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Molecular phylogeny of Juglans (Juglandaceae): a biogeographic perspective

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Abstract

The eastern Asian and eastern North American disjunction in Juglans offers an opportunity to estimate the time since divergence of the Eurasian and American lineages and to compare it with paleobotanical evidence. Five chloroplast DNA noncoding spacer (NCS) sequences: trnT−trnF, psbA−trnH, atpB−rbcL, trnV-16S rRNA, and trnS-trnfM and data from earlier studies (matK, ITS, and nuclear RFLP) were used to reconstruct phylogeny and to estimate the divergence time of major lineages. Seventeen taxa from four sections of Juglans and two outgroup taxa, Pterocarya stenoptera and Carya illinoiensis were included. NCS data was congruent only with matK data. Both maximum parsimony (MP) and maximum likelihood (ML) cladograms were concordant at the sectional level and revealed three well-supported monophyletic clades corresponding to sections Juglans, Cardiocaryon, and Rhysocaryon in both NCS and combined analyses. The single extant American butternut, Juglans cinerea was placed within the poorly resolved, but well-supported Rhysocaryon. Placement of taxa within Rhysocaryon and Cardiocaryon were inconsistent between NCS and combined analyses. Overall, the results suggest that: (1) the NCS sequence divergence observed within and between sections of Juglans is low and the addition of matK data only marginally improved resolution within Rhysocaryon; (2) the early divergence of section Juglans in both MP and ML analyses of NCS and combined data implies its ancient origin in contrast to fossil evidence, which suggests the earliest divergence of sections Rhysocaryon and Cardiocaryon; and (3) the extant taxa may not hold the footprints to unravel the evolutionary history of the genus.

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References

  • Aradhya MK, Manshardt RM, Zee F, Morden CW (1999) A phylogenetic analysis of the genus Carica L (Caricaceae) based on restriction fragment length variation in a cpDNA intergenic spacer region. Genet Resour Crop Evol 46:579–586

    Article  Google Scholar 

  • Axelrod DI (1960) The evolution of flowering plants. In: Tax S (ed) Evolution after Darwin, vol. 1. Chicago University Press, Chicago, pp 227–305

    Google Scholar 

  • Axelrod DI, Bailey HP (1969) Paleotemperature analysis of Tertiary floras. Palaeogeogr Palaeoclimatol Palaeoecol 6:163–195

    Article  Google Scholar 

  • Azuma H, Garcia-Franco JG, Rico-Gray V, Thien LB (2001) Molecular phylogeny of Magnoliaceae: the biogeography of tropical and temperate disjunctions. Am J Bot 88:2275–2285

    Article  CAS  Google Scholar 

  • Baker FK, Lutzoni FM (2002) The utility of the incongruence length difference test. Syst Biol 51:625–637

    Article  Google Scholar 

  • Beug H-J (1975) Man as a factor in the vegetational history of the Balkan Peninsula. In: Jordanov D, Bondev I, Kozuharov S, Kuzmanov B, Palamarev E (eds) Problems of Balkan flora and vegetation. Proceedings of first international symposium on Balkan flora and vegetation, Varna, June 7–14, 1973. Publishing House of the Bulgarian Academy of Sciences, Sofia, Bulgaria, pp 72–78

  • Bonferroni CE (1936) Teoria statistica delle classi e calcolo delle probabilità. Istit Sup Sci Econ Commerc Firenze 8:3–62

    Google Scholar 

  • Bremer K (1988) The limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42:795–803

    Article  CAS  Google Scholar 

  • Chaney RW (1947) Tertiary centres and migration routes. Ecol Monogr 17:139–148

    Article  Google Scholar 

  • Crawford DJ, Lee MS, Stuessy TF (1992) Plant species disjunctions: perspectives from molecular data. Aliso 13:395–409

