Comparative morphology and phylogeny of Nicotiana section Suaveolentes (Solanaceae) in Australia and the South Pacific
Claire E. Marks A , Ed Newbigin A and Pauline Y. Ladiges A B
+ Author Affiliations
- Author Affiliations
A School of Botany, The University of Melbourne, Vic. 3010, Australia.
B Corresponding author. Email: paulinel@unimelb.edu.au
Australian Systematic Botany 24(2) 61-86 https://doi.org/10.1071/SB11006
Submitted: 1 February 2011 Accepted: 25 May 2011 Published: 29 July 2011
Abstract
Molecular phylogenies alone have failed to resolve evolutionary relationships of Nicotiana L. section Suaveolentes Goodsp. (Solanaceae), a section largely comprising Australian endemics. Comparative morphology of Suaveolentes is illustrated and characters, together with the chromosome number, coded for phylogenetic analysis. Morphological characters included discrete characters of seeds and trichomes studied by scanning electron and light microscopy, and gap-coded quantitative measurements of flowers and vegetative organs. These data were analysed using both maximum parsimony and splits network, and compared to and combined with molecular analyses based on published nuclear and chloroplast-DNA sequences. Among morphological characters, there was a high level of homoplasy, possibly attributable to convergent evolution, hybridisation and introgression, and the underlying polyploid origin of the group. There was some conflict between the morphological and molecular datasets; however, overall there was a level of concordance that identified a phylogenetic sequence of taxa that reflected a reduction in the chromosome number. With N. africana as the functional outgroup, analyses showed N. fragrans (New Caledonia and Tongatapu) and N. fatuhivensis (Marquesas islands, formerly N. fragrans var. fatuhivensis) to be a basal lineage in the Australian and South Pacific clade of Suaveolentes. N. forsteri (eastern mainland Australia, Lord Howe Island and New Caledonia) is the sister taxon to all other Australian species of Suaveolentes, which form a well supported monophyletic group. Within this Australian endemic group, species with a chromosome count of n = 24 or 23 are early lineages. Two clades with a reduced chromosome number are the ‘N. simulans clade’ (all taxa with n = 20) and the ‘N. suaveolens clade’ (n = 19, 18, 16, or 15). The position of N. cavicola (n = 20 or 23) is equivocal, and it and several other species require further study. Some widespread taxa require greater sampling of populations to test for variation in morphology, DNA sequences and chromosome number for further elucidation of the evolutionary history of Suaveolentes.
References
Aoki S, Ito M (2000) Molecular phylogeny of Nicotiana (Solanaceae) based on the nucleotide sequence of the matK gene. Plant Biology 2, 316–324.| Molecular phylogeny of Nicotiana (Solanaceae) based on the nucleotide sequence of the matK gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksFSktLo%3D&md5=0fd5c7bef36b658832f6cfbb84581665CAS |
Bahadur B, Farooqui SM (1986) Seed and seed coat characters in Australian Nicotiana. In ‘Solanaceae, biology and systematics’. (Ed. WG D’Arcy). pp. 114–137. (Columbia University Press: New York)
Bryant D, Moulton V (2004) Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Molecular Biology and Evolution 21, 255–265.
| Neighbor-net: an agglomerative method for the construction of phylogenetic networks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisFWmurs%3D&md5=dd0813df566e040213a036783afc353cCAS |
Burbidge NT (1960) The Australian species of Nicotiana L. (Solanaceae). Australian Journal of Botany 8, 342–378.
| The Australian species of Nicotiana L. (Solanaceae).Crossref | GoogleScholarGoogle Scholar |
Chase MW, Knapp S, Cox AV, Clarkson JJ, Butsko Y, Joseph J, Savolainen V, Parokenny AS (2003) Molecular systematics, GISH and the origin of hybrid taxa in Nicotiana (Solanaceae). Annals of Botany 92, 107–127.
| Molecular systematics, GISH and the origin of hybrid taxa in Nicotiana (Solanaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtVKqtL0%3D&md5=5242ec0f26cffab26e570447d2af4d4bCAS |
Clarkson JR, Symon DE (1991) Nicotiana wuttkei (Solanaceae): a new species from north-east Queensland with an unusual chromosome number. Austrobaileya 3, 389–392.
