Plastid phylogenomics of the Eriostemon group (Rutaceae; Zanthoxyloideae): support for major clades and investigation of a backbone polytomy
Harvey K. Orel
A * , Todd G. B. McLay A B , Will C. Neal A , Paul I. Forster C and Michael J. Bayly A
A School of Biosciences, The University of Melbourne, Parkville, Vic. 3010, Australia.
B Royal Botanic Gardens Victoria, Melbourne, Vic. 3004, Australia.
C Queensland Herbarium & Biodiversity Science, Department of Environment & Science, Brisbane Botanic Gardens, Toowong, Qld 4066, Australia.
Australian Systematic Botany 36(5) 355-385 https://doi.org/10.1071/SB23011
Submitted: 28 April 2023 Accepted: 1 August 2023 Published: 22 August 2023
Abstract
Most of Australia’s sclerophyllous Rutaceae belong to a clade informally known as the ‘Eriostemon group’ (including 16 genera, ~209 species). We investigated generic relationships in this group using analyses of complete plastome sequence data for 60 species and analyses of a supermatrix including sequences of four plastome spacer regions for 22 additional species. Maximum likelihood, Bayesian inference, and shortcut coalescent phylogenetic analyses produced congruent phylogenies that were highly supported, except for a series of short unsupported branches in the backbone of the Eriostemon group. We found high support for four major clades branching from this polytomy and discuss evolutionary inferences of generic relationships in each lineage. In an effort to resolve the polytomy, we analysed gene tree topologies in tree space, phylogenetic informativeness with likelihood mapping, and conducted topology tests to assess support for all possible topological resolutions of the polytomy. These approaches did not clarify the polytomy, which may be caused by insufficient data, features of plastome evolution, or rapid radiation. Results from analyses of the combined supermatrix dataset suggest that Philotheca section Philotheca is paraphyletic with regards to Drummondita and Geleznowia. In all phylogenies, Philotheca sections Corynonema and Cyanochlamys were not placed with other members of Philotheca.
Keywords: Asterolasia, Australasia, Australia, Chorilaena, Correa, Crowea, Diplolaena, Drummondita, Eriostemon, Geleznowia, Halfordia, Leionema, likelihood mapping, Muiriantha, Myrtopsis, Nematolepis, Neoschmidia, Phebalium, Philotheca, polytomy, Rutaceae, topology tests, tree space.
References
Anderson BM, Binks RM, Byrne M, Crawford AD, Shepherd KA (2023) Using RADseq to resolve species boundaries in a morphologically complex group of yellow-flowered shrubs (Geleznowia, Rutaceae). Australian Systematic Botany 36(4), 277-311.
| Crossref | Google Scholar |
Appelhans MS, Bayly MJ, Heslewood MM, Groppo M, Verboom GA, Forster PI, Kallunki JA, Duretto MF (2021) A new subfamily classification of the Citrus family (Rutaceae) based on six nuclear and plastid markers. Taxon 70, 1035-1061.
| Crossref | Google Scholar |
Armstrong JA (1979) Biotic pollination mechanisms in the Australian flora – a review. New Zealand Journal of Botany 17, 467-508.
| Crossref | Google Scholar |
Armstrong JA (1987) Pollination syndromes as generic determinants. Australian Systematic Botany Society Newsletter 53, 54-59.
| Google Scholar |
Armstrong JA (1991) Studies on pollination and systematics in the Australian Rutaceae. PhD thesis, University of New South Wales, Sydney, NSW, Australia. Available at http://hdl.handle.net/1959.4/59714
Baker WJ, Bailey P, Barber V, Barker A, Bellot S, Bishop D, Botigué LR, Brewer G, Carruthers T, Clarkson JJ, Cook J (2022) A comprehensive phylogenomic platform for exploring the angiosperm tree of life. Systematic Biology 71, 301-319.
| Crossref | Google Scholar |
Bardon L, Sothers C, Prance GT, Malé P-JG, Xi Z, Davis CC, Murienne J, García-Villacorta R, Coissac E, Lavergne S, Chave J (2016) Unraveling the biogeographical history of Chrysobalanaceae from plastid genomes. American Journal of Botany 103, 1089-1102.