    Google Scholar 

  • Cros J, Combes MC, Trouslot P, Anthony F, Hamon S, Charrier A, Lashermes P (1998) Phylogenetic analysis of chloroplast DNA variation in Coffea L. Mol Phylogenet Evol 9:109–117

    Article  PubMed  CAS  Google Scholar 

  • Cunningham CW (1997) Can three incongruence tests predict when data should be combined? Mol Biol Evol 14:733–740

    PubMed  CAS  Google Scholar 

  • Demesure B, Sodzi N, Petit RJ (1995) A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Mol Ecol 4:129–131

    PubMed  CAS  Google Scholar 

  • Demesure B, Comps B, Petit RJ (1996) Chloroplast DNA phylogeography of the common beech (Fagus sylvatica L) in Europe. Evolution 50:2515–2520

    Article  CAS  Google Scholar 

  • Descourtilz ME (1829) Juglans fraxinifolia. Fl Pitt Med Antill 7:5–8

    Google Scholar 

  • Dode LA (1909a) Contribution to the study of the genus Juglans (English translation by R.E. Cuendett). Bull Soc Dendrol France 11:22–90

    Google Scholar 

  • Dode LA (1909b) Contribution to the study of the genus Juglans (English translation by R.E. Cuendett). Bull Soc Dendrol France 12:165–215

    Google Scholar 

  • Donoghue MJ, Smith SA (2004) Patterns in the assembly of temperate forests around the Northern Hemisphere. Philos Trans R Soc Lond 359:1633–1644

    Article  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Estabrook GF, McMorris FR, Meacham CA (1985) Comparison of undirected phylogenetic trees based on subtrees of four evolutionary units. Syst Zool 34:193–200

    Article  Google Scholar 

  • Farris JS, Kallersjo M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10:315–319

    Article  Google Scholar 

  • Farris JS, Kallersjo M, Kluge AG, Bult C (1995) Constructing a significance test for incongruence. Syst Biol 44:570–572

    Article  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  PubMed  CAS  Google Scholar 

  • Finden CR, Gordon AD (1985) Obtaining common pruned trees. J Classif 2:255–276

    Article  Google Scholar 

  • Fjellstrom RG, Parfitt DE (1995) Phylogenetic analysis and evolution of the genus Juglans (Juglandaceae) as determined from nuclear genome RFLPs. Plant Syst Evol 197:19–32

    Article  CAS  Google Scholar 

  • Gielly L, Taberlet P (1994) Chloroplast DNA polymorphism at the intrageneric level: implications for the establishment of plant phylogenies. Comptes Rendus de l’Académie des Sciences Life Science 317:685–692

    Google Scholar 

  • Graham A (1972) Outline of the origin and historical recognition of floristic affinities between Asia and eastern North America. In: Graham A (ed) Floristics and paleofloristics of Asia and eastern North America. Elsevier, Amsterdam, pp 1–168

    Google Scholar 

  • Gray A (1859) Diagnostic characters of phanerogamous plants, collected in Japan by Charles Wright, botanist of the U.S. North Pacific Exploring Expedition, with observations upon the relationship of the Japanese flora to that of North America and of other parts of northern Temperate Zone. Mem Am Acad Arts Sci 6:377–453

    Google Scholar 

  • Gray A (1878) Forest geography and archaeology. A lecture delivered before the Harvard University Natural History Society. Am J Sci Arts 3(16):85–94, 183–196

    Google Scholar 

  • Hills LV, Klovan JE, Sweet AR (1974) Juglans eocinerea n. sp., Beaufort Formation (Tertiary), southwestern Banks Inland, Arctic Canada. Can J Bot 52:65–90

    Article  Google Scholar 

  • Huelsenbeck JP, Rannala B (1997) Phylogenetic methods come of age: testing hypotheses in an evolutionary context. Science 276:227–232

    Article  PubMed  CAS  Google Scholar 

  • Huntley B, Birks HJB (1983) An atlas of past and present pollen maps for Europe: 0–13,000 years ago. Cambridge University Press, NY

    Google Scholar 

  • Johnson LA, Soltis DE (1998) Assessing incongruence: empirical examples from molecular data. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants II. DNA sequencing. Kluwer, Boston, pp 297–343

    Google Scholar 

  • Kimura M (1981) Estimation of evolutionary distances between homologous nucleotide sequences. Proc Natl Acad Sci USA 78:454–458

    Article  PubMed  CAS  Google Scholar 

  • Kuang K, Cheng S, Li P, Lu P (1979) Juglandaceae (In Chinese, unpublished translation provided by Manning WE). In: Kuang K-Z, Li CP (eds) Flora Reipublicae Popularis Sinicae, Vol. 21. Institutum Botanicum Academiae Sinicae, Peking, pp 8–42

    Google Scholar 

  • Langley CH, Fitch W (1974) An estimation of the constancy of the rate of molecular evolution. J Mol Evol 3:161–177

    Article  PubMed  CAS  Google Scholar 

  • Manchester SR (1987) The fossil history of Juglandaceae. Monogr Syst Bot Mo Bot Gard 21:1–137

    Google Scholar 

  • Manning WE (1948) The morphology of the flowers of the Juglandaceae. III. The staminate flowers. Am J Bot 35:606–621

    Article  Google Scholar 

  • Manning WE (1957) The genus Juglans in Mexico and Central America. J Arnold Arbor 38:121–150

    Google Scholar 

  • Manning WE (1960) The genus Juglans in South America and West Indies. Brittonia 12:1–26

    Article  Google Scholar 

  • Manning WE (1978) The classification within the Juglandaceae. Ann Mo Bot Gard 65:1058–1087

    Article  Google Scholar 

  • Manos PS, Stone DE (2001) Evolution, phylogeny, and systematics of the Juglandaceae. Ann Mo Bot Gard 88:231–269

    Article  Google Scholar 

  • McGranahan G, Leslie C (1991) Walnuts (Juglans). In: Moore JN, Ballington JR Jr. (eds) Genetic resources of temperate fruit and nut crops. International Society for Horticultural Science, Wageningen, pp 907–951

    Google Scholar 

  • McKenna MC (1983) Cenozoic paleogeography of North Atlantic land bridges. In: Bott MHP, Saxov S, Talwani M, Thiede J (eds) Structure and development of the Greenland–Scotland ridge. Plenum, NY, pp 351–399

    Google Scholar 

  • Mickevich MF, Farris JS (1981) The implications of congruence in Menidia. Syst Zool 30:351–370

    Article  Google Scholar 

  • Miller RB (1976) Wood anatomy and identification of species of Juglans. Bot Gaz 137:368–377

    Article  Google Scholar 

  • Mohanty A, Martin JP, Aguinagalde I (2001) Chloroplast DNA study in wild populations and some cultivars of Prunus avium L. Theor Appl Genet 103:112–117

    Article  CAS  Google Scholar 

  • Muse SV, Weir BS (1992) Testing for equality of evolutionary rates. Genetics 132:2698–276

    Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, NY

    Google Scholar 

  • Ogihara Y, Terachi T, Sasakuma T (1991) Molecular analysis of the hot spot region related to length mutations in wheat chloroplast DNAs I Nucleotide divergence of genes and intergenic spacer regions located in the hot spot region. Genetics 129:873–884

    PubMed  CAS  Google Scholar 

  • Palmer JD (1991) Plastid chromosome: structure and evolution. In: Bogorad L, Vasil IK (eds) The molecular biology of plastids. Academic, San Diego, pp 5–53

    Google Scholar 

  • Parks CR, Wendel JF (1990) Molecular divergence between Asian and North American species of Liriodendron (Magnoliaceae) with implications for interpretation of fossil floras. Am J Bot 77:1243–1256

