The impact of multiple molecular and morphological data sets on the phylogenetic reconstruction of subtribe Neurachninae (Poaceae: Panicoideae: Paniceae)
E. J. Thompson A B and Melodina Fabillo AA Queensland Herbarium, Department of Environment and Science, Brisbane Botanic Gardens, Mt Coot-tha Road, Toowong, Qld 4066, Australia.
B Corresponding author. Email: john.thompson@des.qld.gov.au; jthompso@bigpond.net.au
Australian Systematic Botany 34(3) 227-251 https://doi.org/10.1071/SB20015
Submitted: 3 June 2020 Accepted: 16 February 2021 Published: 27 April 2021
Abstract
The taxonomy of Neurachninane has been unstable, with its member genera consisting of Ancistrachne, Calyptochloa, Cleistochloa, Dimorphochloa, Neurachne, Paraneurachne and Thyridolepis, changing since its original circumscription that comprised only the latter three genera. Recent studies on the phylogeny of Neurachninae have focused primarily on molecular data. We analysed the phylogeny of Neurachninae on the basis of molecular data from seven molecular loci (plastid markers: matK, ndhF, rbcL, rpl16, rpoC2 and trnLF, and ribosomal internal transcribed spacer, ITS) and morphological data from 104 morphological characters, including new taxonomically informative micromorphology of upper paleas. We devised an impact assessment scoring (IAS) protocol to aid selection of a tree for inferring the phylogeny of Neurachninae. Combining morphological and molecular data resulted in a well resolved phylogeny with the highest IAS value. Our findings support reinstatement of subtribe Neurachninae in its original sense, Neurachne muelleri and Dimorphochloa rigida. We show that Ancistrachne, Cleistochloa and Dimorphochloa are not monophyletic and Ancistrachne maidenii, Calyptochloa, Cleistochloa and Dimorphochloa form a new group, the cleistogamy group, united by having unique morphology associated with reproductive dimorphism.
References
Aliscioni SS, Giussani LM, Zuloaga FO, Kellogg EA (2003) A molecular phylogeny of Panicum (Poaceae: Paniceae). A test of monophyly and phylogenetic placement within the Panicoideae. American Journal of Botany 90, 796–821.| A molecular phylogeny of Panicum (Poaceae: Paniceae). A test of monophyly and phylogenetic placement within the Panicoideae.Crossref | GoogleScholarGoogle Scholar | 21659176PubMed |
Barthlott W, Neinhuis C, Cutler D, Ditsch F, Meusel I, Wilhelmi H (1998) Classification and terminology of plant epicuticular waxes. Botanical Journal of the Linnean Society 126, 237–260.
| Classification and terminology of plant epicuticular waxes.Crossref | GoogleScholarGoogle Scholar |
Beentje H (2010) ‘The Kew Plant Glossary: an illustrated dictionary of plant terms.’ (Kew Publishing, Royal Botanic Gardens: London, UK)
Blake ST (1941) New genera of Australian grasses. University of Queensland Papers, Department of Biology 1, 1–12.
Blake ST (1958) New criteria for distinguishing genera allied to Panicum (Gramineae). Proceedings of the Royal Society of Queensland 70, 15–19.
Blake ST (1970) Taxonomic and nomenclature studies in the Gramineae. No. 2. Proceedings of the Royal Society of Queensland 81, 1–26.
Blake ST (1972) Neurachne and its allies (Gramineae). Contributions from the Queensland Herbarium 13, 1–53.