| Crossref | Google Scholar |
Barrett RA, Bayly MJ, Duretto MF, Forster PI, Ladiges PY, Cantrill DJ (2014) A chloroplast phylogeny of Zieria (Rutaceae) in Australia and New Caledonia shows widespread incongruence with species-level taxonomy. Australian Systematic Botany 27, 427-449.
| Crossref | Google Scholar |
Batty EL, Holmes GD, Murphy DJ, Forster PI, Neal WC, Bayly MJ (2022) Phylogeny, classification and biogeography of Philotheca sect. Erionema (Rutaceae) based on nrDNA sequences. Australian Systematic Botany 35, 326-338.
| Crossref | Google Scholar |
Bayly MJ (2001) A cladistic and biogeographic analysis of Philotheca (Rutaceae) and allied genera. PhD thesis, The University of Melbourne, Melbourne, Vic., Australia. Available at http://hdl.handle.net/11343/37369
Bayly MJ, Holmes GD, Forster PI, Cantrill DJ, Ladiges PY (2013) Major clades of Australasian Rutoideae (Rutaceae) based on rbcL and atpB sequences. PLoS One 8, e72493.
| Crossref | Google Scholar |
Bayly MJ, Holmes GD, Forster PI, Munzinger J, Cantrill DJ, Ladiges PY (2016) Phylogeny, classification and biogeography of Halfordia (Rutaceae) in Australia and New Caledonia. Plant Systematics and Evolution 302, 1457-1470.
| Crossref | Google Scholar |
Broadhurst LM, Tan BH (2001) Floral biology of the Western Australian endemic ‘yellow bells’, Geleznowia verrucosa Turcz (Rutaceae). Journal of the Royal Society of Western Australia 84, 83-89.
| Google Scholar |
Buckler ES, Holtsford TP (1996) Zea systematics: ribosomal ITS evidence. Molecular Biology and Evolution 13, 612-622.
| Crossref | Google Scholar |
Clowes C, Fowler RM, Fahey PS, Kellermann J, Brown GK, Bayly MJ (2022) Big trees of small baskets: phylogeny of the Australian genus Spyridium (Rhamnaceae: Pomaderreae), focusing on biogeographic patterns and species circumscriptions. Australian Systematic Botany 35, 95-119.
| Crossref | Google Scholar |
Crisp MD, Cook LG (2007) A congruent molecular signature of vicariance across multiple plant lineages. Molecular Phylogenetics and Evolution 43, 1106-1117.
| Crossref | Google Scholar |
da Silva MFGF, Gottlieb OR, Ehrendorfer F (1988) Chemosystematics of the Rutaceae: suggestions for a more natural taxonomy and evolutionary interpretation of the family. Plant Systematics and Evolution 161, 97-134.
| Crossref | Google Scholar |
Doyle JJ (1997) Trees within trees: genes and species, molecules and morphology. Systematic Biology 46, 537-553.
| Crossref | Google Scholar |
Doyle JJ (2021) Defining coalescent genes: theory meets practice in organelle phylogenomics. Systematic Biology 71, 476-489.
| Crossref | Google Scholar |
Duchêne DA, Bragg JG, Duchêne S, Neaves LE, Potter S, Moritz C, Johnson RN, Ho SYW, Eldridge MDB (2018) Analysis of phylogenomic tree space resolves relationships among marsupial families. Systematic Biology 67, 400-412.
| Crossref | Google Scholar |
Duretto MF, Heslewood MM, Bayly MJ (2020) Boronia (Rutaceae) is polyphyletic: reinstating Cyanothamnus and the problems associated with inappropriately defined outgroups. Taxon 69, 481-499.
| Crossref | Google Scholar |
Duretto MF, Heslewood MM, Bayly MJ (2023) Generic and infrageneric limits of Phebalium and its allies (Rutaceae: Zanthoxyloideae). Australian Systematic Botany 36, 107-142.
| Crossref | Google Scholar |
Edwards SV (2009) Is a new and general theory of molecular systematics emerging. Evolution 63, 1-19.
| Crossref | Google Scholar |
Foster CSP, Henwood MJ, Ho SYW (2018) Plastome sequences and exploration of tree-space help to resolve the phylogeny of riceflowers (Thymelaeaceae: Pimelea). Molecular Phylogenetics and Evolution 127, 156-167.