    Article  CAS  Google Scholar 

  • Petit RJ, Pineau E, Demesure B, Bacilieri R, Ducousso A, Kremer A (1997) Chloroplast DNA footprints of postglacial recolonisation by oaks. Proc Natl Acad Sci USA 94:9996–10001

    Article  PubMed  CAS  Google Scholar 

  • Popov MG (1929) Wild growing fruit trees and shrubs of Asia Minor (in Russian). Bull Appl Bot Pl Breed 22:241–483

    Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Rao CR (1973) Linear statistical inference and its applications. Wiley, NY

    Google Scholar 

  • Raven PH (1972) Plant species disjunctions: a summary. Ann Mo Bot Gard 59:234–2146

    Article  Google Scholar 

  • Rehder A (1940) Manual of cultivated trees and shrubs in North America. MacMillan, NY

    Google Scholar 

  • Rieseberg LH, Soltis DE (1991) Phylogenetic consequences of cytoplasmic gene flow in plants. Evol Trends Plants 5:65–84

    Google Scholar 

  • Robinson DF, Foulds LR (1981) Comparison of phylogenetic trees. Math Biosci 53:131–147

    Article  Google Scholar 

  • Sanderson MJ (1997) A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol Biol Evol 14:1218–1231

    CAS  Google Scholar 

  • Sanderson MJ (2002) Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol Biol Evol 19:101–109

    PubMed  CAS  Google Scholar 

  • Sanderson MJ (2003) r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19:101–109; 301–302

    Article  Google Scholar 

  • Schnabel A, Wendel JF (1998) Cladistic biogeography of Gleditsia (Leguminosae) based on NDHF and RPL16 chloroplast gene sequences. Am J Bot 85:1753–1765

    Article  CAS  Google Scholar 

  • Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381

    Article  PubMed  CAS  Google Scholar 

  • Small RL, Ryburn JA, Cronn RC, Seelanan T, Wendel JF (1998) The tortoise and the hare: choosing between noncoding plastome and nuclear ADH sequences for phylogeny reconstruction in a recently diverged plant group. Am J Bot 85:1301–1315

    Article  CAS  Google Scholar 

  • Smith JF, Doyle JJ (1995) A cladistic analysis of chloroplast DNA restriction site variation and morphology for the genera of the Juglandaceae. Am J Bot 82:1163–1172

    Article  Google Scholar 

  • Sorenson MD (1999) TreeRot, Version 2. Boston University, Boston, MA

    Google Scholar 

  • Stanford AM, Harden R, Parks CR (2000) Phylogeny and biogeography of Juglans (Juglandaceae) based on matK and ITS sequence data. Am J Bot 87:872–882

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (1991) When are phylogeny estimates from molecular and morphological data incongruent? In: Miyamoto MM, Cracraft J (eds) Phylogenetic analysis of DNA sequences. Oxford University Press, NY, pp 295–333

    Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (* and other methods), Version 4. Sinauer Associates, Sunderland, MA

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tajima F (1993) Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135:599–607

    PubMed  CAS  Google Scholar 

  • Takezaki N, Rzhetsky A, Nei M (1995) Phylogenetic test of the molecular clock and linearized trees. Mol Biol Evol 12:823–833

    PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Tiffney BH (1985a) Perspectives on the origin of the floristic similarity between eastern Asia and eastern North America. J Arnold Arbor 66:73–94

    Google Scholar 

  • Tiffney BH (1985b) The Eocene North Atlantic land bridge: its importance in Tertiary and modern phytogeography of the Northern Hemisphere. J Arnold Arbor 66:243–273

    Google Scholar 

  • Wen J (1999) Evolution of eastern Asian and eastern North American disjunct distributions in flowering plants. Ann Rev Ecolog Syst 30:421–455

    Article  Google Scholar 

  • Wen J (2001) Evolution of eastern Asian–Eastern North American biogeographic disjunctions: a few additional issues. Int J Plant Sci 162:S117–S122

