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Biochemical and molecular genetic markers in biosystematic studies of forest trees

  • Review paper
  • Biosystematics and adaptive significance of biochemical markers
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Abstract

Biochemical and molecular markers have proven to be powerful tools for discerning biosystematic, biogeographic, and phylogenetic relationships. Biosystematic information can be important for guiding traditional breeding programs, gene transfer, interspecific hybridization, and gene conservation. A phylogenetic framework is usually necessary, but frequently ignored, for making valid statistical tests in studies of adaptive evolution. Several studies have indicated a strong correlation between biochemical “races” and traits important to growth and adaptation, suggesting that evolutionary legacy may affect genetic architecture of fitness traits — with consequences for seed transfer, breeding strategies, and tolerance of climate change. A number of methods for phylogenetic analysis exist, but differ in their assumptions. Use of an inappropriate method — such as a method that assumes constant rates of evolution when rates in fact vary — can lead to incorrect phylogenies. Because of their complexity, phylogenetic topologies are often difficult to determine unambiguously; estimates of statistical confidence should therefore accompany phylogenetic trees if they are to be regarded as providing new knowledge, or strong confirmation, of relationships. Molecular genetic markers are more expensive than biochemical markers such as allozymes and terpenes, but they provide increased accuracy and expanded scope of biosystematic inference, and facilitate statistical analyses of phylogenetic trees.

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Abbreviations

BMGMs:

biochemical and molecular genetic markers

cpDNA:

chloroplast DNA

OTU:

operational taxonomic unit

rbcL:

chloroplast gene encoding ribulose 1,5-bisphosphate carboxylase large subunit

rbcS:

nuclear gene encoding ribulose 1,5-bisphosphate carboxylase small subunit

rDNA:

ribosomal DNA

RFLP:

restriction fragment length polymorphism

UPGMA:

unweighted pair group method of clustering using averages

References

  • Adams, R. and Simmons, D. 1987. A chemosystematic study of Calluris (Cupressaceae) in south-eastern Australia using volatile oils. Aust. For. Res. 17: 113–125.

    Google Scholar 

  • Arbez, M., Bernard-Dagan, C. and Fillon, C. 1974. Intraspecific variability of Pinus nigra monoterpenes: analysis of the first results. Ann. Sci. For. 31:57–70.

    Google Scholar 

  • Archie, J. W. 1989. Homoplasy excess ratios: new indices for measuring levels of homoplasy in phylogenetic systematics and a critique of the consistency index. Syst. Zool. 38: 253–269.

    Google Scholar 

  • Avise, J. C., Arnold, J., Ball, R. M., Bermingham, E., Lamb, T., Neigel, J. E., Reeb, C. A. and Saunders, N. C. 1987. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu. Rev. Ecol. Syst. 18: 489–522.

    Google Scholar 

  • Benfey, P. N. and Chua, N. H. 1989. Regulated genes in transgenic plants. Science 244: 174–181.

    Google Scholar 

  • Bousquet, J., Cheliak, W. M. and Lalonde, M. 1987a. Genetic differentiation among 22 mature populations of green alder (Alnus crispa) in central Quebec. Can. J. For. Res. 17: 219–227.

    Google Scholar 

  • Bousquet, J., Cheliak, W. M. and Lalonde, M. 1987b. Genetic diversity within and among 11 juvenile populations of green alder (Alnus crispa) in Canada. Physiol. Plant. 70: 311–318.

    Google Scholar 

  • Bousquet, J., Cheliak, W. M. and Lalonde, M.. 1988. Allozyme variation within and among mature populations of speckled alder (Alnus rugosa) and relationships with green alder (A. crispa). Am. J. Bot. 75: 1678–1686.

    Google Scholar 

  • Bousquet, J., Cheliak, W. M., Wang, J. and Lalonde, M. 1990. Genetic divergence and introgressive hybridization between Alnus sinuata and A. crispa (Betulaceae). Plant Syst. Evol. 170:107–124.

    Google Scholar 

  • Bousquet, J., Girouard, E., Strobeck, C., Dancik, B. P. and Lalonde, M. 1989. Restriction fragment polymorphisms in the rDNA region among seven species of Alnus and Betula papyrifera. Plant Soil 118: 231–240.

    Google Scholar 

  • Brotschol, J. V., Roberds, J. H. and Namkoong, G. 1986. Allozyme variation among North Carolina populations of Liriodendron tulipifera L. Silvae Genet. 35:131–138.

    Google Scholar 

  • Bruce, W. B., Christensen, A. H., Klein, T., Fromm, M. and Quail, P. H. 1989. Photoregulation of a phytochrome gene from oat transferred into rice by particle bombardment. Proc. Natl. Acad. Sci. USA 86:9692–9696.

    Google Scholar 

  • Burt, A. 1989. Comparative methods using phylogenetically independent contrasts, pp. 33–53. In: Harvey, P. H. and Partridge, L. (Eds) Oxford Surveys in Evolutionary Biology, Vol. 6. Oxford Univ. Press, England.

    Google Scholar 

  • Bush, R. M. and Smouse, P. E. 1992. Evidence for the adaptive significance of allozymes in forest trees. This issue, pp. 179–196.

  • Cavalli-Sforza, L. L. and Edwards, A. W. F. 1967. Phylogenetic analyses: models and estimation procedures. Am. J. Human Genet. 19: 233–257.

    Google Scholar 

  • Clegg, M. T. 1989. Molecular diversity in plant populations, pp. 98–115. In: Brown, A. H. D., Clegg, M. T., Kahler, A. L. and Weir, B. S. (Eds) Plant Population Genetics, Breeding, and Genetic Resources. Sinauer Associates, Inc. Publishers, Sunderland, Massachusetts.

    Google Scholar 

  • Coates, D. J. and Sokolowski, R. E. 1989. Geographic patterns of genetic diversity in Karri (Eucalyptus diversicolor F. Muell.). Aust. J. Bot. 37:145–156.

    Google Scholar 

  • Comps, B., Barriere, G., Merzeau, D. and Letouzey, J. 1987. La variability alloenzymatique des hêtraies dans les sous-domaines medio- et eu-atlantiques d'Europe. Can. J. For. Res. 17:1043–1049.

    Google Scholar 

  • Conkle, M. T. and Critchfield, W. B. 1988. Genetic variation and hybridization of pon-derosa pine, pp. 27–43. In: Ponderosa Pine: The Species and its Management. Washington State Univ. Cooperative Extension, Pullman, WA.

    Google Scholar 

  • Conkle, M. T., Schiller, G. and Grunwald, C. 1988. Electrophoretic analysis of diversity and phylogeny of Pinus brutia and closely related taxa. Syst. Bot. 13: 411–424.

    Google Scholar 

  • Copes, D. L. and Beckwith, R. C. 1977. Isoenzyme identification of Picea glauca, P. sitchensis, and P. lutzii populations. Bot. Gaz. 138: 512–521.

    Google Scholar 

  • Critchfield, W. B. 1975. Interspecific hybridization in Pinus a summary review, pp. 99–105 In: Fowler, D.P. and Yeatman, C. W. (Eds) Proc. 14th Meet., Canad. Tree Improvement Assoc., Part 2.

  • Critchfield, W. B. 1984. Impact of the Pleistocene on the genetic structure of North American conifers, pp. 70–118. In: Lanner, R. M. (Ed) Proc. 8th North American Forest Biology Workshop, Dept. of Forest Resources, Utah State Univ., Logan, UT.

    Google Scholar 

  • Cwynar, L. C. and MacDonald, G. M. 1987. Geographical variation of lodgepole pine in relation to population history. Am. Nat. 129:463–469.

    Google Scholar 

  • Doolittle, R F. (Ed) 1990. Methods in Enzymology, Vol. 183. Molecular Evolution: Computer Analysis of Protein and Nucleic Acid Sequences. Academic Press, San Diego, California, 736 pp.

    Google Scholar 

  • Duffield, J. W. 1952. Relationships and species hybridization in the genus Pinus. Z. Forstgenetik 1(4): 93–97.

    Google Scholar 

  • Epperson, B. 1992. Sptial structure of genetic variation within forest trees. This issue, pp. 257–278.

  • Erdtman, H., Kimland, B. and Norin, T. 1966. Pine phenolics and pine classification. Bot. Mag. Tokyo 79: 499–505.

    Google Scholar 

  • Evans, I. J., James, A. M. and Barnes, S. R. 1983. Organization and evolution of repeated DNA sequences in closely related plant genomes. J. Mol. Biol. 170: 803–826.

    Google Scholar 

  • Falconer, D. S. 1981. Introduction to Quantitative Genetics, Second Ed. Longman, NY.

    Google Scholar 

  • Farris, J. S. 1970. Methods for computing Wagner trees. Syst. Zool. 19: 83–92.

    Google Scholar 

  • Farris, J. S.. 1972. Estimating phylogenetic trees from distance matrices. