Abstract
Kangaroo apples, subgenus Archaesolanum, are a unique and still poorly known group within the genus Solanum. Here we aimed to reveal phylogeny, historical biogeography and age of diversification of Archaesolanum. We sampled all recognized species of the group and sequenced three chloroplast regions, the trnT-trnL spacer, trnL intron and trnL-trnF spacer to calibrate a molecular clock to estimate the age of the group. Distributional data were combined with the results of phylogenetic analysis to track the historical processes responsible for the current range of the group. Our analysis supported the monophyly of the kangaroo apples and the biogeographical disjunction between the two subclades within the group. Based on the divergence time estimates the most recent common ancestor of kangaroo apples is from the late Miocene age (~9 MYA). Based on the age estimate the common ancestors of the kangaroo apples are presumed to have arrived in Australia by long-distance dispersal. The two distinct lineages within the group have separated during the aridification of the continent and further speciated in the brief resurgence of rainforests during the Pliocene.
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Notes
Basionym of Solanum section Archaesolanum (Bitter ex Marzell) Danert.
S. brisbanense Geras. is now recognized as synonym of S. aviculare; while S. cheesmanii Geras. refers to the white flowered (var. albiflorum) variety and S. baylisii Geras. to the broad leaf (var. latifolium) mutant of S. aviculare.
References
Randell BR, Symon DE (1976) Chromosome numbers in Australian Solanum species. Aust J Bot 24:369–379
Bohs L, Olmstead RG (2001) A reassessment of Normania and Triguera (Solanaceae). Plant Syst Evol 228:33–48
Bohs L (2005) Major clades in Solanum based on ndhF sequences. In: Keating RC, Hollowell VC, Croat TB (eds) A festschrift for William G. D’Arcy: the legacy of a taxonomist. Monographs in systematic botany from the Missouri Botanical Garden, vol 104. Missouri Botanical Garden Press, St. Louis, pp 27–49
Weese TL, Bohs L (2007) A three-gene phylogeny of the genus Solanum (Solanaceae). Syst Bot 32:445–463
Poczai P, Taller J, Szabó I (2008) Analysis of phylogenetic relationships in the genus Solanum (Solanaceae) as revealed by RAPD markers. Plant Syst Evol 275:59–67
Forster JGA (1786) Dissertatio inauguralis botanico-medica de plantis esculentis insularum oceani australis. Typis Frankianus, Halle
Lamarck JPAPM de B (1792) Encyclopédie méthodique, Botanique, vol. 3(2). Plomteux, Liége
L’Héritier CL de B (1805) Solanum. In: Persoon CH (ed) Synopsis plantarum, vol 1. CF Cramer, Paris
Mueller F (1855) Account of the gunyang: a new indigenous fruit of Victora. In: Robertson G (ed) Transactions and proceedings of the Victorian Institute for the Advancement of Science. Melbourne, Australia, pp 67–70
Hooker JD (1857) The botany of the Antarctic voyage. III. Flora Tasmaniae. Part 1 (4). Reeve, London
Spooner DM (2009) DNA barcoding will frequently fail in complicated groups: an example in wild potatoes. Am J Bot 96:1177–1189
Baylis GTS (1963) A cytogenetical study of the Solanum aviculare species complex. Aust J Bot 11:168–177
Symon DE (1994) Kangaroo apples: Solanum sect. Archaesolanum. Author, Keswick
Dunal MF (1852) Solanaceae. In: De Candolle AP (ed) Prodromus systematis naturalis regni vegetabilis, vol 13. Treuttel and Würz, Paris
Bitter G (1927) Archaesolanum. In: Hegi G (ed) Illustrierte Flora von Mitter-Europa. Band V. Tiel. 4. JF Lehmann, München
Danert S (1970) Infragenerische Taxa der Gattung Solanum. Kulturpflanzen 18:253–297
D’Arcy WG (1972) Solanaceae studies II: typification of subdivisions of Solanum. Ann Mo Bot Gard 59:262–278