Brown R (1810) ‘Prodomus Florae Novae Hollandiae et Insulae Van-Diemen’. Vol. 1, pp. 145–590. (Richard Taylor and Associates: London, UK)
Campbell CS, Quinn JA, Cheplick GP, Bell TJ (1983) Cleistogamy in grasses. Annual Review of Ecology and Systematics 14, 411–441.
| Cleistogamy in grasses.Crossref | GoogleScholarGoogle Scholar |
Chase A (1918) Axillary cleistogenes in some American grasses. American Journal of Botany 5, 254–258.
| Axillary cleistogenes in some American grasses.Crossref | GoogleScholarGoogle Scholar |
Cheplick GP (2007) Plasticity of chasmogamous and cleistogamous reproductive allocation grasses. Aliso 23, 286–294.
| Plasticity of chasmogamous and cleistogamous reproductive allocation grasses.Crossref | GoogleScholarGoogle Scholar |
Christin PA, Wallace MJ, Clayton H, Furbank RT, Hattersley PW, Sage RF, Macfarlane TD, Ludwig M (2012) Multiple photosynthetic transitions, polypoidy, and lateral gene transfer in the grass subtribe Neurachninae. Journal of Experimental Botany 63, 6297–6308.
| Multiple photosynthetic transitions, polypoidy, and lateral gene transfer in the grass subtribe Neurachninae.Crossref | GoogleScholarGoogle Scholar | 23077201PubMed |
Clayton WD, Renvoize SA (1986) ‘Genera Graminum Grasses of the World.’ (Her Majesty’s Stationery Office: London, UK)
Columbus JT, Cerros-Tlatilpa R, Kinney MS, Siqueiros-Delgado ME, Bell HL, Griffith MP, Refulio-Rodriguez NF (2007) Phylogenetics of Chloridoideae (Gramineae): a preliminary study based on nuclear ribosomal internal transcribed spacer and chloroplast trnL-F sequences. Aliso 23, 565–579.
Connor HE (1979) Breeding systems in the grasses: a survey. New Zealand Journal of Botany 17, 547–574.
| Breeding systems in the grasses: a survey.Crossref | GoogleScholarGoogle Scholar |
Culley TM, Klooster MR (2007) The cleistogamous breeding system: a review of its frequency, evolution, and ecology in angiosperms. Botanical Review 73, 1–30.
| The cleistogamous breeding system: a review of its frequency, evolution, and ecology in angiosperms.Crossref | GoogleScholarGoogle Scholar |
Dengler NG, Dengler RE, Hattersley PW (1985) Differing ontogenetic origins of PCR (‘Kranz’) sheaths in leaf blades of C4 grasses (Poaceae). American Journal of Botany 72, 284–302.
| Differing ontogenetic origins of PCR (‘Kranz’) sheaths in leaf blades of C4 grasses (Poaceae).Crossref | GoogleScholarGoogle Scholar |
Doyle J, Doyle J (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19, 11–15.
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
| MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 15034147PubMed |
Ellis RP (1976) A procedure for standardizing comparative leaf anatomy in the Poaceae: 1. The leaf-blade as viewed in transverse section. Bothalia 12, 65–109.
| A procedure for standardizing comparative leaf anatomy in the Poaceae: 1. The leaf-blade as viewed in transverse section.Crossref | GoogleScholarGoogle Scholar |
Ellis RP (1979) A procedure for standardizing comparative leaf anatomy in the Poaceae: 2. The epidermis as seen in surface view. Bothalia 12, 641–671.
| A procedure for standardizing comparative leaf anatomy in the Poaceae: 2. The epidermis as seen in surface view.Crossref | GoogleScholarGoogle Scholar |
Felsenstein J (1985) Confidence-limits on phylogenies: an approach using bootstraps. Evolution 39, 783–791.
| Confidence-limits on phylogenies: an approach using bootstraps.Crossref | GoogleScholarGoogle Scholar | 28561359PubMed |
Freckmann RW, Lelong MG (2003) Dichanthelium (Hitch. & Chase) Gould. In ‘Flora of North America’. (Eds ME Barkworth, KM Capels, S Long, MB Piep) Vol. 24, pp. 406–450. (Oxford University Press: New York, NY, USA)
Frohlich MW (1984) Freehand sectioning with parafilm. Stain Technology 59, 61–62.
| Freehand sectioning with parafilm.Crossref | GoogleScholarGoogle Scholar | 6548052PubMed |
Grass Phylogeny Working Group (2001) Phylogeny and subfamilial classification of the grasses (Poaceae). Annals of the Missouri Botanical Garden 88, 373–457.
