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Plant Systematics and Evolution

, Volume 259, Issue 1, pp 53–71 | Cite as

Phylogenetic analysis of morphology in Prunus reveals extensive homoplasy

  • E. Bortiri
  • B. Vanden Heuvel
  • D. PotterEmail author
Article

Abstract

Prunus is a large and economically important genus with considerable morphological variation. The evolution of vegetative and reproductive characters are examined here by parsimony reconstruction on trees obtained from data of ITS, trnL-trnF, trnS-trnG, and 25 morphological characters of 37 species of Prunus and representatives of eight other genera of Rosaceae. Prunus grayana is supported as the sister species to the rest of Prunus and the common ancestor of Prunus is reconstructed as having deciduous and serrated leaves, leafy racemes and fruit with well-developed pericarp. All diagnostic characters used in classification of the raceme-bearing species show some degree of convergent evolution and do not reflect phylogenetic relatedness. Some character states, such as evergreen foliage and entire leaf margin, are likely adaptations to environments with higher humidity and mean temperature. However, these hypotheses need to be tested by including species formerly classified in genus Pygeum, which were not available for this study. A clade consisting of subgenera Prunus, Amygdalus, Emplectocladus and section Microcerasus (formerly in subgenus Cerasus) is characterized by having axillary buds organized in groups of three, two of which give rise to flowers or inflorescences and one to a vegetative shoot. Fruits with thin pericarps are common in Prunus but they arose more than once independently. Dry fruits also evolved more than once, and only in species of Prunus living in arid environments, suggesting that this feature is another example of adaptation. Maddenia hypoleuca is nested within Prunus and the morphological characters used to segregate it from Prunus have been misinterpreted or are also found in species of Prunus previously classified in genus Pygeum.