D’Arcy WG (1991) The Solanaceae since 1976, with a review of its biogeography. In: Hawkes JG, Lester RN, Nee M, Estrada-Ramos N (eds) Solanaceae III: taxonomy, chemistry, evolution. Royal Botanic Gardens, Kew, pp 75–137
Nee M (1999) Synopsis of Solanum in the new world. In: Nee M, Symon DE, Lester RN, Jessop JP (eds) Solanaceae IV: advances in biology and utilization. Royal Botanic Gardens, Kew, pp 285–333
Hunziker AT (2001) The genera of Solanaceae. ARG Gantner Verlag, Ruggel
Gerasimenko II (1970) Conspectus subgeneris Archaesolanum Bitt. ex Marz. generis Solanum L. Novosti Sist Vyssh Rast 7:270–275
Jigden B, Wang H, Samadan N, Yang D-C (2010) Molecular identification of oriental medical plant Anemarrhena asphoides Bunge (‘Jimo’) by multiplex PCR. Mol Biol Rep 37:955–960
Borsch T, Hilu KW, Quandt D, Wilde V, Neinhuis C, Barthlott (2003) Noncoding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms. J Evol Biol 16:558–576
Borsch T, Hilu KW, Wiersema JH, Löhne C, Barthlott W, Wilde V (2007) Phylogeny of Nymphaea (Nymphaeaceae): evidence from substitutions and microstructural changes in the chloroplast trnT-trnL region. Int J Plant Sci 168:639–671
Panwar P, Saini RK, Sharma N, Yadav D, Kumar A (2010) Efficiency of RAPD, SSR and cytochrome P450 gene based markers in accessing genetic variability amongst finger millet (Eleusine coracana) accessions. Mol Biol Rep 37:4075–4082
Pamidimarri DVNS, Chattopadhyay B, Reddy MP (2009) Genetic divergence and phylogenetic analysis of genus Jatropha based on nuclear ribosomal DNA ITS sequence. Mol Biol Rep 36:1929–1935
Liu QL, Zhang N, Li L, Liu J (2010) Identification of Elymus (Triticaceae, Poaceae) and its related genera genomes by RFLP analysis of PCR-amplified Adh genes. Mol Biol Rep 37:3249–3257
Ciarmiello LF, Piccirillo P, Pontecorvo G, De Luca A, Kafantaris I, Woodrow P (2010) A PCR based SNPs marker for specific characterization of English walnut (Juglans regia L.) cultivars. Mol Biol Rep. doi:10.1007/s11033-010-0223-y
Wang H, Sun H, Kwon W-S, Jin H, Yang D-C (2010) A PCR-based SNP marker for specific authentication of Korean ginseng (Panax ginseng) cultivar “Chunpoong”. Mol Biol Rep 37:1053–1057
Pamidimarri DVNS, Mastan SG, Rahman H, Reddy MP (2010) Molecular characterization and genetic diversity analysis of Jatropha curcas L. in India using RAPD and AFLP analysis. Mol Biol Rep 37:2249–2257
Grativol C, Lira-Medeiros CDF, Hemerly AS, Ferreira PCG (2010) High efficiency and reliability of inter-simple sequence repeats (ISSR) markers for evaluation of genetic diversity in Brazilian cultivated Jatropha curcas L. accessions. Mol Biol Rep. doi:10.1007/s11033-010-0547-7
Müller K, Borsch T, Hilu KW (2006) Phylogenetic utility of rapidly evolving DNA at high taxonomic levels: contrasting matK, trnT-F, and rbcL in basal angiosperms. Mol Phylogenet Evol 41:99–117
Olmstead RG, Bohs L, Migid HA, Santiago-Valentin E, Garcia VF, Collier SM (2008) A molecular phylogeny of the Solanaceae. Taxon 57:1159–1181
Paape T, Igric B, Smith SD, Olmstead E, Bohs L, Kohn JR (2008) A 15-Myr-old genetic bottleneck. Mol Biol Evol 25:655–663
Poczai P, Hyvönen J (2010) On the origin of Solanum nigrum: can networks help? Mol Biol Rep. doi:10.1007/s11033-010-0215-y
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid Symp Ser 41:95–98
Goloboff PA (1999) NONA, version 2.0. www.cladistics.com. Accessed 16 Aug 2010
Nixon KC (2002) Winclada, version 1.00.08. www.cladistics.com. Accessed 20 July 2010
Nixon KC (1999) The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15:407–414
Farris JS, Albert VA, Källersjö M, Lipscomb D, Kluge AG (1996) Parsimony jackknifing outperforms neighbor-joining. Cladistics 12:99–124