| Phylogeny and subfamilial classification of the grasses (Poaceae).Crossref | GoogleScholarGoogle Scholar |
Grass Phylogeny Working Group II (2012) New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytologist 193, 304–312.
| New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins.Crossref | GoogleScholarGoogle Scholar |
Harris JG, Harris MW (1994) ‘Plant Identification Terminology: an Illustrated Glossary.’ (Spring Lake Publishing: Spring Lake, UT, USA)
Hattersley PW, Watson L, Johnson CR (1982) Remarkable leaf anatomical variations in Neurachne and its allies (Poaceae) in relation to C3 and C4 photosynthesis. Botanical Journal of the Linnean Society 84, 265–272.
| Remarkable leaf anatomical variations in Neurachne and its allies (Poaceae) in relation to C3 and C4 photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Heath TA, Hedtke SM, Hillis DM (2008) Taxon sampling and the accuracy of phylogenetic analyses. Journal of Systematics and Evolution 46, 239–257.
Hewson HJ (1988) Plant indumentum: a handbook of terminology. In ‘Australian Flora and Fauna Series’. Vol. 9, pp. 1–27. (Australian Government Publishing Service: Canberra, ACT, Australia)
Hillis DM (1987) Molecular versus morphological approaches to systematics. Annual Review of Ecology and Systematics 18, 23–42.
| Molecular versus morphological approaches to systematics.Crossref | GoogleScholarGoogle Scholar |
Hillis DM, Wiens JJ (2000) Molecules versus morphology in systematics: conflicts, artifacts, and misconceptions. In ‘Phylogenetic Analysis of Morphological Data’. (Ed. JJ Wiens) pp. 1–19. (Smithsonian Institution Press: Washington, DC, USA)
Hilu KW, Wright K (1982) Systematics of Gramineae, a cluster analysis study. Taxon 31, 9–36.
| Systematics of Gramineae, a cluster analysis study.Crossref | GoogleScholarGoogle Scholar |
Hubbard CE (1933a) Cleistochloa subjuncea C.E.Hubbard. Hooker’s Icones Plantarum 33, 1–6.
Hubbard CE (1933b) Calyptochloa gracillima C.E.Hubbard. Hooker’s Icones Plantarum 33, 1–3.
Jacobs SWL, Wall CA (1993) Ancistrachne. In ‘Flora of New South Wales’. (Ed. GJ Harden) Vol. 4, pp. 452–453. (New South Wales University Press: Sydney, NSW, Australia)
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 | 22543367PubMed |
Kellogg EA (2015) ‘The Families and Genera of Vascular Plants. Flowering Plants: Monocots: Poaceae.’ (Springer: Cham, Switzerland)
Kellogg EA, Campbell CS (1987) Phylogenetic analysis of the Gramineae. In ‘Grass Systematics and Evolution’. (Eds TR Soderstrom, W Hilu, CS Campbell, ME Barkworth) pp. 310–322. (Smithsonian Institution Press: Washington, DC, USA)
Khoshravesh R, Stata M, Busch FA, Saladie M, Castellii JM, Dakin N, Hattersley PW, Macfarlane TD, Sage RF, Ludwig M, Sage TL (2020) The evolutionary origin of C4 photosynthesis in the grass subtribe Neurachninae. Plant Physiology 182, 566–583.
| The evolutionary origin of C4 photosynthesis in the grass subtribe Neurachninae.Crossref | GoogleScholarGoogle Scholar | 31611421PubMed |
Lipscomb DL (1992) Parsimony, homology and the analysis of multistate characters. Cladistics 8, 45–65.
