Skip to main content
SpringerLink
Log in

Phylogeny, classification and biogeography of Halfordia (Rutaceae) in Australia and New Caledonia

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

Abstract

Halfordia F.Muell is a genus of rainforest trees or shrubs native to New Guinea, New Britain, New Caledonia, Vanuatu and eastern Australia. There is debate about the number of species that should be recognised in the genus. Four species have been named, but authors have commonly recognised only two species, and some recent treatments accept just one widespread species with a broad ecological range. We sequenced two nrDNA markers (ITS and ETS) and two cpDNA markers (rbcL and trnL–trnF) from samples across the range of Halfordia in Australia and New Caledonia. Three allopatric nrDNA groups were resolved: one from southeast Queensland and northern New South Wales (Group A); one from the Wet Tropics region of North Queensland (Group B); and one from the Cape York region of North Queensland, Torres Strait and New Caledonia (Group C). These groups were also partly differentiated by more slowly evolving cpDNA markers; the exception was one widespread haplotype in Australia (presumed ancestral). The nrDNA groups support recognition of three previously described species: H. leichhardtii (Group A), H. scleroxyla (Group B) and H. kendack (Group C). Divergences among eastern Australia populations are best explained by vicariance and correlate with geographic breaks documented for other taxa (ranging in estimated ages from the mid-late Miocene to the Pleistocene). The broad distribution of Group C, from Cape York to New Caledonia, with less genetic divergence, arguably reflects recent range expansion into New Caledonia involving bird dispersal of fleshy fruits.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bache F, Sutherland R, Stagpoole V, Herzer R, Collot J, Rouillard P (2012) Stratigraphy of the southern Norfolk Ridge and the Reinga Basin: a record of initiation of Tonga–Kermadec–Northland subduction in the southwest Pacific. Earth Planet Sci Lett 321–322:41–53

    Article  Google Scholar 

  • Bailey FM (1899) The Queensland flora, part I. HJ Diddams and Co., Brisbane

    Google Scholar 

  • Barker RD, Vestjens WJM (1989) The food of Australian birds: 1 non-passerines. CSIRO Publishing, Melbourne

    Google Scholar 

  • Barrett RA, Bayly MJ, Duretto MF, Forster PI, Ladiges PY, Cantrill DJ (2015) A chloroplast phylogeny of Zieria (Rutaceae) in Australia and New Caledonia shows widespread incongruence with species-level taxonomy. Austral Syst Bot 27:427–449

    Article  Google Scholar 

  • Bayly MJ, Holmes GD, Forster PI, Cantrill DJ, Ladiges PY (2013a) Major clades of Australasian Rutoideae (Rutaceae) based on rbcL and atpB sequences. PLoS ONE 8:e72493. doi:10.1371/journal.pone.0072493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bayly MJ, Rigault P, Spokevicius A, Ladiges PY, Ades PK, Anderson C, Bossinger G, Merchant A, Udovicic F, Woodrow I, Tibbits J (2013b) Chloroplast genome analysis of Australian eucalypts: Eucalyptus, Corymbia, Angophora, Allosyncarpia and Stockwellia (Myrtaceae). Molec Phylogen Evol 69:704–716

    Article  CAS  Google Scholar 

  • Bayly MJ, Duretto MF, Holmes GD, Forster PI, Cantrill DC, Ladiges PY (2015) Transfer of the New Caledonian genus Boronella to Boronia (Rutaceae) based on analyses of cpDNA and nrDNA. Austral Syst Bot 28:111–123

    Article  Google Scholar 

  • Bergsten J (2005) A review of long-branch attraction. Cladistics 21:163–193

    Article  Google Scholar 

  • Bock DG, Andrew RL, Rieseberg LH (2014) On the adaptive value of cytoplasmic genomes in plants. Molec Ecol 23:4899–4911

    Article  Google Scholar 

  • Brown GK, Murphy DJ, Kidman J, Ladiges PY (2012) Phylogenetic connections of phyllodinous species of Acacia outside Australia are explained by geological history and human-mediated dispersal. Austral Syst Bot 25:390–403

    Article  Google Scholar 

  • Burke JM, Ladiges PY, Batty EL, Adams PB, Bayly MJ (2013) Divergent lineages in two species of Dendrobium orchids (D. speciosum and D. tetragonum) correspond to major geographic breaks in eastern Australia. J Biogeogr 40:2071–2081

    Article  Google Scholar 

  • Byrne M, Steane DA, Joseph L, Yeates DK, Jordan GJ, Crayn D, Aplin K, Cantrill DJ, Cook LG, Crisp MD, Keogh JS, Melville J, Moritz C, Porch N, Sniderman JMK, Sunnucks P, Weston PH (2011) Decline of a biome: evolution, contraction, fragmentation, extinction and invasion of the Australian mesic zone biota. J Biogeogr 38:1635–1656