Goloboff PA, Farris JS, Nixon KC (2008) TNT: tree analysis using new technology. Program and documentation available from the authors. http://www.zmuc.dk/public/phylogeny/TNT/. Accessed 21 April 2010
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214
Palmer JD (1991) Plastid chromosome: structure and evolution. In: Bogorad L, Vasil IK (eds) The molecular biology of plastids. Academic Press, San Diego, pp 5–53
Schnabel A, Wendell JF (1998) Cladistic biogeography of Gleditsia (Leguminosae) based on ndhF and rpl16 chloroplast gene sequences. Am J Bot 85:1753–1765
Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:699–710
Crepet WL, Nixon KC, Gandolfo MA (2004) Fossil evidence and phylogeny: the age of major angiosperm clades based on mesofossil and macrofossil evidence from cretaceous deposits. Am J Bot 91:1666–1682
Benton MJ (1993) The fossil record 2. Chapman and Hall, London
Magallón S, Crane PR, Herendeen PS (1999) Phylogenetic pattern, diversity, and diversification of eudicots. Ann Mo Bot Gard 86:297–372
Rambaut A, Drummond AJ (2007) Tracer ver. 1.5 http://tree.bio.ed.ac.uk/software/tracer/. Accessed 10 March 2010
Beiko RG, Keith JM, Harlow TJ, Ragan MA (2006) Searching for convergence in phylogenetic Markov chain Monte Carlo. Syst Biol 55:553–565
Rambaut A (2008) FigTree ver. 1.3.1. http://tree.bio.ed.ac.uk/software/figtree/. Accessed 20 Feb 2010
Parks DH, Porter M, Churcher S, Wang S, Blouin C, Whalley J, Brooks S, Beiko RG (2009) GenGIS: a geospatial information system for genomic data. Genome Res 19:1896–1904
Parks D, Beiko R (2010) GenGIS MapMaker v1.0. http://kiwi.cs.dal.ca/GenGIS/MapMaker. Accessed 20 Dec 2010
Ronquist F (1997) Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Syst Biol 46:195–203
Hausdorf B (1998) Weighted ancestral area analysis and a solution of the redundant distribution problem. Syst Biol 47:445–456
Symon DE (1981) A revision of Solanum in Australia. J Adel Bot Gard 4:1–367
Heiberg E (2008) SEEVA ver. 0.33. Software for spatial evolutionary and ecological vicariance analysis. Available from the author. http://seeva.heiberg.se. Accessed 20 April 2010
Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen–Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644
Heiberg E, Struwe L (2008) SEEVA manual. On-line publication, Rutgers University. http://seeva.heiberg.se and http://www.rci.rutgers.edu/~struwe/seeva. Accessed 20 April 2010
Kluge AG, Farris JS (1969) Quantitative phyletics and the evolution of Anurans. Syst Zool 18:1–32
Farris JS (1989) The retention index and homoplasy excess. Syst Zool 38:406–407
Nixon KC, Carpenter JM (1996) On consensus, collapsibility, and clade concordance. Cladistics 12:305–321
Poczai P, Cseh A, Taller J, Symon DE (2011) Genetic diversity and relationships in Solanum subg. Archaesolanum (Solanaceae) based on RAPD and chloroplast PCR-RFLP analyses. Plant Syst Evol 291:35–47
Symon DE (1985) Solanaceae of New Guinea. J Adel Bot Gard 8:1–171
Gerasimenko II (1969) Inter an intraspecific hybridization in the genus Solanum subgenus Archaesolanum Bitter ex Marzell. Genetika 5:51–60
Gerasimenko II (1971) Interpscific variation in Solanum laciniatum. Ait Rast Resur 7:363–371
Korneva EI, Ostretsova IN, Kondratenko PN (1969) Characteristic biological features of S. laciniatum and its intraspecific hybrids. Rast Resur 5:197–201
Korneva EI, Balakhova OF (1973) Polyploid hybrids of Solanum aviculare var. brisbanense, S. aviculare var. albiflorum in relation to the appearance of S. laciniatum type. Genetika 9:47–53
Knapp S (2006) Solanum aviculare. In: Solanaceae Source, 2010. http://www.nhm.ac.uk/research-curation/projects/solanaceaesource/taxonomy/description-detail.jsp?spnumber=1213. Accessed 12 Nov 2010
