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

Molecular phylogeny of subgenus Polypompholyx (Utricularia; Lentibulariaceae) based on three plastid markers: diversification and proposal for a new section

Richard W. Jobson A C , Paulo C. Baleeiro A and Markus S. Reut B
+ Author Affiliations
- Author Affiliations

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

B Jagiellonian University in Kraków, Department of Plant Cytology and Embryology, 9 Gronostajowa Street, PO-31-044 Kraków, Poland.

C Corresponding author. Email: richard.jobson@rbgsyd.nsw.gov.au

Australian Systematic Botany 30(3) 259-278 https://doi.org/10.1071/SB17003
Submitted: 5 January 2017  Accepted: 12 July 2017   Published: 20 October 2017

Abstract

Phylogenetic relationships among all of the 47 recognised species and 10 putative new taxa of Utricularia subgenus Polypompholyx, were assessed using maximum parsimony and Bayesian inference analyses of DNA sequences representing the plastid rps16 intron, trnL–F intron and spacer regions and the trnD–T intron. We found strong jackknife and posterior-probability support for a monophyletic subgenus Polypompholyx and a sister relationship between the sections Polypompholyx + Tridentaria and Pleiochasia. Within the section Pleiochasia, are two well-supported major clades, each containing three supported clades. Our S-DIVA biogeographic analysis, using five major Australian drainage basins and New Zealand as geographic areas, estimated two early vicariance events between south-western and north-western mainland regions, corresponding with known periods of increased aridity at 15 and 6 million years ago. Subsequent dispersal events were estimated between northern and south-eastern Australia, with recent dispersal of species from south-western regions to the south-east and New Zealand occurring between 4 million and 1 million years ago. There were 28 speciation events inferred within the north-western region, followed by 9 for the south-western and south-eastern regions, indicating that the north-western monsoonal savanna habitats are a biodiversity hotspot for the lineage. We also show the evolutionary shifts in growth habit, and show that lifecycle corresponds strongly with shifts in seasonality between temperate and monsoonal regions. On the basis of our molecular phylogenetic results and morphology, we here designate a new sectional ranking for subgenus Polypompholyx.

Additional keywords: Australia, biogeography, character evolution, Lamiales, phylogenetics.


References

Bell CD, Soltis DE, Soltis PS (2010) The age and diversification of the angiosperms re-revisited. American Journal of Botany 97, 1296–1303.
The age and diversification of the angiosperms re-revisited.Crossref | GoogleScholarGoogle Scholar |

Bowman DMJS, Brown GK, Braby MF, Brown JR, Cook LG, Crisp MD, Ford F, Haberle S, Hughes J, Isagi Y, Joseph L, McBride J, Nelson G, Ladiges PY (2010) Biogeography of the Australian monsoon tropics. Journal of Biogeography 37, 201–216.
Biogeography of the Australian monsoon tropics.Crossref | GoogleScholarGoogle Scholar |

Brown R (1810) Prodromus floræ Novæ Hollandiæ et Insulæ Van-Diemen: exhibens characteres plantarum quas annis 1802–1805. (R. Taylor et socii: London, UK)

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. Journal of Biogeography 38, 1635–1656.
Decline of a biome: evolution, contraction, fragmentation, extinction and invasion of the Australian mesic zone biota.Crossref | GoogleScholarGoogle Scholar |

Catullo RA, Lanfear R, Doughty P, Keogh JS (2014) The biogeographical boundaries of northern Australia: evidence from ecological niche models and a multi-locus phylogeny of Uperoleia toadlets (Anura: Myobatrachidae). Journal of Biogeography 41, 659–672.
The biogeographical boundaries of northern Australia: evidence from ecological niche models and a multi-locus phylogeny of Uperoleia toadlets (Anura: Myobatrachidae).Crossref | GoogleScholarGoogle Scholar |

Cowie ID (2010) Notes on the identity, distribution and conservation status of the threatened plant species ‘Utricularia singeriana’ F.Muell. (Lentibulariaceae). The Beagle: Records of the Museums and Art Galleries of the Northern Territory 26, 119–121.