Clarkson JJ, Knapp S, Garcia VF, Olmstead RG, Leitch AR, Chase MW (2004) Phylogenetic relationships in Nicotiana (Solanaceae) inferred from multiple plastid DNA regions. Molecular Phylogenetics and Evolution 33, 75–90.
| Phylogenetic relationships in Nicotiana (Solanaceae) inferred from multiple plastid DNA regions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvFCrsb8%3D&md5=e3a77fa5ce985a363437c78e97e566d0CAS |
Clarkson JJ, Kelly LJ, Leitch AR, Knapp S, Chase MW (2010) Nuclear glutamine synthetase evolution in Nicotiana: phylogenetics and the origins of allotetraploid and homoploid (diploid) hybrids. Molecular Phylogenetics and Evolution 55, 99–112.
| Nuclear glutamine synthetase evolution in Nicotiana: phylogenetics and the origins of allotetraploid and homoploid (diploid) hybrids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXit1Gnt7k%3D&md5=1a99145634a7cded4e934c07ba40e45cCAS |
Corner EJH (1976) ‘The seeds of dicotyledons.’ (Cambridge University Press: Cambridge, UK)
Edmonds JM (1982) Epidermal hair morphology in Solanum L. section Solanum. Botanical Journal of the Linnean Society 85, 153–167.
Edmonds JM (1983) Seed coat structure and development in Solanum (Solanaceae). Botanical Journal of the Linnean Society 87, 229–246.
| Seed coat structure and development in Solanum (Solanaceae).Crossref | GoogleScholarGoogle Scholar |
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
| Confidence limits on phylogenies: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar |
Garcia VF, Olmstead RG (2003) Phylogenetics of the tribe Anthocercideae (Solanaceae) based on ndhF and trnL/F sequence data. Systematic Botany 28, 609–615.
Garcia-Cruz J, Sosa V (2006) Coding quantitative character data for phylogenetic analysis: a comparison of five methods. Systematic Botany 31, 302–309.
| Coding quantitative character data for phylogenetic analysis: a comparison of five methods.Crossref | GoogleScholarGoogle Scholar |
Gemeinholzer B, Wink M (2001) Solanaceae: occurrence of secondary compounds versus molecular phylogeny. In ‘Solanaceae V: advances in taxonomy and utilization’. (Eds RG van den Berg, GWM Barendse, GM van der Weerden, C Mariani) pp. 165–178. (Nijmegen University Press: Nijmegen, The Netherlands)
Goloboff PA, Mattoni CI, Quinteros AS (2006) Continuous characters analyzed as such. Cladistics 22, 589–601.
| Continuous characters analyzed as such.Crossref | GoogleScholarGoogle Scholar |
Goodspeed TH (1945) Studies in Nicotiana III. A taxonomic organization of the genus. University of California Publications in Botany 18, 335–343.
Goodspeed TH (1954) ‘The genus Nicotiana: origins, relationships and evolution of its species in the light of their distribution, morphology and cytokinetics.’ (Chronica Botanica Company: Waltham, MA)
Gunn CR, Gaffney FB (1974) Seed characteristics of 42 economically important species of Solanaceae in the United States. United States Department of Agriculture Technical Bulletin 1471, 1–32.
Haegi L (1991) Trichomes of Solanaceae tribe Anthocercidae. In ‘Solanaceae III: taxonomy, chemistry, evolution’. (Eds JG Hawkes, RN Lester, M Nee, N Estrada) pp. 181–195. (Royal Botanic Gardens Kew and Linnean Society of London: London)
Hamming RW (1950) Error detecting and error correcting codes. The Bell System Technical Journal 26, 147–160.
Harris JG, Harris MW (2001) ‘Plant identification terminology: an illustrated glossary.’ (Spring Lake Publishing: Spring Lake, UT)
Horton P (1981) A taxonomic revision of Nicotiana (Solanaceae) in Australia. Journal of the Adelaide Botanic Gardens 3, 1–56.