    Article  Google Scholar 

  • Centre for Australian National Biodiversity Research (2010) Australian tropical rainforest plants edition 6 [online version]. Available at: http://www.anbg.gov.au/cpbr/cd-keys/rfk/index.html

  • CHAH (2016) Australian plant census. IBIS database, Centre for Australian National Biodiversity Research, Council of Heads of Australasian Herbaria. Available at: https://www.anbg.gov.au/chah/apc/

  • Chapple DG, Hoskin CJ, Chapple SNJ, Thompson MB (2011) Phylogenetic divergence in the widespread delicate skink (Lamropholis delicata) corresponds to dry habitat barrier in eastern Australia. BMC Evol Biol 11:191

  • Conn BJ, Damas KQ (2005) Guide to trees of Papua New Guinea. Available at: http://www.pngplants.org/PNGtrees

  • Cooper W, Cooper WT (2004) Fruits of the Australian tropical rainforest. Nokomis Editions, Melbourne

    Google Scholar 

  • Cracraft J (1986) Origin and evolution of continental biotas: speciation and historical congruence within the Australian avifauna. Evolution 40:977–996

    Article  Google Scholar 

  • De Beuque SV, Auzende J-M, Lafoy Y, Missegue F (1998) Tectonique et volcanisme tertiaire sur la ride de Lord Howe (Sud-Ouest Pacifique). Compt Rend Acad Sci Ser IIA Earth Planet Sci 326:663–669

    Google Scholar 

  • Exon NF, Hill PJ, Lafoy Y, Heine C, Bernardel G (2006) Kenn Plateau off northeast Australia: a continental fragment in the southwest Pacific jigsaw. Austral J Earth Sci 53:541–564

    Article  Google Scholar 

  • Farris JS, Källersjö M, Kluge AG, Bult C (1995a) Constructing a significance test for incongruence. Syst Biol 44:570–572

    Article  Google Scholar 

  • Farris JS, Källersjö M, Kluge AG, Bult C (1995b) Testing significance of incongruence. Cladistics 10:315–319

    Article  Google Scholar 

  • Floyd AG (1989) Rainforest trees of mainland south-eastern Australia. Inkata Press, Melbourne

    Google Scholar 

  • Ford J (1986) Avian hybridization and allopatry in the region of the Einasleigh Uplands and Burdekin-Lynd Divide, north-eastern Queensland. Emu 86:87–110

    Article  Google Scholar 

  • Ford J (1987) Hybrid zones in Australian birds. Emu 87:158–178

    Article  Google Scholar 

  • Forshaw J, Cooper WT (2015) Pigeons and doves in Australia. CSIRO Publishing, Melbourne

    Google Scholar 

  • Forster PI (2002) Rutaceae. In: Henderson RJF (ed) Names and distribution of Queensland plants, algae and lichens. Environmental Protection Agency, Brisbane, pp 177–181

    Google Scholar 

  • Forster PI, Brophy JJ, Goldsack RJ (2004) Variation in Australian populations of Halfordia kendack s.l. (Rutaceae): evidence from leaf essential oils. Austral Syst Bot 17:571–580

    Article  Google Scholar 

  • Francis WD (1951) Australian rain-forest trees. Forestry and Timber Bureau, Sydney

    Google Scholar 

  • Gibbs D, Barnes E, Cox J (2001) Pigeons and doves: a guide to the pigeons and doves of the world. A & C Black, London

    Google Scholar 

  • Groppo M, Pirani JRR, Salatino MLF, Blanco SR, Kallunki JA (2008) Phylogeny of Rutaceae based on two noncoding regions from cpDNA. Amer J Bot 95:985–1005

    Article  CAS  Google Scholar 

  • Groppo M, Kallunki JA, Pirani JR, Antonelli A (2012) Chilean Pitavia more closely related to Oceania and Old World Rutaceae than to Neotropical groups: evidence from two cpDNA non-coding regions, with a new subfamilial classification of the family. PhytoKeys 19:9–29

    Article  Google Scholar 

  • Hartley T (2001) Morphology and biogeography in Australasian–Malesian Rutaceae. Malayan Nat J 55:197–219

    Google Scholar 

  • Hartley TG (2013) Halfordia. Flora Aust 26:83–84

    Google Scholar 

  • Hollingsworth PM, Graham SW, Damon PL (2011) Choosing and using a plant DNA barcode. PloS ONE 6:e19254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holmes GD, Downing TL, James EA, Blacket MJ, Hoffman AA, Bayly MJ (2014) Phylogeny of the holly grevilleas (Proteaceae) based on nuclear ribosomal and chloroplast DNA. Austral Syst Bot 27:56–77