| Parsimony, homology and the analysis of multistate characters.Crossref | GoogleScholarGoogle Scholar |
McClusker A (1999). Glossary. In ‘Flora of Australia: Introduction’. (Eds AE Orchard, HS Thompson) Vol. 1, pp. 585–636. (ABRS: Canberra, ACT, Australia; and CSIRO Publishing: Melbourne, Vic., Australia)
Mejia-Saules T, Bisby FA (2003) Silica bodies and hooked papillae of Melica species (Gramineae: Pooideae). Botanical Journal of the Linnean Society 141, 447–463.
| Silica bodies and hooked papillae of Melica species (Gramineae: Pooideae).Crossref | GoogleScholarGoogle Scholar |
Metcalfe CR (1960) ‘Anatomy of the Monocotyledons 1. Gramineae.’ (Oxford Press University: London, UK)
Morat P (1978) Note sur les graminees de la Nouvelle-Caledonie. Adansonia 18, 257–266.
Morrone O, Denham SS, Aliscioni SS, Zuloaga FO (2008) Parodiophyllochloa, a new genus segragated from Panicum (Paniceae, Poaceae) based on morphological and molecular data. Systematic Botany 33, 66–76.
| Parodiophyllochloa, a new genus segragated from Panicum (Paniceae, Poaceae) based on morphological and molecular data.Crossref | GoogleScholarGoogle Scholar |
Morrone O, Aagesen L, Scataglini MA, Salariato DL, Denham SS, Chemisquy MA, Sede SM, Giussani LM, Kellogg EA, Zuloaga FO (2012) Phylogeny of the Paniceae (Poaceae: Panicoideae): integrating plastid DNA sequences and morphology into a new classification. Cladistics 28, 333–356.
| Phylogeny of the Paniceae (Poaceae: Panicoideae): integrating plastid DNA sequences and morphology into a new classification.Crossref | GoogleScholarGoogle Scholar |
NSW Government (2018) Threatened species. Available at http://www.environment.nsw.gov.au/topics/animals-and-plants/threatened-species [accessed 20 November 2018]
Ortúñez E, Cano-Ruiz J (2013) Epidermal micromorphology of the genus Festuca L. subgenus Festuca (Poaceae). Plant Systematics and Evolution 299, 1471–1483.
| Epidermal micromorphology of the genus Festuca L. subgenus Festuca (Poaceae).Crossref | GoogleScholarGoogle Scholar |
Ortúñez E, de la Fuente V (2010) Epidermal micromorphology of the genus Festuca L. (Poaceae) in the Iberian Peninsula. Plant Systematics and Evolution 284, 201–218.
| Epidermal micromorphology of the genus Festuca L. (Poaceae) in the Iberian Peninsula.Crossref | GoogleScholarGoogle Scholar |
Poe S, Wiens JJ (2000) Character selection and the methodology of morphological phylogenetics. In ‘Phylogenetic Analysis of Morphological Data’. (Ed. JJ Wiens) pp. 20–36. (Smithsonian Institution Press: Washington, DC, USA)
Quinn JA (1998) Ecological aspects of sex expression in grasses. In ‘Population Biology of Grasses’. (Ed. GP Cheplick) pp. 136–154. (Cambridge University Press: Cambridge, UK)
Quiroga RE, Golluscio RA, Blanco LJ, Fernandez RJ (2010) Aridity and grazing as convergent selective forces: an experiment with an Arid Chaco bunchgrass. Ecological Applications 20, 1876–1889.
| Aridity and grazing as convergent selective forces: an experiment with an Arid Chaco bunchgrass.Crossref | GoogleScholarGoogle Scholar | 21049876PubMed |
Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenback JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
| MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar | 22357727PubMed |
Rost TL, Simper AD (1975) The germination lid: a characteristic of the lemma in the Paniceae. Madrono 23, 68–72.