McNeill J, Barrie FR, Burdet HM, Demoulin V, Hawksworth DL et al (2006) International code of botanical nomenclature (Vienna code). ARG Ganter Verlag, Ruggell
Knapp S, Bohs L, Nee M, Spooner DM (2004) Solanaceae: a model for linking genomics with biodiversity. Comp Funct Genom 5:285–291
Hawkes JG (1990) The potato: evolution, biodiversity and genetic resources. Smithsonian Institution Press, Whasington
Bohs L, Olmstead RG (1997) Phylogenetic realationships in Solanum (Solanaceae) based on ndhF sequences. Syst Bot 22:5–17
Olmstead RG, Palmer JD (1997) Implications for the phylogeny, classification, and biogeography of Solanum from cpDNA restriction site variation. Syst Bot 22:19–29
Francisco-Ortega J, Hawkes JG, Lester RN, Acebes-Ginovés JR (1993) Normania, an endemic Macarinesian genus distinct from Solanum (Solanaceae). Plant Syst Evol 185:189–205
Scotese CR, Gahagan LM, Larson RL (1988) Plate tectonic reconstructions of the Cretaceous and Cenozoic ocean basins. Tectonophysics 155:27–48
Pigram CJ, Davies HL (1987) Terranes and the accretion history of the New Guinean orogen. BMR J Aust Geol Geophys 10:193–211
Woodburne MO, Case JA (1996) Dispersal, vicariance, and the late cretaceous to early tertiary land mammal biogeography from South America to Australia. J Mammal Evol 3:121–161
Sanmartín I, Ronquist F (2004) Southern hemisphere biogeography inferred by event-based models: plant versus animal patterns. Syst Biol 53:216–243
De Queiroz A (2005) The reconstruction of oceanic dispersal in historical biogeography. Trend Ecol Evol 20:68–73
Pulquério MJF, Nichols RA (2007) Dates from the molecular clock: how wrong can we be? Trend Ecol Evol 22:180–184
Wikström N, Savolainen V, Chase MW (2001) Evolution of the angiosperms: calibrating the family tree. P Roy Soc B Biol Sci 268:2211–2220
Carlquist S (1967) The biota of long-distance dispersal. V. Plant dispersal to the Pacific Islands. B Torrey Bot Club 94:129–162
Mummenhoff K, Franzke A (2007) Gone with the bird: late Tertiary and Quaternary intercontinental long-distance dispersal and allopolyploidization in plants. Syst Biodivers 5:255–260
Winkworth RC, Wagstaff SJ, Glenny D, Lockhart PJ (2002) Plant dispersal N.E.W.S. from New Zealand. Trend Ecol Evol 17:514–520
Proctor VW (1968) Long-distance dispersal of seeds by retention in digestive tract of birds. Science 160:321–322
Keighery G (1984) Solanum berries and wattlebirds. West Aust Nat 16:22
Willson MF, Graff DA, Whelan CJ (1990) Color preferences of frugivorous birds in relation to the colors of fleshy fruits. Condor 92:545–555
Janson CH (1983) Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science 219:187–189
Willson MF, Irvine AK, Walsh NG (1989) Vertebrate dispersal syndromes in some Australian and New Zealand plant communities, with geographic comparisons. Biotropica 21:133–147
Bell DT, Moredoundt JC, Longeragan WA (1987) Grazing pressure by tamer (Macropus eugenii Desm.) on the vegetation of Garden Island, W. Aust. J Roy Soc West Aust 69:89–94
Bitter G (1911) Steinzellkonkretionen im Fruschtfleisch beerentragender Solanaceaen und deren systematische Bedeutung. Bot Jahrb 45:483–507
Carlquist S (1983) Intercontinental dispersal. In: Kubitzki K (ed) Dispersal and distribution. Paul Parey, Hamburg, pp 37–47
Mummenhoff K, Linder P, Friesen N, Bowman JL, Lee J-Y, Fanzke A (2004) Molecular evidence for biocontinental hybridsogenous genomic constitution in Lepidium sensu strict (Brassicaceae) species from Australia and New Zealand. Am J Bot 91:254–261