Keywords

Prunus evolution morphology homoplasy parsimony likelihood topology tests 

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References

  1. Akaike, H. 1974A new look at the statistical model identification criteriaIEEE T. Automat. Cont.19716723CrossRefGoogle Scholar
  2. Blake, M. A. 1932The J. H. Hale peach as a parent in peach crossesP. Am. Soc. Hort. Sci.29131136Google Scholar
  3. Bortiri, E., Oh, S.-H., Gao, F.-Y., Potter, D. 2002The phylogenetic utility of nucleotide sequences of sorbitol 6-phosphate dehydrogenase in Prunus (Rosaceae)Amer. J. Bot.8916971708Google Scholar
  4. Bortiri, E., Oh, S.-H., Jiang, J., Baggett, S., Granger, A., Weeks, C., Buckingham, M., Potter, D., Parfitt, D. E. 2001Phylogeny and systematics of Prunus (Rosaceae) as determined by sequence analysis of ITS and the chloroplast trnL-trnF spacer DNASyst. Bot.26797807Google Scholar
  5. Brako, L., Zarucchi, J. L. 1993Catalogue of the flowering plants and gymnosperms of PeruMissouri Botanical GardenSt. Louis, USAGoogle Scholar
  6. Bremer, K. 1988The limits of amino acid sequence data in angiosperm phylogenetic reconstructionEvolution42795803CrossRefGoogle Scholar
  7. Browicz, K., Zohary, D. 1996The genus Amygdalus L. (Rosaceae): Species relationships, distribution, and evolution under domesticationGenet. Resour. Crop Ev.43229247CrossRefGoogle Scholar
  8. Buckley, T. R. 2002Model misspecification and probabilistic tests of topology: evidence from empirical data setsSyst. Biol.51509523PubMedCrossRefGoogle Scholar
  9. Fedorov, A. A., Komarov, V. L., Kostina, K. F., Kovalev, N. V., Krishtofovich, A. N., Linchevskii, I. A., Poyarkova, A. I. 1971Rosaceae -Rosoideae, PrunoideaeKomarov, V. L. eds. Flora of the U.S.S.R, vol 10Botanical Institute of the Academy of Sciences of the USSRMoscow, Russia380448Google Scholar
  10. Felsenstein, J. 1985Confidence limits on phylogenies: an approach using the bootstrapEvolution39783791CrossRefGoogle Scholar
  11. Goldblatt, P. 1976Cytotaxonomic studies in the tribe Quillajeae (Rosaceae)Ann. Missouri. Bot. Gard.63200206CrossRefGoogle Scholar
  12. Goldman, N., Anderson, J. P., Rodrigo, A. G. 2000Likelihood-based tests of topologies in phylogeneticsSyst. Biol.49652670PubMedCrossRefGoogle Scholar
  13. Graham, S. W., Reeves, P. A., Burns, A. C. E., Olmstead, R. G. 2000Microstructural changes in noncoding chloroplast DNA: interpretation, evolution, and utility of indels and inversions in basal angiosperm phylogenetic inferenceInt. J. Pl. Sci.161S83S96CrossRefGoogle Scholar
  14. Grant, V., Grant, K. 1965Flower pollination in the phlox familyColumbia University PressNew York, USAGoogle Scholar
  15. Huelsenbeck, J. P., Ronquist, F. 2001MRBAYES: Bayesian inference of phylogenyBioinformatics17754755PubMedCrossRefGoogle Scholar
  16. Kalkman, C. 1965The Old World species of Prunus subgenus Laurocerasus including those formerly referred to PygeumBlumea131174Google Scholar
  17. Koehne, E. 1915Zur Kenntnis von Prunus Grex Calycopadus und Grex Gymnopadus sect. LaurocerasusBot. Jahrb.52279333Google Scholar
  18. Krüssmann, G. 1986Manual of cultivated broad-leaved trees and shrubs, Vol. 3Timber PressPortland, USAGoogle Scholar
  19. Kuitert, W. 1999Japanese flowering cherriesTimber PressPortland, USAGoogle Scholar
  20. Lee, S., Wen, J. 2001A phylogenetic analysis of Prunus and the Amygdaloideae (Rosaceae) using ITS sequences of nuclear ribosomal DNAAmer. J. Bot.88150160Google Scholar
  21. Lersten, N. R., Horner, H. T. 2000Calcium oxalate crystal types and trends in their distribution patterns in leaves of Prunus (Rosaceae: Prunoideae)Pl. Syst. Evol.2248396CrossRefGoogle Scholar
  22. Lewis, P. O. 2001A likelihood approach to estimating phylogeny from discrete morphological character dataSyst. Biol.50913925PubMedCrossRefGoogle Scholar
  23. Lutzoni, F., Wagner, P., Reeb, V., Zoller, S. 2000Integrating ambiguously aligned regions of DNA sequences in phylogenetic analyses without violating positional homologySyst. Biol.49628651PubMedCrossRefGoogle Scholar
  24. Maddison, D. R., Maddison, W. P. 2003MacClade v. 4.06Sinauer Associates, IncSunderland, USAGoogle Scholar
  25. Mason, S. C. 1913The pubescent-fruited species of Prunus of the Southwestern StatesJ. Agr. Res.1147179Google Scholar
  26. McVaugh, R. 1951A revision of North American black cherries (Prunus serotina Ehrh and relatives)Brittonia7279315CrossRefGoogle Scholar
  27. Moore, J. N., Ballington, J. R.,Jr. 1990Genetic resources of temperate fruit and nut cropsInternational Society for Horticultural ScienceWageningen, The NetherlandsGoogle Scholar
  28. Morgan, D. R., Soltis, D. E., Robertson, K. R. 1994Systematic and evolutionary implications of rbcL sequence variation in RosaceaeAmer. J. Bot.81890903CrossRefGoogle Scholar
  29. Mowrey, B. D., Werner, D. J. 1990Phylogenetic relationships among species of Prunus as inferred by isozyme markersTheor. Appl. Genet.80129133CrossRefGoogle Scholar