| Crossref | Google Scholar |
French PA, Brown GK, Bayly MJ (2016) Incongruent patterns of nuclear and chloroplast variation in Correa (Rutaceae): introgression and biogeography in south-eastern Australia. Plant Systematics and Evolution 302, 447-468.
| Crossref | Google Scholar |
Gonçalves DJP, Simpson BB, Ortiz EM, Shimizu GH, Jansen RK (2019) Incongruence between gene trees and species trees and phylogenetic signal variation in plastid genes. Molecular Phylogenetics and Evolution 138, 219-232.
| Crossref | Google Scholar |
Gonçalves DJP, Jansen RK, Ruhlman TA, Mandel JR (2020) Under the rug: abandoning persistent misconceptions that obfuscate organelle evolution. Molecular Phylogenetics and Evolution 151, 106903.
| Crossref | Google Scholar |
Grandcolas P (2017) Ten false ideas about New Caledonia biogeography. Cladistics 33, 481-487.
| Crossref | Google Scholar |
Groppo M, Pirani JR, Salatino MLF, Blanco SR, Kallunki JA (2008) Phylogeny of Rutaceae based on two noncoding regions from cpDNA. American Journal of Botany 95, 985-1005.
| Crossref | 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.
| Crossref | Google Scholar |
Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307-321.
| Crossref | Google Scholar |
Hammer TA, Zhong X, Colas des Francs‐Small C, Nevill PG, Small ID, Thiele KR (2019) Resolving intergeneric relationships in the aervoid clade and the backbone of Ptilotus (Amaranthaceae): evidence from whole plastid genomes and morphology. Taxon 68, 297-314.
| Crossref | Google Scholar |
Hartley TG (1995) A new combination in Boronella (Rutaceae) and a view on relationships of the genus. Adansonia 17, 107-111.
| Google Scholar |
Hartley TG (2001) Morphology and biogeography in Australasian–Malesian Rutaceae. Malayan Nature Journal 55, 197-220.
| Google Scholar |
Hartley TG (2003) Neoschmidia, a new genus of Rutaceae from New Caledonia. Adansonia 25, 7-12.
| Google Scholar |
Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35, 518-522.
| Crossref | Google Scholar |
Hou N, Wang G, Feng SJ, Wei AZ (2018) The complete chloroplast genome of an aromatic Chinese pepper (Zanthoxylum simulans). Mitochondrial DNA Part B 3, 26-27.
| Crossref | Google Scholar |
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23, 254-267.
| Crossref | Google Scholar |
Jin J-J, Yu W-B, Yang J-B, Song Y, DePamphilis CW, Yi T-S, Li D-Z (2020) GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biology 21, 241.
| Crossref | Google Scholar |
Johnson MG, Pokorny L, Dodsworth S, Botigué LR, Cowan RS, Devault A, Eiserhardt WL, Epitawalage N, Forest F, Kim JT, Leebens-Mack JH, Leitch IJ, Maurin O, Soltis DE, Soltis PS, Wong GK, Baker WJ, Wickett NJ (2019) A universal probe set for targeted sequencing of 353 nuclear genes from any flowering plant designed using k-medoids clustering. Systematic Biology 68, 594-606.
| Crossref | Google Scholar |
Jombart T, Kendall M, Almagro-Garcia J, Colijn C (2017) treespace: statistical exploration of landscapes of phylogenetic trees. Molecular Ecology Resources 17, 1385-1392.
| Crossref | Google Scholar |
Joyce EM, Appelhans MS, Buerki S, et al. (2023) Phylogenomic analyses of Sapindales support new family relationships, rapid Mid-Cretaceous Hothouse diversification, and heterogeneous histories of gene duplication. Frontiers in Plant Science 14, 1063174.
| Crossref | Google Scholar |
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587-589.
| Crossref | Google Scholar |
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772-780.
| Crossref | Google Scholar |
Katoh K, Misawa K, Kuma K-i, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059-3066.
| Crossref | Google Scholar |
Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. Journal of Molecular Evolution 29, 170-179.