    Article  Google Scholar 

  • Hugall A, Moritz C, Moussalli A, Stanisic J (2002) Reconciling paleodistribution models and comparative phylogeography in the wet tropics rainforest land snail Gnarosophia bellendenkerensis (Brazier 1875). Proc Natl Acad Sci USA 99:6112–6117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hyland BPM, Whiffin T (1993) Australian tropical rain forest trees, an interactive identification system. CSIRO Publishing, Melbourne

    Google Scholar 

  • Hyland BPM, Whiffin T, Christophel DC, Gray B, Elick RW, Ford AJ (1999) Australian tropical rain forest trees and shrubs. CSIRO Publishing, Melbourne

    Google Scholar 

  • Hyland BPM, Whiffin T, Christophel DC, Gray B, Elick RW (2003) Australian tropical rain forest plants: trees, shrubs and vines. CD-ROM. CSIRO Publishing, Melbourne

    Google Scholar 

  • Joseph L, Moritz C, Hugall A (1995) Molecular support for vicariance as source diversity in rainforest. Proc Roy Soc B 260:177–182

    Article  CAS  Google Scholar 

  • Kapralov MV, Filatov DA (2007) Widespread positive selection in the photosynthetic Rubisco enzyme. BMC Evol Biol 7:73

    Article  PubMed  PubMed Central  Google Scholar 

  • Keast A (1957) Variation and speciation in the genus Climacteris Temminck (Aves: Sittidae). Austral J Zool 5:474–495

    Article  Google Scholar 

  • Ladiges PY, Cantrill D (2007) New Caledonia–Australian connections: biogeographic patterns and geology. Austral Syst Bot 20:383–389

    Article  Google Scholar 

  • McKinnon GE, Vaillancourt RE, Jackson HD, Potts BM (2001) Chloroplast sharing in the Tasmanian eucalypts. Evolution 55:703–711

    Article  CAS  PubMed  Google Scholar 

  • Meudt HM, Bayly MJ (2008) Phylogeographic patterns in the Australasian genus Chionohebe (Veronica s.l., Plantaginaceae) based on AFLP and chloroplast DNA sequences. Molec Phylogen Evol 47:319–338

    Article  CAS  PubMed  Google Scholar 

  • Moritz C, Patton JL, Schneider CJ, Smith TB (2000) Diversification of rainforest faunas: an integrated molecular approach. Ann Rev Ecol Syst 31:533–563

    Article  Google Scholar 

  • Moritz C, Hoskin C, Graham CH, Hugall A, Moussalli A (2005) Historical biogeography, diversity and conservation of Australia’s tropical rainforest herpetofauna. In: Purvis A, Gittleman JL, Brooks T (eds) Phylogeny and conservation. Cambridge University Press, Cambridge, pp 243–264

    Chapter  Google Scholar 

  • Moritz C, Hoskin CJ, MacKenzie JB, Philips BL, Tonione M, Silva N, VanDerWal J, Williams SE, Graham CH (2009) Identification and dynamics of a cryptic suture zone in tropical rainforest. Proc Roy Soc B: Biol Sci 276:1235–1244

    Article  CAS  Google Scholar 

  • Mortimer N (2004) New Zealand’s geological foundations. Gondwana Res 7:261–272

    Article  Google Scholar 

  • Morton CM, Telmer C (2014) New subfamily classification for the Rutaceae. Ann Missouri Bot Gard 99:620–641

    Article  Google Scholar 

  • Moussalli A, Hugall AF, Moritz C (2005) A mitochondrial phylogeny of the rainforest skink genus Saproscincus, Wells and Wellington (1984). Molec Phylogenet Evol 34:190–202

    Article  CAS  PubMed  Google Scholar 

  • Nevill PG, Despres T, Bayly MJ, Bossinger G, Ades PK (2014) Shared phylogeographic patterns and widespread chloroplast haplotype sharing in Eucalyptus species with different ecological tolerances. Tree Genet Genomes 10:1079–1092

    Article  Google Scholar 

  • Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala

    Google Scholar 

  • O’Connor D, Moritz C (2003) A molecular phylogeny of the Australian skink genera Eulamprus, Gnypetoscincus and Nangura. Austral J Zool 51:317–330

    Article  Google Scholar 

  • Petit RJ, Excoffier L (2009) Gene flow and species delimitation. Trends Ecol Evol 24:386–393

    Article  PubMed  Google Scholar 

  • Pollock LJ, Bayly MJ, Nevill PG, Vesk PA (2013) Chloroplast DNA diversity associated with protected slopes and valleys for hybridizing Eucalyptus species on isolated ranges in south-eastern Australia. J Biogeogr 40:155–167