Huson DH (1998) SplitsTree: analysing and visualizing evolutionary data. Bioinformatics 14, 68–73.
| SplitsTree: analysing and visualizing evolutionary data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisFygs70%3D&md5=9ba79031383b1e7ef5b7c4b425bd66ecCAS |
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23, 254–267.
| Application of phylogenetic networks in evolutionary studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntValsw%3D%3D&md5=9273bd0ef9f8697d1661c22911814306CAS |
James SH (1981) Cytoevolutionary patterns, genetic systems and the phytogeography of Australia. In ‘Ecological biogeography of Australia’. (Ed. A Keast) pp. 761–782. (W. Junk: The Hague, The Netherlands)
Kelly LJ, Leitch AR, Clarkson JJ, Hunter RB, Knapp S, Chase MW (2010) Intragenic recombination events and evidence for hybrid speciation in Nicotiana (Solanaceae). Molecular Biology and Evolution 27, 781–799.
| Intragenic recombination events and evidence for hybrid speciation in Nicotiana (Solanaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjslaltbo%3D&md5=4f432741935e5d57bfb351dae5ec425aCAS |
Kitching IJ, Forey PL, Humphries CJ, Williams DM (1998) ‘Cladistics: the theory and practice of parsimony analysis.’ (Oxford University Press: Oxford, UK)
Knapp S (2001) Is morphology dead in Solanum taxonomy? In ‘Solanaceae V: advances in taxonomy and utilization’. (Eds RG van den Berg, GWM Barendse, GM van der Weerden, C Mariani) (Nijmegen University Press: Nijmegen, The Netherlands)
Knapp S (2002) Tobacco to tomatoes: a phylogenetic perspective on fruit diversity in the Solanaceae. Journal of Experimental Botany 53, 2001–2022.
| Tobacco to tomatoes: a phylogenetic perspective on fruit diversity in the Solanaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVGks7o%3D&md5=2af34ec82b7e84052e8f2c15720eb4d0CAS |
Knapp S (2010) On ‘various contrivances’: pollination, phylogeny and flower form in the Solanaceae. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365, 449–460.
| On ‘various contrivances’: pollination, phylogeny and flower form in the Solanaceae.Crossref | GoogleScholarGoogle Scholar |
Knapp S, Chase MW, Clarkson JJ (2004) Nomenclatural changes and a new sectional classification in Nicotiana (Solanaceae). Taxon 53, 73–82.
| Nomenclatural changes and a new sectional classification in Nicotiana (Solanaceae).Crossref | GoogleScholarGoogle Scholar |
Kovarik A, Dadejova M, Lim KY, Chase MW, Clarkson JJ, Knapp S, Leitch AR (2008) Evolution of rDNA in Nicotiana allopolyploids: a potential link between rDNA homogenization and epigenetics. Annals of Botany 101, 815–823.
| Evolution of rDNA in Nicotiana allopolyploids: a potential link between rDNA homogenization and epigenetics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntVait7s%3D&md5=bda5c820af590232478f506ab6ea3619CAS |
Ladiges PY, Marks CE, Nelson G (2011) Biogeography of Nicotiana section Suaveolentes (Solanaceae) reveals geographic tracks in arid Australia. Journal of Biogeography 38,
| Biogeography of Nicotiana section Suaveolentes (Solanaceae) reveals geographic tracks in arid Australia.Crossref | GoogleScholarGoogle Scholar |
Laskowska D, Berbec A (2003) Preliminary study of the newly discovered tobacco species Nicotiana wuttkei Clarkson et Symon. Genetic Resources and Crop Evolution 50, 835–839.
| Preliminary study of the newly discovered tobacco species Nicotiana wuttkei Clarkson et Symon.Crossref | GoogleScholarGoogle Scholar |
Leitch IJ, Hanson L, Lim KY, Kovarik A, Chase MW, Clarkson JJ, Leitch AR (2008) The ups and downs of genome size evolution in polyploid species of Nicotiana (Solanaceae). Annals of Botany 101, 805–814.
