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

The genealogy of geebungs: phylogenetic analysis of Persoonia (Proteaceae) and related genera in subfamily Persoonioideae

Gareth D. Holmes A C , Peter H. Weston B , Daniel J. Murphy A , Carolyn Connelly B and David J. Cantrill A
+ Author Affiliations
- Author Affiliations

A Royal Botanic Gardens Victoria, Birdwood Avenue, Melbourne, Vic. 3004, Australia.

B National Herbarium of New South Wales, Royal Botanic Gardens and Domain Trust, Mrs Macquaries Road, Sydney, NSW 2000, Australia.

C Corresponding author. Email: gareth.holmes@rbg.vic.gov.au

Australian Systematic Botany 31(2) 166-189 https://doi.org/10.1071/SB16052
Submitted: 17 November 2016  Accepted: 8 January 2018   Published: 7 May 2018

Abstract

Proteaceae subfamily Persoonioideae, as presently circumscribed, consists of the monogeneric tribe Placospermeae (Placospermum) and the tribe Persoonieae. The latter comprises the diverse genus Persoonia and monospecific genera found in New Zealand (Toronia), New Caledonia (Garnieria) and south-western Western Australia (Acidonia). Persoonia has 101 species distributed across Australia and has been classified into 11 informal groups. Using data derived from plastid DNA (trnL–trnF region), nuclear rDNA (ITS) and morphological characters, we constructed a phylogeny of Persoonioideae and compared the results to the existing classification. Bayesian and parsimony analyses indicated that Persoonia, as currently defined, is non-monophyletic. The molecular data and combined molecular and morphological data place Toronia in a moderately well supported clade with the monophyletic Rufiflora group of Persoonia from Western Australia. This clade is sister to Acidonia, Garnieria and the remaining Persoonia species. Of the other informal groups in Persoonia, the Teretifolia, Quinquenervis, Laurina, Arborea, Graminea and Chapmaniana groups are supported as monophyletic. The Lanceolata group can be re-circumscribed to be monophyletic by the addition of P. elliptica R.Br. (Longifolia group) and the Dillwynioides group. Relationships within this large, geographically widespread clade are largely unresolved and low DNA-sequence variation within it suggests a recent radiation followed by isolation in south-western and eastern Australia. All endemic Tasmanian Persoonia (Gunnii group taxa) are unresolved at the second-most basal node of the Persoonieae. Our results suggest that the Rufiflora group should be treated as a new genus and that the infrageneric taxonomy of Persoonia requires minor amendment.

Additional keywords: ITS, morphology, phylogeny, trnL–trnF.


References

Atchison J (2009) Human impacts on Persoonia falcata. Perspectives on post-contact vegetation change in the Keep River region, Australia, from contemporary vegetation surveys. Vegetation History and Archaeobotany 18, 147–157.
Human impacts on Persoonia falcata. Perspectives on post-contact vegetation change in the Keep River region, Australia, from contemporary vegetation surveys.Crossref | GoogleScholarGoogle Scholar |

Auld TD, Denham AJ, Turner K (2007) Dispersal and recruitment dynamics in the fleshy-fruited Persoonia lanceolata (Proteaceae). Journal of Vegetation Science 18, 903–910.
Dispersal and recruitment dynamics in the fleshy-fruited Persoonia lanceolata (Proteaceae).Crossref | GoogleScholarGoogle Scholar |

Barker NP, Weston PH, Rourke JP, Reeves G (2002) The relationships of the southern African Proteaceae as elucidated by internal transcribed spacer (ITS) DNA sequence data. Kew Bulletin 57, 867–883.
The relationships of the southern African Proteaceae as elucidated by internal transcribed spacer (ITS) DNA sequence data.Crossref | GoogleScholarGoogle Scholar |

Bayly MJ, Udovicic F, Gibbs AK, Parra-O C, Ladiges P (2008) Ribosomal DNA pseudogenes are widespread in the eucalypt group (Myrtaceae): implications for phylogenetic analysis. Cladistics 24, 131–146.
Ribosomal DNA pseudogenes are widespread in the eucalypt group (Myrtaceae): implications for phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar |

Benson D, McDougall L (2000) Ecology of Sydney plant species, Part 7b. Dicotyledon families Proteaceae to Rubiaceae. Cunninghamia 6, 1016–1202.