    Article  Google Scholar 

  • Rambaut A (2002) Se-Al: sequence alignment editor. Available at: http://tree.bio.ed.ac.uk/software/seal/

  • Rambaut A, Drummond AJ (2009) Tracer, version 1.5, MCMC trace analysis package. Available at: http://beast.bio.ed.ac.uk/Tracer

  • Richards PG (2002) Halfordia. In: Harden GJ (ed) Flora of New South Wales, vol 2, Revised edition. University of New South Wales Press, Sydney, pp 320–321

  • Rieseberg LH, Soltis DE (1991) Phylogenetic consequences of cytoplasmic gene flow in plants. Evol Trends Pl 5:65–84

    Google Scholar 

  • Rix MG, Harvey MS (2012) Phylogeny and historical biogeography of ancient assassin spiders (Araneae: Archaeidae) in the Australian mesic zone: evidence for miocene speciation within tertiary refugia. Molec Phylogen Evol 62:375–396

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rossetto M, Crayn D, Ford A, Mellick R, Sommerville K (2009) The influence of environment and life-history traits on the distribution of genes and individuals: a comparative study of 11 rainforest trees. Molec Ecol 18:1422–1438

    Article  CAS  Google Scholar 

  • Salzburger W, Ewing GB, Von Haeseler A (2011) The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Molec Ecol 20:1952–1963

    Article  Google Scholar 

  • Schneider CJ, Cunningham M, Moritz C (1998) Comparative phylogeography and the history of endemic vertebrates in the wet tropics rainforests of Australia. Molec Ecol 7:487–498

    Article  Google Scholar 

  • Schodde R, Mason I (1999) The directory of Australian birds: passerines. CSIRO Publishing, Melbourne

    Google Scholar 

  • Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381

    Article  CAS  PubMed  Google Scholar 

  • Stanley TD, Ross EM (1983) Flora of south-eastern Queensland. Queensland Department of Primary Industries, Brisbane

    Book  Google Scholar 

  • Sutherland R, Collot J, Lafoy Y, Logan GA, Hackney R, Stagpoole V, Uruski C, Hashimoto T, Higgins K, Herzer RH, Wood R, Mortimer N, Rollet N (2010) Lithosphere delamination with foundering of lower crust and mantle caused permanent subsidence of New Caledonia Trough and transient uplift of Lord Howe Rise during Eocene and Oligocene initiation of Tonga-Kermadec subduction, western Pacific. Tectonics 29:TC2004

    Article  Google Scholar 

  • Swofford D (2002) PAUP* 4.0b10: phylogenetic analysis using parsimony (* and other methods). Version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Yeates DK, Bouchard P, Monteith GB (2002) Patterns and levels of endemism in the Australian wet tropics rainforest: evidence from flightless insects. Invert Syst 16:605–619

    Article  Google Scholar 

Download references

Acknowledgments

This study was funded by the Australian Research Council (LP0776737) and the Australian Biological Resources Study (PD208-02). Collecting permits were provided by the New South Wales Parks and Wildlife Service, the former Queensland Environmental Protection Agency, and conservation authorities of the North and South Provinces of New Caledonia (DDEE, Direction du Développement Économique et de l’Environnement; DENV, Direction de l’Environnement). We thank Garry Sankowsky, Andrew Ford, Kris Kupsch, David Fell, Greg Smyrell, Bruce Wannan, Mike Mathieson, Gareth Nelson, Gillian Brown, and Carlos Parra-O. for assistance with fieldwork or provision of samples.

Author information

Authors and Affiliations

  1. School of BioSciences, The University of Melbourne, Parkville, VIC, 3010, Australia

    Michael J. Bayly, Gareth D. Holmes & Pauline Y. Ladiges

  2. Royal Botanic Gardens Victoria, Melbourne, VIC, 3004, Australia

    Gareth D. Holmes & David J. Cantrill

  3. Department of Science, Information Technology and Innovation, Queensland Herbarium, Brisbane Botanic Gardens, Toowong, QLD, 4066, Australia

    Paul I. Forster

  4. Institut de Recherche pour le Développement (IRD), UMR Botanique et Modélisation de l’Architecture des Plantes et des Végétations (AMAP), 34000, Montpellier, France

    Jérôme Munzinger

Authors
  1. Michael J. Bayly
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gareth D. Holmes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paul I. Forster
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jérôme Munzinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David J. Cantrill
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Pauline Y. Ladiges
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael J. Bayly.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling editor: Christian Parisod.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bayly, M.J., Holmes, G.D., Forster, P.I. et al. Phylogeny, classification and biogeography of Halfordia (Rutaceae) in Australia and New Caledonia. Plant Syst Evol 302, 1457–1470 (2016). https://doi.org/10.1007/s00606-016-1344-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-016-1344-0

Keywords

Search

Navigation