Vijverberg K, Mes THM, Bachmann K (1999) Chloroplast DNA evidence for the evolution of Miscroseris (Asteraceae) in Australia and New Zealand after long-distant dispersal from western North America. Am J Bot 86:1448–1463
Vijverberg K, Kuperus P, Breeuwer JAJ, Bachmann K (2000) Incipient adaptive radiation of New Zealand and Australian Microseris (Asteraceae): an amplified fragment length polymorphism (AFLP) study. J Evol Biol 13:997–1008
Fukuda T, Yokoyama J, Ohashi H (2001) Phylogeny and biogeography of the genus Lycium (Solanaceae): inferences from chloroplast DNA sequences. Mol Phylogenet Evol 19:246–258
Miller JS (2002) Phylogenetic relationships and the evolution of gender dimorphism in Lycium (Solanaceae). Syst Bot 27:416–428
Marks CE (2010) Definition of South Pacific taxa of Nicotiana section Suaveolentes. Muelleria 28:74–94
Chase MW, Knapp S, Cox AV, Clarkson JJ, Butsko Y, Joseph J, Savolainen V, Parokonny AS (2003) Molecular systematics, GISH and the origin of hybrid taxa in Nicotiana (Solanaceae). Ann Bot 90:1446–1454
Kemp EM (1978) Tertiary climatic evolution and vegetation history in the Southeast Indian Ocean region. Paleogeogr Paleoecol 24:169–208
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? Philos T R Soc B 359:1551–1571
Pain CF, Ollier CD (1983) Drainage patterns and tectonics around Milne Bay, Eastern Papua New Guinea. Rev Geomorph Dyn 32:113–120
Barlow BA (1994) Phytogeography of the Australian region. In: Groves RH (ed) Australian vegetation. University Press, Cambridge, pp 3–36
Polhemus DA, Polhemus JT (1998) Assembling New Guinea: 40 million years of island arc accretion as indicated by the distributions of aquatic Heteroptera (Insecta). In: Hall R, Holloway JD (eds) Biogeography and geological evolution of SE Asia. Buckhuys, Leiden, pp 327–340
Beebe NW, Cooper RD (2002) Distribution and evolution of the Anopheles punctulatus group (Diptera: Culicidae) in Australia and Papua New Guinea. Int J Parasitol 32:563–574
Acknowledgments
We thank Donovan Parks, for his help and advice with the GenGIS analysis. This study was supported by the CIMO Fellowship Grant, Finland and by the Finnish Government’s Scholarship provided to the first author. We also thank several Botanical Gardens, collectors of the plant material, and colleagues at the University of Helsinki for helpful discussions and ideas. We thank the Willi Hennig Society for making the program TNT publicly available. This research represents a partial fulfillment of the requirements for the degree of Doctor of Philosophy (PhD) in Plant Genetics and Biotechnology in the University of Pannonia, Hungary.
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ESM 1
Location set (sample sites) file used in GenGIS analysis. (PDF 72 kb)
ESM 2
Plant material used in the study. aSubgeneric names are according to D’Arcy (1972,1991); bmajor clades after Weese and Bohs (2007). cThese genera are now nested within the Solanum genus. Accession numbers in bold are provided by this study. (XLS 19 kb)
ESM 3
Geospatial representation of the phylogeny of the subgenus Archaesolanum in 3D. Phylogenetic tree of kangaroo apples is based on the BEAST and Maximum Parsimony phylogeny obtained from the combined trnT-trnF chloroplast region. Different species are indicated with unique colouring of branches. (PNG 1316 kb)
ESM 4 Video representation of the phylogeny of the subgenus Archaesolanum. (AVI 10910 kb)
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Poczai, P., Hyvönen, J. & Symon, D.E. Phylogeny of kangaroo apples (Solanum subg. Archaesolanum, Solanaceae). Mol Biol Rep 38, 5243–5259 (2011). https://doi.org/10.1007/s11033-011-0675-8
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DOI: https://doi.org/10.1007/s11033-011-0675-8