Bernhardt P, Weston PH (1996) The pollination ecology of Persoonia (Proteaceae) in eastern Australia. Telopea 6, 775–804.
The pollination ecology of Persoonia (Proteaceae) in eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Brock J (2001) ‘Native Plants of Northern Australia.’ (New Holland Publishers, Sydney, NSW, Australia)

Butcher R, Markey AS (2007) Persoonia manotricha (Proteaceae: Persoonioideae), a new species associated with Banded Iron Formation ranges in the Midwest region, Western Australia. Nuytsia 17, 135–146.

Carpenter RJ, Bannister JM, Jordan GJ, Lee DE (2010) Leaf fossils of Proteaceae tribe Persoonieae from the Late Oligocene–Early Miocene of New Zealand. Australian Systematic Botany 23, 1–15.
Leaf fossils of Proteaceae tribe Persoonieae from the Late Oligocene–Early Miocene of New Zealand.Crossref | GoogleScholarGoogle Scholar |

Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Research 31, 3497–3500.
Multiple sequence alignment with the Clustal series of programs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltVWjsrg%3D&md5=519c5a30f62a86d0723e9c83883150d1CAS |

Cornish-Bowden A (1985) Nomenclature for incompletely specified bases in nucleic acid sequences: recommendations 1984. Nucleic Acids Research 13, 3021–3030.
Nomenclature for incompletely specified bases in nucleic acid sequences: recommendations 1984.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXktVagsb4%3D&md5=c5cca6c41ceaca9603796b92862fe78cCAS |

Crisp MD, Cook LG (2007) A congruent molecular signature of vicariance across multiple plant lineages. Molecular Phylogenetics and Evolution 43, 1106–1117.
A congruent molecular signature of vicariance across multiple plant lineages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlvVOrtbw%3D&md5=4891cb4b26cd6c7e738cbcbf3effbcc5CAS |

Crisp MD, Cook LG (2009) Explosive radiation or cryptic mass extinction? Interpreting signature in molecular phylogenies. Evolution 63, 2257–2265.
Explosive radiation or cryptic mass extinction? Interpreting signature in molecular phylogenies.Crossref | GoogleScholarGoogle Scholar |

Crisp M, Cook L, Steane D (2004) Radiation of the Australian flora: what can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present-day communities? Philosophical Transactions of the Royal Society of London – B. Biological Sciences 359, 1551–1571.
Radiation of the Australian flora: what can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present-day communities?Crossref | GoogleScholarGoogle Scholar |

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

Federov AA (1974) ‘Chromosome Numbers of Flowering Plants.’ (Academy of Natural Sciences of the USSR: Leningrad, USSR)

Gardner RO (2008) Gender dimorphism in Toronia toru (Proteaceae). New Zealand Natural Sciences 33, 43–46.

Goldblatt P (1981) Index to plant chromosome numbers 1975–1978. Monographs in Systematic Botany, Missouri Botanic Gardens 6, 1–553.

Grimm GW, Denk T (2008) ITS evolution in Platanus (Platanaceae): homoeologues, pseudogenes and ancient hybridization. Annals of Botany 101, 403–419.
ITS evolution in Platanus (Platanaceae): homoeologues, pseudogenes and ancient hybridization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsl2jt7g%3D&md5=52505d631b7f0198699f25c0d43c73dcCAS |

Gurr E (1962) ‘Staining Animal Tissues. Practical and Theoretical.’ (Leonard Hill (Books): London, UK)

Hickey LJ (1973) Classification of the architecture of dicotyledonous leaves. American Journal of Botany 60, 17–33.
Classification of the architecture of dicotyledonous leaves.Crossref | GoogleScholarGoogle Scholar |

Holmes GD, Downing TL, James EA, Blacket MJ, Hoffmann AA, Bayly MJ (2014) Phylogeny of the holly grevilleas (Proteaceae) based on nuclear ribosomal and chloroplast DNA. Australian Systematic Botany 27, 56–77.
Phylogeny of the holly grevilleas (Proteaceae) based on nuclear ribosomal and chloroplast DNA.Crossref | GoogleScholarGoogle Scholar |

