
Evolution of obligate pollination mutualism in New Caledonian Phyllanthus (Euphorbiaceae).Crossref | GoogleScholarGoogle Scholar |

Kawakita A, Kato M (2004b) Obligate pollination mutualism in Breynia (Phyllanthaceae): further documentation of pollination mutualism involving Epicephala moths (Gracillariidae). American Journal of Botany 91, 1319–1325.
Obligate pollination mutualism in Breynia (Phyllanthaceae): further documentation of pollination mutualism involving Epicephala moths (Gracillariidae).Crossref | GoogleScholarGoogle Scholar |

Kawakita A, Kato M (2009) Repeated independent evolution of obligate pollination mutualism in the Phyllantheae–Epicephala association. Proceedings of the Royal Society of London. Series B. Biological Sciences 276, 417–426.
Repeated independent evolution of obligate pollination mutualism in the Phyllantheae–Epicephala association.Crossref | GoogleScholarGoogle Scholar |

Kellogg EA, Appels R, Mason-Gamer RJ (1996) When genes tell different stories: the diploid genera of Triticeae (Graminae). Systematic Botany 21, 321–347.
When genes tell different stories: the diploid genera of Triticeae (Graminae).Crossref | GoogleScholarGoogle Scholar |

Li PT (1994) ‘Euphorbiaceae–Phyllanthoideae. Flora Reipublicae Popularis Sinicae 44, 1.’ (Science Press: Beijing) [in Chinese].

Maddison DR, Maddison WP (2001) ‘MacClade 4: Analysis of phylogeny and character evolution. Version 4.08.’ (Sinauer Associates: Sunderland, MA)

Mason-Gamer RJ, Kellogg BG (1996) Testing for phylogenetic conflict among molecular datasets in the tribe Triticeae. Systematic Biology 45, 524–545.
Testing for phylogenetic conflict among molecular datasets in the tribe Triticeae.Crossref | GoogleScholarGoogle Scholar |

Moore S (1920) A contribution to the Flora of Australia. Journal of the Linnean Society. Botany 45, 159–220.
A contribution to the Flora of Australia.Crossref | GoogleScholarGoogle Scholar |

Müller AJ (1865) Euphorbiaceae. Vorläufige Mitteilungen aus dem für De Candolle’s Prodromus bestimmten Manuscript über diese Familie. Linnaea 32, 72–73.

Nylander JAA (2004) ‘Mr Modeltest v2.’ (Evolutionary Biology Centre, Uppsala University: Uppsala, Sweden)

Pax F, Hoffmann K (1922) Euphorbiaceae–Phyllanthoideae–Phyllantheae. In ‘Das Pflanzenreich IV.147.xv’. (Ed. A Engler) pp. 215–226. (Wilhelm Engelmann: Leipzig, Germany)

Pruesapan K, Telford IRH, Bruhl JJ, Draisma SGA, van Welzen PC (2008) Delimitation of Sauropus (Phyllanthaceae) based on plastid matK and nuclear ribosomal ITS DNA sequence data. Annals of Botany 102, 1007–1018.
Delimitation of Sauropus (Phyllanthaceae) based on plastid matK and nuclear ribosomal ITS DNA sequence data.Crossref | GoogleScholarGoogle Scholar |

Radcliffe-Smith A (2001) ‘Genera Euphorbiacearum.’ (Royal Botanic Gardens, Kew: London)

Rambaut A, Drummond AJ (2004) ‘Tracer. Version 1.3.’ (University of Oxford: Oxford, UK)

Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed model. Bioinformatics 19, 1572–1574.
MrBayes 3: Bayesian phylogenetic inference under mixed model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=c3efa0cf361d593855ae82b9093dc1d2CAS |

Samuel R, Kathriarachchi H, Hoffmann P, Barfuss HJ, Wurdack KJ, Davis CC, Chase MW (2005) Molecular phylogenetics of Phyllanthaceae: evidence from plastid matK and nuclear PHYC sequences. American Journal of Botany 92, 132–141.
Molecular phylogenetics of Phyllanthaceae: evidence from plastid matK and nuclear PHYC sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1KlsbY%3D&md5=c40d52336ec60a21a44da286f8fb7bf7CAS |

Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. American Journal of Botany 94, 275–288.
Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktFOjsLg%3D&md5=173f3147f19074042486bac04c90c492CAS |

Small RL, Ryburn JA, Cronn RC, Seelanan T, Wendel JF (1998) The tortoise and the hare: choosing between noncoding plastome and nuclear ADH sequences for phylogeny reconstruction in a recently diverged plant group. American Journal of Botany 85, 1301–1315.
The tortoise and the hare: choosing between noncoding plastome and nuclear ADH sequences for phylogeny reconstruction in a recently diverged plant group.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmsFehtrY%3D&md5=519b3f160e0be4526a3d1774af9164e0CAS |

Suzuki Y, Glazko GV, Nei M (2002) Overcredibility of molecular phylogenies obtained by Bayesian phylogenetics. Proceedings of the Natural Academy of Sciences of the United States of America – Physical Science 99, 16 138–16 143.
Overcredibility of molecular phylogenies obtained by Bayesian phylogenetics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xps1ensLw%3D&md5=a4d5f8168ed242f1f6c4df14ffb052e5CAS |

Swofford DL (2003) ‘PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4.0b10.’ (Sinauer Associates: Sunderland, MA)

van Welzen PC (2003) Revision of the Malesian and Thai species of Sauropus (Euphorbiaceae: Phyllanthoideae). Blumea 48, 319–391.

van Welzen PC, Pruesapan K (2010) Four new species of Breynia (Phyllanthaceae/Euphorbiaceae s.lat.) and one new combination from Thailand and Malaysia. Thai Forest Bulletin (Botany) 38, 111–119.

Vorontsova MS, Hoffmann P (2008) A phylogenetic classification of tribe Poranthereae (Phyllanthaceae, Euphorbiaceae sensu lato). Kew Bulletin 63, 41–59.
A phylogenetic classification of tribe Poranthereae (Phyllanthaceae, Euphorbiaceae sensu lato).Crossref | GoogleScholarGoogle Scholar |

Vorontsova MS, Hoffmann P, Maurin O, Chase MW (2007) Molecular phylogenetics of tribe Poranthereae (Phyllanthaceae, Euphorbiaceae sensu lato). American Journal of Botany 94, 2026–2040.
Molecular phylogenetics of tribe Poranthereae (Phyllanthaceae, Euphorbiaceae sensu lato).Crossref | GoogleScholarGoogle Scholar |

Webster GL (1994) Synopsis of the genera and suprageneric taxa of Euphorbiaceae. Annals of the Missouri Botanical Garden 81, 33–144.
Synopsis of the genera and suprageneric taxa of Euphorbiaceae.Crossref | GoogleScholarGoogle Scholar |

Webster GL, Carpenter KJ (2008) Pollen morphology and systematics of palaeotropical Phyllanthus and related genera of subtribe Phyllanthinae (Euphorbiaceae). Botanical Journal of the Linnean Society 157, 591–608.
Pollen morphology and systematics of palaeotropical Phyllanthus and related genera of subtribe Phyllanthinae (Euphorbiaceae).Crossref | GoogleScholarGoogle Scholar |

Wendel JF, Doyle JJ (1998) Phylogenetic incongruence: window into genome history and molecular evolution. In ‘Molecular systematics of plants 2’. (Eds DE Soltis, PS Soltis, JJ Doyle) pp. 265–296. (Kluwer Academic Publishers: Dordrecht, the Netherlands)

White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In ‘PCR protocols: a Guide to Methods and Applications’. (Eds MA Innis, DH Gelfand, JJ Sninsky, TJ White) pp. 315–322. (Academic Press: New York)

Wiens JJ (2003) Missing data, incomplete taxa, and phylogenetic accuracy. Systematic Biology 52, 528–538.
Missing data, incomplete taxa, and phylogenetic accuracy.Crossref | GoogleScholarGoogle Scholar |

Wurdack KJ, Hoffmann P, Samuel R, de Bruijn A, van der Bank M, Chase MW (2004) Molecular phylogenetic analysis of Phyllanthaceae (Phyllanthoideae pro parte, Euphorbiaceae sensu lato) using plastid rbcL DNA sequences. American Journal of Botany 91, 1882–1900.
Molecular phylogenetic analysis of Phyllanthaceae (Phyllanthoideae pro parte, Euphorbiaceae sensu lato) using plastid rbcL DNA sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFajsr3J&md5=8fe98960434374fc85aedfa23e469340CAS |