  30. Nylander, J. A. A., Ronquist, F., Huelsenbeck, J. P., Nieves-Aldrey, J. L. 2004Bayesian phylogenetic analysis of combined dataSyst. Biol.534767PubMedCrossRefGoogle Scholar
  31. Oh, S.-H., Potter, D. 2004Molecular phylogenetic systematics and biogeography of tribe Neillieae (Rosaceae) using DNA sequences of cpDNA, rDNA, and leafyAmer. J Bot.92179192Google Scholar
  32. Posada, D., Buckley, T. R. 2004Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio testsSyst. Biol.53793808PubMedCrossRefGoogle Scholar
  33. Posada, D., Crandall, K. A. 2001Selecting the best-fit model of nucleotide substitutionSyst. Biol.50580601PubMedCrossRefGoogle Scholar
  34. Posada, D., Crandall, K. A. 1998Modeltest: testing the model of DNA substitutionBioinformatics14817818PubMedCrossRefGoogle Scholar
  35. Potter, D., Gao, F., Bortiri, E., Oh, S.-H., Baggett, S. 2002Phylogenetic relationships in Rosaceae from chloroplast matK and trnL-trnF nucleotide sequence dataPl. Syst. Evol.2317789CrossRefGoogle Scholar
  36. Rambaut A. (2001) Sequence Alignment Editor 2.0. Available from the author at: http://evolve.zoo.ox.ac.ukGoogle Scholar
  37. Raven, P. H. 1972Plant species disjunctions: a summaryAnn. Missouri Bot. Gard.59234246CrossRefGoogle Scholar
  38. Rehder, A. 1940Manual of cultivated trees and shrubs hardy in North America. 2nd ednMacmillanNew York, USAGoogle Scholar
  39. Roemer, M. J. 1847Familiarum naturalium regni vegetabilis synopses monographicae 4WeimarGermanyGoogle Scholar
  40. Schulze-Menz G. K. (1964) Rosaceae. In: Melchior H. (ed.) Engler's Syllabus der Pflanzenfamilien II Gebrüder Borntraeger, Berlin, Germany, pp. 209–218Google Scholar
  41. Shaw, J., Small, R. 2004Addressing the ``hardest puzzle in American pomology:'' Phylogeny of Prunus sect. Prunocerasus (Rosaceae) based on seven noncoding chloroplast DNA regionsAmer. J. Bot.91985996Google Scholar
  42. Shimodaira, H., Hasegawa, M. 1999Multiple comparison of log-likelihoods with applications to phylogenetic inferenceMol. Biol. Evol.1611141116Google Scholar
  43. Simmons, M. P., Ochoterena, H., Carr, T. G. 2001Incorporation, relative homoplasy, and effect of gap characters in sequence-based phylogenetic analysesSyst. Biol.50454462PubMedCrossRefGoogle Scholar
  44. Sorenson, M. D. 1999TreeRot, version 2Boston UniversityBoston, USAGoogle Scholar
  45. Sterling, C. 1964Comparative morphology of the carpel in the Rosaceae. II. Amygdaloideae: Maddenia, Pygeum, OsmaroniaAmer. J. Bot.51354360CrossRefGoogle Scholar
  46. Stevens, P. F. 1991Character states, morphological variation, and phylogenetic analysis: a reviewSyst. Bot.16553583CrossRefGoogle Scholar
  47. Swofford, D. L. 2001PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4Sinauer, SunderlandMassachusetts, USAGoogle Scholar
  48. Takhtajan, A. 1997Diversity and classification of flowering plantsColumbia University PressNew York, USAGoogle Scholar
  49. Tamura, K., Nei, M. 1996Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzeesMolec. Biol. Evol.10512526Google Scholar
  50. Templeton, A. R. 1983Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apesEvolution37221244CrossRefGoogle Scholar
  51. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., Higgins, D. G. 1997The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis toolsNucleic Acids Res.2548764882PubMedCrossRefGoogle Scholar
  52. Wen J. (1999) Evolution of eastern Asian and eastern North American disjunct distribution in flowering plants. Annual. Rev. Ecol. Syst. 421–455.Google Scholar
  53. Wight, W. F. 1915Native American species of PrunusB. U.S. Dep. Agr.179175Google Scholar
  54. Wilf, P. 1997When are leaves good thermometers? A new case for Leaf Margin AnalysisPaleobiology23373390Google Scholar
  55. Wilken, D. H. 1993PrunusHickman, J. C. eds. The Jepson manual: higher plants of CaliforniaUniversity of California PressBerkeley, USA969970Google Scholar
  56. Wojciechowski, M. F., Sanderson, M. J., Hu, J.-M. 1999Evidence on the monophyly of Astragalus (Fabaceae) and its major subgroups based on nuclear ribosomal DNA ITS and chloroplast DNA trnL intron dataSyst. Bot.24409437CrossRefGoogle Scholar
  57. Wyatt, R. 1983Pollinator-plant interactions and the evolution of breeding systemsReal, L. eds. Pollination BiologyAcademic Press IncLondon, UK5195Google Scholar
  58. Yü, T. T., Lu, L. T., Ku, T. C., Li, C. L., Chen, S. X. 1986Rosaceae (3), Amygdaloideae. Flora Reipublicae Popularis Sinicae, vol. 38Science PressBeijing, ChinaGoogle Scholar
  59. Zhang S.-Y. (1992a) Systematic wood anatomy of the Rosaceae. Blumea 37: 81–158.Google Scholar
  60. Zhang S.-Y. (1992b) Wood anatomy of trees and shrubs from China. III. Rosaceae. IAWA 13: 21–91.Google Scholar

Copyright information

© Springer-Verlag Wien 2006

Authors and Affiliations

  1. 1.Plant Gene Expression CenterAlbanyUSA
  2. 2.Department of BiologyColorado State University-PuebloPuebloUSA
  3. 3.Departament of Plant SciencesUniversity of CaliforniaDavisUSA

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