Sauquet H, Doyle J, Scharaschkin T, Borsch T, Hilu KW, Chatrou LW, Thomas AL (2003) Phylogenetic analysis of Magnoliales and Myristicaceae based on multiple data sets: implications for character evolution. Botanical Journal of the Linnean Society 142, 125–186.
| Phylogenetic analysis of Magnoliales and Myristicaceae based on multiple data sets: implications for character evolution.Crossref | GoogleScholarGoogle Scholar |
Scataglini MA, Aliscioni S, Zuloaga FO (2014) On the taxonomic position of Panicum scabridum (Poaceae, Panicoideae, Paspaleae). Phytotaxa 163, 1–15.
| On the taxonomic position of Panicum scabridum (Poaceae, Panicoideae, Paspaleae).Crossref | GoogleScholarGoogle Scholar |
Scotland RW, Olmstead RG, Bennett JR (2003) Phylogenetic reconstruction: the role of morphology. Systematic Biology 52, 539–548.
| Phylogenetic reconstruction: the role of morphology.Crossref | GoogleScholarGoogle Scholar | 12857644PubMed |
Simon BK (2002) Key to genera of Australian grasses. In ‘Flora of Australia. Poaceae 1: Introduction and Atlas’. (Eds K Mallett, AE Orchard) Vol. 43, pp. 263–277. (ABRS: Canberra, ACT, Australia; and CSIRO Publishing: Melbourne, Vic., Australia)
Simon BK (2007) Grass phylogeny and classification: conflict of morphology and molecules. Aliso 23, 259–266.
| Grass phylogeny and classification: conflict of morphology and molecules.Crossref | GoogleScholarGoogle Scholar |
Smith GR (1990) Homology in morphometrics and phylogenetics. In ‘Proceedings of the Michigan Morphometrics Workshop’, 16–28 May 1988, Ann Arbor, MI, USA. (Eds FJ Rohlf, FL Bookstein) pp. 325–338. (The University of Michigan Museum of Zoology: Ann Arbor, MI, USA)
Smith ND, Turner AH (2005) Morphology’s role in phylogenetic reconstruction: perspective from paleontology. Systematic Biology 54, 166–173.
| Morphology’s role in phylogenetic reconstruction: perspective from paleontology.Crossref | GoogleScholarGoogle Scholar |
Soreng RJ, Davis JI (1998) Phylogenetics and character evolution in the grass family (Poaceae): simultaneous analysis of morphological and chloroplast DNA restriction site character sets. Botanical Review 64, 1–85.
| Phylogenetics and character evolution in the grass family (Poaceae): simultaneous analysis of morphological and chloroplast DNA restriction site character sets.Crossref | GoogleScholarGoogle Scholar |
Soreng RJ, Peterson PM, Romaschenko K, Davidse G, Zuloaga FO, Judziewicz EJ, Filgueiras TS, Davis JI, Morrone O (2015) A worldwide phylogenetic classification of the Poaceae (Gramineae). Journal of Systematics and Evolution 53, 117–137.
| A worldwide phylogenetic classification of the Poaceae (Gramineae).Crossref | GoogleScholarGoogle Scholar |
Soreng RJ, Peterson PM, Romaschenko K, Davidse G, Teisher JK, Clark LG, Barbera P, Gillespie LJ, Zuloaga FO (2017) A worldwide phylogenetic classification of the Poaceae (Gramineae) II: and update and a comparison of the two 2015 classifications. Journal of Systematics and Evolution 55, 259–290.
| A worldwide phylogenetic classification of the Poaceae (Gramineae) II: and update and a comparison of the two 2015 classifications.Crossref | GoogleScholarGoogle Scholar |
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
| RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar | 16928733PubMed |
Stevens PF (1991) Character states, morphological variation, and phylogenetic analysis: a review. Systematic Botany 16, 553–583.
| Character states, morphological variation, and phylogenetic analysis: a review.Crossref | GoogleScholarGoogle Scholar |
Swofford D (2002) ‘Phylogenetic analysis using parsimony (PAUP 4.0* b10).’ (Sinauer Associates Inc.: Sunderland, MA, USA)
Thompson EJ (2017) Elionurus purpureus (Panicoideae: Andropogoneae: Rottboelliinae), a new species for Queensland: circumscription and breeding system Austrobaileya 10, 139–162.