| Crossref | Google Scholar |
Kishino H, Miyata T, Hasegawa M (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. Journal of Molecular Evolution 31, 151-160.
| Crossref | Google Scholar |
Ladiges PY, Cantrill D (2007) New Caledonia-Australian connections: biogeographic patterns and geology. Australian Systematic Botany 20, 383-389.
| Crossref | Google 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.
| Crossref | Google Scholar |
Lin GN, Zhang C, Xu D (2011) Polytomy identification in microbial phylogenetic reconstruction. BMC Systems Biology 5, S2.
| Crossref | Google Scholar |
Minh BQ, Hahn MW, Lanfear R (2020a) New methods to calculate concordance factors for phylogenomic datasets. Molecular Biology and Evolution 37, 2727-2733.
| Crossref | Google Scholar |
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R (2020b) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37, 1530-1534.
| Crossref | Google Scholar |
Mole BJ, Udovicic F, Ladiges PY, Duretto MF (2004) Molecular phylogeny of Phebalium (Rutaceae: Boronieae) and related genera based on the nrDNA regions ITS 1 + 2. Plant Systematics and Evolution 249, 197-212.
| Crossref | Google Scholar |
Mueller F (1869) ‘Fragmenta phytographiæ Australiæ. Vol. 7.’ (Auctoritate Guberni Coloniæ Victoriæ, Ex Officina Joannis Ferres: Melbourne, Australia) Available at https://www.biodiversitylibrary.org/item/7224
Nattier R, Pellens R, Robillard T, Jourdan H, Legendre F, Caesar M, Nel A, Grandcolas P (2017) Updating the phylogenetic dating of New Caledonian biodiversity with a meta-analysis of the available evidence. Scientific Reports 7, 3705.
| Crossref | Google Scholar |
Neal WC, James EA, Bayly MJ (2019) Phylogeography, classification and conservation of pink zieria (Zieria veronicea; Rutaceae): influence of changes in climate, geology and sea level in south-eastern Australia. Plant Systematics and Evolution 305, 503-520.
| Crossref | Google Scholar |
Nge FJ, Biffin E, Thiele KR, Waycott M (2020) Extinction pulse at Eocene–Oligocene boundary drives diversification dynamics of two Australian temperate floras. Proceedings of the Royal Society of London – B. Biological Sciences 287, 20192546.
| Crossref | Google Scholar |
Othman RNA, Jordan GJ, Worth JRP, Steane DA, Duretto MF (2010) Phylogeny and infrageneric classification of Correa Andrews (Rutaceae) on the basis of nuclear and chloroplast DNA. Plant Systematics and Evolution 288, 127-138.
| Crossref | Google Scholar |
Palumbi SR, Cipriano F, Hare MP (2001) Predicting nuclear gene coalescence from mitochondrial data: the three-times rule. Evolution 55, 859-868.
| Crossref | Google Scholar |
Penny D, Hendy MD (1985) The use of tree comparison metrics. Systematic Zoology 34, 75-82.
| Crossref | Google Scholar |
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901-904.
| Crossref | Google Scholar |
Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3, 217-223.
| Crossref | Google Scholar |
Rieseberg LH, Soltis DE (1991) Phylogenetic consequences of cytoplasmic gene flow in plants. Evolutionary Trends in Plants 5, 65-84.
| Google Scholar |
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539-542.
| Crossref | Google Scholar |
Sang T, Crawford DJ, Stuessy TF (1997) Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). American Journal of Botany 84, 1120-1136.
| Crossref | Google Scholar |
Sayyari E, Mirarab S (2018) Testing for polytomies in phylogenetic species trees using quartet frequencies. Genes 9, 132.
| Crossref | Google Scholar |
Schuster TM, Setaro SD, Tibbits JFG, Batty EL, Fowler RM, McLay TGB, Wilcox S, Ades PK, Bayly MJ (2018) Chloroplast variation is incongruent with classification of the Australian bloodwood eucalypts (genus Corymbia, family Myrtaceae). PLoS One 13, e0195034.
| Crossref | Google Scholar |
Shepherd LD, McLay TGB (2011) Two micro-scale protocols for the isolation of DNA from polysaccharide-rich plant tissue. Journal of Plant Research 124, 311-314.