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=6133292eafeac6b6796b3da613933d6bCAS |

Crisp MD, Cook LG (2013) How was the Australian flora assembled over the last 65 million years? A molecular phylogenetic perspective. Annual Review of Ecology Evolution and Systematics 44, 303–324.
How was the Australian flora assembled over the last 65 million years? A molecular phylogenetic perspective.Crossref | GoogleScholarGoogle Scholar |

Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772
jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=73923fa81b12f7189024e36149b9c579CAS |

Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.
Bayesian phylogenetics with BEAUti and the BEAST 1.7.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFagu7fO&md5=f63ae629377ad80ee4088ee8ef3c1021CAS |

Fujita MK, McGuire JA, Donnellan SC, Moritz C (2010) Diversification and persistence at the arid-monsoonal interface: Australia-wide biogeography of the Bynoe’s gecko (Heteronotia binoei; Gekkonidae). Evolution 64, 2293–2314.
Diversification and persistence at the arid-monsoonal interface: Australia-wide biogeography of the Bynoe’s gecko (Heteronotia binoei; Gekkonidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFaltL3M&md5=23fcab1fa3e6fdf563269368c098195fCAS |

Gassin R (1993) Utricularia beaugleholei (Lentibulariaceae: subgenus Utricularia: section Pleiochasia), a new species from south-eastern Australia. Muelleria 8, 37–42.

Goloboff PA (1998) ‘NONA.’ (Published by the author: Túcuman, Argentina)

Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 52, 696–704.
A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood.Crossref | GoogleScholarGoogle Scholar |

Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.

Ibarra-Laclette E, Lyons E, Hernández-Guzmán G, Pérez-Torres CA, Carretero-Paulet L, Chang T-H, Lan T, Welch AJ, Abraham Juárez MJ, Simpson J, Fernández-Cortés A, Arteaga-Vázquez M, Góngora-Castillo E, Acevedo-Hernández G, Schuster SC, Himmelbauer H, Minoche AE, Xu S, Lynch M, Oropeza-Aburto A, Cervantes-Pérez SA, de Jesús Ortega-Estrada M, Cervantes-Luevano JI, Michael TP, Mockler T, Bryant D, Herrera-Estrella A, Albert VA, Herrera-Estrella L (2013) Architecture and evolution of a minute plant genome. Nature 498, 94–98.
Architecture and evolution of a minute plant genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXotFSms7c%3D&md5=3186ae31e181a689c52166ed822ac7a6CAS |

Jobson RW (2012) A new species of Utricularia (Lentibulariaceae) from northern Queensland, Australia. Telopea 14, 49–57.
A new species of Utricularia (Lentibulariaceae) from northern Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |

Jobson RW (2013) Five new species of Utricularia (Lentibulariaceae) from Australia. Telopea 15, 127–142.
Five new species of Utricularia (Lentibulariaceae) from Australia.Crossref | GoogleScholarGoogle Scholar |

Jobson RW, Baleeiro PC (2015) Two new species of Utricularia (Lentibulariaceae) from the North West region of Western Australia. Telopea 18, 201–208.
Two new species of Utricularia (Lentibulariaceae) from the North West region of Western Australia.Crossref | GoogleScholarGoogle Scholar |

Jobson RW, Playford J, Cameron KM, Albert VA (2003) Molecular phylogenetics of Lentibulariaceae inferred from plastid rps16 intron and trnL–F DNA sequences: implications for character evolution and biogeography. Systematic Botany 28, 157–171.
Molecular phylogenetics of Lentibulariaceae inferred from plastid rps16 intron and trnL–F DNA sequences: implications for character evolution and biogeography.Crossref | GoogleScholarGoogle Scholar |

Juniper BE, Robbins RJ, Joel DM (1989) ‘The Carnivorous Plants.’ (Academic: London, UK)

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, Meintjes 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 |

Lavin M, Luckow M (1993) Origins and relationships of tropical North America in the context of the boreotropics hypothesis. American Journal of Botany 80, 1–14.
Origins and relationships of tropical North America in the context of the boreotropics hypothesis.Crossref | GoogleScholarGoogle Scholar |

Lowrie A (1998) A new species of Utricularia (Lentibulariaceae) from the south-west of Western Australia. Nuytsia 12, 37–41.

Lowrie A (2002) Utricularia petertaylorii (Lentibulariaceae), a new species from the south west of Western Australia. Nuytsia 14, 405–410.

Müller K, Borsch T (2005) Phylogenetics of Utricularia (Lentibulariaceae) and molecular evolution of the trnK intron in a lineage with high substitutional rates. Plant Systematics and Evolution 250, 39–67.
Phylogenetics of Utricularia (Lentibulariaceae) and molecular evolution of the trnK intron in a lineage with high substitutional rates.Crossref | GoogleScholarGoogle Scholar |

Pagel M (1994) Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proceedings of the Royal Society of London 255, 37–45.
Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters.Crossref | GoogleScholarGoogle Scholar |

Pepper M, Doughty P, Keogh JS (2013) Geodiversity and endemism in the iconic Australian Pilbara region: a review of landscape evolution and biotic response in an ancient refugium. Journal of Biogeography 40, 1225–1239.
Geodiversity and endemism in the iconic Australian Pilbara region: a review of landscape evolution and biotic response in an ancient refugium.Crossref | GoogleScholarGoogle Scholar |