| The ups and downs of genome size evolution in polyploid species of Nicotiana (Solanaceae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c3kvVKisg%3D%3D&md5=b358db367e8deaaa6a2c9e9da18256c7CAS |
Lester RN (1991) Evolutionary relationships of tomato, potato, pepino and wild species of Lycopersicon and Solanum. In ‘Solanaceae III: taxonomy, chemistry, evolution’. (Eds JG Hawkes, RN Lester, M Nee, N Estrada) pp. 283–301. (Royal Botanic Gardens Kew & Linnean Society of London: London)
Lockhart PJ, Cameron SA (2001) Trees for bees. Trends in Ecology & Evolution 16, 84–88.
| Trees for bees.Crossref | GoogleScholarGoogle Scholar |
Marks CE (2010a) Definition of South Pacific taxa of Nicotiana section Suaveolentes. Muelleria 28, 74–84.
Marks CE (2010b) The evolution of Nicotiana section Suaveolentes. PhD Thesis, The University of Melbourne.
Martins TR, Barkman TJ (2005) Reconstruction of Solanaceae phylogeny using the nuclear gene SAMT. Systematic Botany 30, 435–447.
| Reconstruction of Solanaceae phylogeny using the nuclear gene SAMT.Crossref | GoogleScholarGoogle Scholar |
Merxmüller H, Buttler KP (1975) Nicotiana in der Afrikanischen Namib – ein Planzengeographisches und phylogenetisches Ratsel. Mitteilungen (aus) der Botanischen Staatssammlung München 12, 91–104.
National Centre for Biotechnology Information (2010) ‘Genbank.’ (National Centre for Biotechnology Information, NCBI). Available at http://www.ncbi.nlm.nih.gov/nucleotide/ [accessed 1 March 2010].
Olmstead RG, Palmer JD (1992) A chloroplast DNA phylogeny of the Solanaceae: subfamilial relationships and character evolution. Annals of the Missouri Botanical Garden 79, 346–360.
| A chloroplast DNA phylogeny of the Solanaceae: subfamilial relationships and character evolution.Crossref | GoogleScholarGoogle Scholar |
Olmstead RG, Sweere JA (1994) Combining data in phylogenetic systematics: an empirical approach using three molecular data sets in the Solanaceae. Systematic Biology 43, 467–481.
| Combining data in phylogenetic systematics: an empirical approach using three molecular data sets in the Solanaceae.Crossref | GoogleScholarGoogle Scholar |
Olmstead RG, Sweere JA, Spangler RE, Bohs L, Palmer JD (1999) Phylogeny and provisional classification of the Solanaceae based on chloroplast DNA. In ‘Solanaceae IV’. (Eds M Nee, DE Symon, RN Lester and JP Jessop) pp. 111–137. (Royal Botanic Gardens, Kew: London)
Olmstead RG, Bohs L, Migid HA, Santiago-Valentin E, Garcia VF, Collier SM (2008) A molecular phylogeny of the Solanaceae. Taxon 57, 1159–1181.
Perrie LR, Lockhart PJ, Brownsey PJ, Large MF (2000) Morphological and molecular concordance for the recognition of two species in the New Zealand Polystichum richardii (Hook.) J.Smith complex. Plant Systematics and Evolution 224, 97–107.
| Morphological and molecular concordance for the recognition of two species in the New Zealand Polystichum richardii (Hook.) J.Smith complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosFyht7g%3D&md5=a3dfb80890dc27c93b06ded53f10c63fCAS |
Purdie RW, Symon DE, Haegi L (1982) Solanaceae. In ‘Flora of Australia’. (Australian Government Publishing Service: Canberra)
Rambaut A (2002) ‘Se-Al v2.0a11.’ (University of Oxford: Oxford, UK)
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstruction of phylogenetic trees. Molecular Biology and Evolution 4, 406–425.