| Crossref | Google Scholar |
Shimodaira H (2002) An approximately unbiased test of phylogenetic tree selection. Systematic Biology 51, 492-508.
| Crossref | Google Scholar |
Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16, 1114-1116.
| Crossref | Google Scholar |
Slowinski JB (2001) Molecular Polytomies. Molecular Phylogenetics and Evolution 19, 114-120.
| Crossref | Google Scholar |
Smith MR (2022) Robust Analysis of Phylogenetic Tree Space. Systematic Biology 71, 1255-1270.
| Crossref | Google Scholar |
Smith-White S (1954) Chromosome numbers in the Boronieae (Rutaceae) and their bearing on the evolutionary development of the tribe in the Australian flora. Australian Journal of Botany 2, 287-303.
| Crossref | Google Scholar |
Stace HM, Armstrong JA (1992) New chromosome numbers for Rutaceae. Australian Systematic Botany 5, 501-505.
| Crossref | Google Scholar |
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312-1313.
| Crossref | Google Scholar |
Strimmer K, Rambaut A (2002) Inferring confidence sets of possibly misspecified gene trees. Proceedings of the Royal Society of London – B. Biological Sciences 269, 137-142.
| Crossref | Google Scholar |
Strimmer K, von Haeseler A (1997) Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proceedings of the National Academy of Sciences 94, 6815-6819.
| Crossref | Google Scholar |
Tate JA, Simpson BB (2003) Paraphyly of Tarasa (Malvaceae) and diverse origins of the polyploid species. Systematic Botany 28, 723-737.
| Crossref | Google Scholar |
Telford IRH, Bruhl JJ (2020) Morphological data indicate the subspecies of Leionema elatius (Rutaceae) are not conspecific. Telopea 23, 197-203.
| Crossref | Google Scholar |
Tibshirani R, Walther G, Hastie T (2001) Estimating the number of clusters in a data set via the gap statistic. Journal of the Royal Statistical Society – B. Statistical Methodology 63, 411-423.
| Crossref | Google Scholar |
Tillich M, Lehwark P, Pellizzer T, Ulbricht-Jones ES, Fischer A, Bock R, Greiner S (2017) GeSeq – versatile and accurate annotation of organelle genomes. Nucleic Acids Research 45, W6-W11.
| Crossref | Google Scholar |
Toews DPL, Brelsford A (2012) The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology 21, 3907-3930.
| Crossref | Google Scholar |
Tsitrone A, Kirkpatrick M, Levin DA (2003) A model for chloroplast capture. Evolution 57, 1776-1782.
| Crossref | Google Scholar |
Whitfield JB, Lockhart PJ (2007) Deciphering ancient rapid radiations. Trends in Ecology & Evolution 22, 258-265.
| Crossref | Google Scholar |
Williams AV, Miller JT, Small I, Nevill PG, Boykin LM (2016) Integration of complete chloroplast genome sequences with small amplicon datasets improves phylogenetic resolution in Acacia. Molecular Phylogenetics and Evolution 96, 1-8.
| Crossref | Google Scholar |
Wilson PG (1970) A taxonomic revision of the genera Crowea, Eriostemon and Phebalium (Rutaceae). Nuytsia 1, 3-155.
| Crossref | Google Scholar |
Wilson PG (1971) Taxonomic notes on the family Rutaceae, principally of Western Australia. Nuytsia 1, 197-207.
| Crossref | Google Scholar |
Wilson PG (1998a) A taxonomic review of the genera Eriostemon and Philotheca (Rutaceae: Boronieae). Nuytsia 12, 239-265.
| Google Scholar |
Wilson PG (1998b) New species and nomenclatural changes in Phebalium and related genera (Rutaceae). Nuytsia 12, 267-288.
| Google Scholar |
Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proceedings of the National Academy of Sciences 84, 9054-9058.
| Crossref | Google Scholar |
Zeng L, Zhang Q, Sun R, Kong H, Zhang N, Ma H (2014) Resolution of deep angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times. Nature Communications 5, 4956.
| Crossref | Google Scholar |
Zhang C, Rabiee M, Sayyari E, Mirarab S (2018) ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics 19, 153.
| Crossref | Google Scholar |