Huelsenbeck JP, Ronquist F (2001) MrBAYES: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.
MrBAYES: Bayesian inference of phylogeny.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvotV2isw%3D%3D&md5=c4a07e50b5513f9a72a171025f88f729CAS |

Jobes DV, Thien LB (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.
A conserved motif in the 5.8S ribosomal RNA (rRNA) gene is a useful diagnostic marker for plant internal transcribed spacer (ITS) sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjs1arurY%3D&md5=235caedb66d275833cf2296c6f344279CAS |

Johnson LAS, Briggs BG (1975) On the Proteaceae: the evolution and classification of a southern family. Botanical Journal of the Linnean Society 70, 83–182.
On the Proteaceae: the evolution and classification of a southern family.Crossref | GoogleScholarGoogle Scholar |

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.
Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar |

Kondo T, Crisp MD, Linde C, Bowman DMJS, Kawamura K, Kaneko S, Isagi Y (2012) Not an ancient relic: the endemic Livistona palms of arid central Australia could have been introduced by humans. Proceedings. Biological Sciences 279, 2652–2661.
Not an ancient relic: the endemic Livistona palms of arid central Australia could have been introduced by humans.Crossref | GoogleScholarGoogle Scholar |

Ladiges PY, Bayly MJ, Nelson G (2012) Searching for ancestral areas and artifactual centers of origin in biogeography: with comment on east–west patterns across southern Australia. Systematic Biology 61, 703–708.
Searching for ancestral areas and artifactual centers of origin in biogeography: with comment on east–west patterns across southern Australia.Crossref | GoogleScholarGoogle Scholar |

Lewis PO (2001) A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology 50, 913–925.
A likelihood approach to estimating phylogeny from discrete morphological character data.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38zntVKlsQ%3D%3D&md5=727faadfc3725555eea716bceab6d6fcCAS |

Liu JS, Schardl CL (1994) A conserved sequence in internal transcribed spacer 1 of plant nuclear rRNA genes. Plant Molecular Biology 26, 775–778.
A conserved sequence in internal transcribed spacer 1 of plant nuclear rRNA genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitVeisLs%3D&md5=887de17b2f3a1ebffb4be6b75cbdbd3bCAS |

Mast AR, Givnish TJ (2002) Historical biogeography and the origin of stomatal distributions in Banksia and Dryandra (Proteaceae) based on their cpDNA phylogeny. American Journal of Botany 89, 1311–1323.
Historical biogeography and the origin of stomatal distributions in Banksia and Dryandra (Proteaceae) based on their cpDNA phylogeny.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXislejsw%3D%3D&md5=ebed5ef50a7c2122354dafcbe1bfd3faCAS |

McIntosh E, Rossetto M, Weston PH, Wardle G (2014) Maintenance of strong morphological differentiation despite ongoing natural hybridization between sympatric species of Lomatia (Proteaceae). Annals of Botany 113, 861–872.
Maintenance of strong morphological differentiation despite ongoing natural hybridization between sympatric species of Lomatia (Proteaceae).Crossref | GoogleScholarGoogle Scholar |

Milner ML, Rossetto M, Crisp MD, Weston PH (2012) The impact of multiple biogeographic barriers and hybridization on species-level differentiation. American Journal of Botany 99, 2045–2057.
The impact of multiple biogeographic barriers and hybridization on species-level differentiation.Crossref | GoogleScholarGoogle Scholar |

Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
Biodiversity hotspots for conservation priorities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhs1Olsr4%3D&md5=a214f132668bcfcbc12ca78c08b4505fCAS |

Okuyama Y, Fujii N, Wakabayashi M, Kawakita A, Ito M, Watanabe M, Murakami N, Kato M (2005) Non-uniform 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.
Non-uniform concerted evolution and chloroplast capture: heterogeneity of observed introgression patterns in three molecular data partition phylogenies of Asian Mitella (Saxifragaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXptFGhtg%3D%3D&md5=54dc1795c3083e09c6ce739b00763567CAS |