Seithe A (1979) Hair types as taxonomic characters in Solanum. In ‘The biology and taxonomy of the Solanaceae’. (Eds JG Hawkes, RN Lester, AD Skelding) pp. 307–319. (Academic Press: London)
Shan F, Yan G, Plummer JA (2006) Basic chromosome number in Boronia (Rutaceae) – competing hypotheses examined. Australian Journal of Botany 54, 681–689.
| Basic chromosome number in Boronia (Rutaceae) – competing hypotheses examined.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVyqt77F&md5=5ece75c0b146b703697fe43b7d0b0857CAS |
Smith VS, Page RDM, Johnson KP (2004) Data incongruence and the problem of avian louse phylogeny. Zoologica Scripta 33, 239–259.
| Data incongruence and the problem of avian louse phylogeny.Crossref | GoogleScholarGoogle Scholar |
Stace HM, James SH (1996) Another perspective on cytoevolution in Lobelioideae (Campanulaceae). American Journal of Botany 83, 1356–1364.
| Another perspective on cytoevolution in Lobelioideae (Campanulaceae).Crossref | GoogleScholarGoogle Scholar |
Swofford DL (2003) ‘PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4.’ (Sinauer Associates: Sunderland, MA)
Symon DE (1984) A new species of Nicotiana (Solanaceae) from Dalhousie Springs, South Australia. Journal of the Adelaide Botanic Gardens 7, 117–121.
Symon DE (1991) Gondwanan elements of the Solanaceae. In ‘Solanaceae III: taxonomy, chemistry, evolution’. (Eds JG Hawkes, RN Lester, M Nee, N Estrada) pp. 139–150. (Royal Botanic Gardens Kew & Linnean Society of London: London)
Symon DE (1998) A new Nicotiana (Solanceae) from near Coober Pedy, South Australia. Journal of the Adelaide Botanic Gardens 18, 1–4.
Symon DE (2004) Nicotiana in Australia. Australian Biologist 17, 63–68.
Symon DE, Kenneally KF (1994) A new species of Nicotiana (Solanaceae) from near Broome, Western Australia. Nuytsia 9, 421–425.
Tepe EJ, Bohs L (2010) A molecular phylogeny of Solanum sect. Pteroidea (Solanaceae) and utility of COSII markers in resolving relationships among closely related species. Taxon 59, 733–743.
Thiele K (1993) The Holy Grail of the perfect character: the cladistic treatment of morphometric data. Cladistics 9, 275–304.
| The Holy Grail of the perfect character: the cladistic treatment of morphometric data.Crossref | GoogleScholarGoogle Scholar |
von Minden MD (1899) Beiträge zur anatomischen und physiologischen Kenntnis Wasser-secernierender Organe. Bibliotheca Botanica 9, 1–76.
Wheeler HM (1945) A contribution to the cytology of the Australia–South Pacific species of Nicotiana. Proceedings of the National Academy of Sciences, USA 31, 177–185.
| A contribution to the cytology of the Australia–South Pacific species of Nicotiana.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zhvFKitg%3D%3D&md5=8f9479f967f49229b7e55a8b9982adb4CAS |
Williams E (1975) A new chromosome number in the Australian species Nicotiana cavicola L. (Burbidge). New Zealand Journal of Botany 13, 811–812.
Wollscheid E, Wägele H (1999) Initial results on the molecular phylogeny of the Nudibranchia (Gastropoda, Opisthobranchia) based on 18S rDNA data. Molecular Phylogenetics and Evolution 13, 215–226.
| Initial results on the molecular phylogeny of the Nudibranchia (Gastropoda, Opisthobranchia) based on 18S rDNA data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotFOhuro%3D&md5=b6cbdbe1b1810121d78cf0374700ec29CAS |
Zhang Z-Y, Yang D-Z, Lu A-M, Knapp S (2005) Seed morphology of the tribe Hyoscyameae (Solanaceae). Taxon 54, 71–83.
| Seed morphology of the tribe Hyoscyameae (Solanaceae).Crossref | GoogleScholarGoogle Scholar |