Thompson EJ (2019) A re-evaluation of the taxonomic status of the Australian species of Arthraxon Beauv. and Thelepogon Roth (Poaceae: Panicoideae: Andropogoneae) based on gross morphological, micromorphology and anatomical characters. Austrobaileya 10, 480–505.
Thompson EJ, Simon BK (2012) A revision of Calyptochloa C.E.Hubb. (Poaceae), with two new species and a new subspecies. Austrobaileya 8, 634–652.
Vickery JW (1961a) Contributions to the taxonomy of Australian grasses. Contributions from the New South Wales National Herbarium 3, 84
Vickery JW (1961b) 19. Gramineae. Contributions from the New South Wales National Herbarium, Flora Series 19, 1–124.
Wagner GP (1989) The origin of morphological characters and the biological basis of homology. Evolution 43, 1157–1171.
| The origin of morphological characters and the biological basis of homology.Crossref | GoogleScholarGoogle Scholar | 28564509PubMed |
Washburn JD, Schnable JC, Davidse G, Pires C (2015) Phylogenetic and photosynthesis of the grass subtribe Paniceae. American Journal of Botany 102, 1493–1505.
| Phylogenetic and photosynthesis of the grass subtribe Paniceae.Crossref | GoogleScholarGoogle Scholar | 26373976PubMed |
Watson L, Dallwitz MJ (1992) ‘The Grass Genera of the World.’ (University Press: Cambridge, UK)
Weatherwax P (1928) Cleistogamy in two species of Danthonia. Botanical Gazette 85, 104–109.
| Cleistogamy in two species of Danthonia.Crossref | GoogleScholarGoogle Scholar |
Webster RD (1987) ‘The Australian Paniceae (Poaceae).’ (J. Cramer: Berlin, Germany)
Wiens JJ (2004) The role of morphological data in phylogenetic reconstruction. Systematic Biology 53, 653–661.
| The role of morphological data in phylogenetic reconstruction.Crossref | GoogleScholarGoogle Scholar |
Wills KE, Whalley RDB, Bruhl JJ (2000) Systematic Studies in Paniceae (Poaceae): Homopholis and Whalleya gen. et sp. nov. Australian Systematic Botany 13, 437–468.
| Systematic Studies in Paniceae (Poaceae): Homopholis and Whalleya gen. et sp. nov.Crossref | GoogleScholarGoogle Scholar |
Wortley AH, Bennett JR, Scotland RW (2002) Taxonomy and phylogenetic reconstruction: two distinct research agendas in systematics. Edinburgh Journal of Botany 59, 335–349.
| Taxonomy and phylogenetic reconstruction: two distinct research agendas in systematics.Crossref | GoogleScholarGoogle Scholar |
Wortley AH, Rudall PJ, Harris DJ, Scotland RW (2005) How much data are needed to resolve a difficult phylogeny? Case study in Lamiales. Systematic Biology 54, 697–709.
| How much data are needed to resolve a difficult phylogeny? Case study in Lamiales.Crossref | GoogleScholarGoogle Scholar | 16195214PubMed |
Zelditch ML, Fink WL, Swiderski DL (1995) Morphometrics, homology, and phylogenetics: quantified characters as synapomorphies. Systematic Biology 44, 179–189.
| Morphometrics, homology, and phylogenetics: quantified characters as synapomorphies.Crossref | GoogleScholarGoogle Scholar |
Zuloaga FO, Morrone O, Giussani LM (2000) A cladistic analysis of the Paniceae: a preliminary approach. In ‘Grasses: Systematics and Evolution’. (Eds SWL Jacobs, JE Everett) pp. 123–135. (CSIRO Publishing: Melbourne, Vic., Australia)
Zwickl DJ, Hillis DM (2002) Increased taxon sampling greatly reduces phylogenetic error. Systematic Biology 51, 588–598.
| Increased taxon sampling greatly reduces phylogenetic error.Crossref | GoogleScholarGoogle Scholar | 12228001PubMed |