Ramsay H (1963) Chromosome numbers in the Proteaceae. Australian Journal of Botany 11, 1–20.
Chromosome numbers in the Proteaceae.Crossref | GoogleScholarGoogle Scholar |

Rangan H, Bell KL, Baum DA, Fowler R, McConvell P, Saunders T, Spronck S, Kull CA, Murphy DJ (2015a) New genetic and linguistic analyses show ancient human influence on baobab evolution and distribution in Australia. PLoS One 10, e0119758
New genetic and linguistic analyses show ancient human influence on baobab evolution and distribution in Australia.Crossref | GoogleScholarGoogle Scholar |

Rangan H, Bell KL, Baum DA, Fowler R, McConvell P, Saunders T, Spronck S, Kull CA, Murphy DJ (2015b) Correction: New genetic and linguistic analyses show ancient human influence on baobab evolution and distribution in Australia. PLoS One 10, e0127582
Correction: New genetic and linguistic analyses show ancient human influence on baobab evolution and distribution in Australia.Crossref | GoogleScholarGoogle Scholar |

Ronquist F, Huelsenbeck JP (2003) MrBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
MrBAYES 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=6664bded48a2cfc2057fa199d4219cadCAS |

Rymer PD, Whelan RJ, Ayre DJ, Weston PH, Russell KG (2005) Reproductive success and pollinator effectiveness differ in common and rare Persoonia species (Proteaceae). Biological Conservation 123, 521–532.
Reproductive success and pollinator effectiveness differ in common and rare Persoonia species (Proteaceae).Crossref | GoogleScholarGoogle Scholar |

Sauquet H, Weston PH, Anderson CL, Barker NP, Cantrill DJ, Mast AR, Savolainen V (2009) Contrasted patterns of hyperdiversification in Mediterranean hotspots. Proceedings of the National Academy of Sciences of the United States of America 106, 221–225.
Contrasted patterns of hyperdiversification in Mediterranean hotspots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltF2ksw%3D%3D&md5=3dd12da098b7190752e84b8e92bf45daCAS |

Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Systematic Biology 49, 369–381.
Gaps as characters in sequence-based phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38zntlKjtg%3D%3D&md5=9fe1c3eaff3ec5fe4f7fc9e6c3d8f2fbCAS |

Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for the amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology 17, 1105–1109.
Universal primers for the amplification of three non-coding regions of chloroplast DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xhslel&md5=dbb6cf1b9b7bff238449de5a2f428176CAS |

Weston PH (1994) The Western Australian species of subtribe Persooniinae (Proteaceae: Persoonioideae: Persoonieae). Telopea 6, 51–165.
The Western Australian species of subtribe Persooniinae (Proteaceae: Persoonioideae: Persoonieae).Crossref | GoogleScholarGoogle Scholar |

Weston PH (1995a) Persoonioideae. In ‘Flora of Australia, Vol. 16’. (Ed. P McCarthy) pp. 47–125. (CSIRO: Melbourne, Vic., Australia)

Weston PH (1995b) Bellendenoideae. In ‘Flora of Australia, Vol. 16’. (Ed. P McCarthy) pp. 125–127. (CSIRO: Melbourne, Vic., Australia)

Weston PH (1999) Persoonia pauciflora (Proteaceae): a new species from the Hunter Valley, New South Wales. Telopea 8, 159–164.
Persoonia pauciflora (Proteaceae): a new species from the Hunter Valley, New South Wales.Crossref | GoogleScholarGoogle Scholar |

Weston PH, Barker NP (2006) A new suprageneric classification of the Proteaceae. Telopea 11, 314–344.
A new suprageneric classification of the Proteaceae.Crossref | GoogleScholarGoogle Scholar |

Weston PH, Johnson LAS (1997) Persoonia hindii (Proteaceae), a new species from the Newnes Plateau, New South Wales. Telopea 7, 199–203.
Persoonia hindii (Proteaceae), a new species from the Newnes Plateau, New South Wales.Crossref | GoogleScholarGoogle Scholar |