Reut MS, Fineran BA (1999) An evaluation of the taxonomy of Utricularia dichotoma Labill., U. monanthos Hook.f., and U. novae-zelandiae Hook.f. (Lentibulariaceae). New Zealand Journal of Botany 37, 243–255.
An evaluation of the taxonomy of Utricularia dichotoma Labill., U. monanthos Hook.f., and U. novae-zelandiae Hook.f. (Lentibulariaceae).Crossref | GoogleScholarGoogle Scholar |

Reut MS, Fineran BA (2000) Ecology and vegetative morphology of the carnivorous plant Utricularia dichotoma (Lentibulariaceae) in New Zealand. New Zealand Journal of Botany 38, 433–450.
Ecology and vegetative morphology of the carnivorous plant Utricularia dichotoma (Lentibulariaceae) in New Zealand.Crossref | GoogleScholarGoogle Scholar |

Reut MS, Jobson RW (2010) A phylogenetic study of subgenus Polypompholyx: a parallel radiation of Utricularia (Lentibulariaceae) throughout Australasia. Australian Systematic Botany 23, 152–161.
A phylogenetic study of subgenus Polypompholyx: a parallel radiation of Utricularia (Lentibulariaceae) throughout Australasia.Crossref | GoogleScholarGoogle Scholar |

Shaw J, Shafer HL, Leonard OR, Kovach MJ, Schorr M, Morris AB (2005) The tortoise and the hare ii: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. American Journal of Botany 92, 142–166.
The tortoise and the hare ii: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Klsbc%3D&md5=92e13057054b00f2f11658f12b17c693CAS |

Sniderman JMK, Pilmans B, O’Sullivan PB, Kersaw AP (2007) Climate and vegetation in southeastern Australia respond to southern hemisphere insolation forcing in the late Pliocene–early Pleistocene. Geology 35, 41–44.
Climate and vegetation in southeastern Australia respond to southern hemisphere insolation forcing in the late Pliocene–early Pleistocene.Crossref | GoogleScholarGoogle Scholar |

Sniderman JMK, Woodhead JD, Hellstrom J, Jordan GJ, Drysdale RN, Tyler JJ, Porch N (2016) Pliocene reversal of late Neogene aridification. Proceedings of the National Academy of Sciences of the United States of America 113, 1999–2004.
Pliocene reversal of late Neogene aridification.Crossref | GoogleScholarGoogle Scholar |

Stein JL, Hutchinson MF, Stein JA (2014) A new stream and nested catchment framework for Australia. Hydrology and Earth System Sciences 18, 1917–1933.
A new stream and nested catchment framework for Australia.Crossref | GoogleScholarGoogle Scholar |

Sun Y, Li Y, Vargas-Mendoza CF, Wang F, Xing F (2016) Colonization and diversification of the Euphorbia species (sect. Aphyllis subsect. Macaronesicae) on the Canary Islands. Scientific Reports 6, 34454
Colonization and diversification of the Euphorbia species (sect. Aphyllis subsect. Macaronesicae) on the Canary Islands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhs1Smu7jI&md5=0a0ff665b0f58010ccf54320c1e2caf5CAS |

Taylor P (1989) The genus Utricularia. In ‘Kew Bulletin, Additional Series XIV’. (HMSO: London, UK)

Toon A, Crisp MD, Gamage H, Mant J, Morris DC, Schmidt S, Cook LG (2015) Key innovation or adaptive change? A test of leaf traits using Triodiinae in Australia. Scientific Reports 5, 12398
Key innovation or adaptive change? A test of leaf traits using Triodiinae in Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtlCjtrrP&md5=f8866410c33cb565ad925566adbbe540CAS |

Wakabayashi H (2010) Utricularia linearis (Lentibulariaceae), a new species from the Howard Springs, Northern Territory, Australia. The Journal of Insectivorous Plant Society 61, 88–92.

Yu Y, Harris AJ, He XJ (2010) S-DIVA (statistical dispersal-vicariance analysis): a tool for inferring biogeographic histories. Molecular Phylogenetics and Evolution 56, 848–850.
S-DIVA (statistical dispersal-vicariance analysis): a tool for inferring biogeographic histories.Crossref | GoogleScholarGoogle Scholar |

Yu Y, Harris AJ, Blair C, He XJ (2015) RASP (reconstruct dispersal-vicariance analysis): a tool for historical biogeography. Molecular Phylogenetics and Evolution 87, 46–49.
RASP (reconstruct dispersal-vicariance analysis): a tool for historical biogeography.Crossref | GoogleScholarGoogle Scholar |