    Article  Google Scholar 

  • Wen J, Stuessy TF (1993) The phylogeny and biogeography of Nyssa (Cornaceae). Syst Bot 18:68–79

    Article  Google Scholar 

  • Wendel JF, Albert VA (1992) Phylogenetics of the cotton genus (Gossypium): character-state weighted parsimony analysis of chloroplast–DNA restriction site data and its systematic and biogeographic implications. Syst Bot 17:115–143

    Article  Google Scholar 

  • Wendel JF, Stewart JMcD, Rettig JH (1991) Molecular evidence of homoploid reticulate evolution among Australian species of Gossypium. Evolution 45:694–711

    Article  Google Scholar 

  • Wilken DH (1993) Juglandaceae. In: Hickman JC (ed) The Jepson manual: higher plants of California. University of California Press, Berkeley, p 709

    Google Scholar 

  • Wolfe JA (1969) Neogene floristic and vegetational history of the Pacific northwest. Madrono 20:83–110

    Google Scholar 

  • Wolfe JA (1971) Tertiary climatic fluctuations and methods of analysis of Tertiary floras. Palaeogeogr Palaeoclimatol Palaeoecol 9:27–57

    Article  Google Scholar 

  • Wolfe JA (1972) An interpretation of Alaskan Tertiary floras. In: Graham A (ed) Floristics and paleofloristics of Asia and eastern North America. Elsevier, Amsterdam, pp 201–233

    Google Scholar 

  • Wolfe JA (1975) Some aspects of plant geography of the Northern Hemisphere during the late Cretaceous and Tertiary. Ann Mo Bot Gard 62:264–279

    Article  Google Scholar 

  • Wolfe JA (1978) A paleobotanical interpretation of Tertiary climates in the Northern Hemisphere. Am Sci 66:694–703

    Google Scholar 

  • Wolfe JA (1985) Distribution of major vegetational types during the Tertiary. In: Sundquist ET, Broecker WS (eds) The carbon cycle and the atmospheric CO2: natural variations Archean to present, (Geophysical Monograph 32). American Geophysical Union, Washington, DC, pp 357–375

    Google Scholar 

  • Wolfe JA, Leopold EB (1967) Neogene and early Quaternary vegetation of northwestern North America and northeastern Asia. In: Hopkins DM (ed) The Bering land bridge. Stanford University Press, Stanford, pp 193–206

    Google Scholar 

  • Wolfe KH, Li W–H, Sharp P (1987) Rates of nucleotide substitution vary greatly among plant mitochondria, chloroplast, nuclear DNAs. Proc Natl Acad Sci USA 84:9054–9058

    Article  PubMed  CAS  Google Scholar 

  • Xiang Q, Soltis DE, Soltis PS, Manchester SR, Crawford DL (2000) Timing the eastern Asian–eastern North American floristic disjunction: molecular clock corroborates paleontological estimates. Mol Phylogenet Evol 15:462–472

    Article  PubMed  CAS  Google Scholar 

  • Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V (ed) Evolving genes and proteins. Academic, NY, pp 97–106

    Google Scholar 

  • Zurawski G, Clegg MT (1987) Evolution of higher-plant chloroplast DNA-encoded genes: implications for structure–function and phylogenetic studies. Annu Rev Plant Physiol 38:391–418

    Article  CAS  Google Scholar 

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Acknowledgements

This study was funded by the U.S. Department of Agriculture, Agricultural Research Service (ARS Project No. 5306-21000-015-00D). We thank Clay Weeks, Warren Roberts, and Chuck Leslie for contributing to collection of samples and many helpful suggestions.

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Correspondence to Mallikarjuna K. Aradhya.

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Aradhya, M.K., Potter, D., Gao, F. et al. Molecular phylogeny of Juglans (Juglandaceae): a biogeographic perspective. Tree Genetics & Genomes 3, 363–378 (2007). https://doi.org/10.1007/s11295-006-0078-5

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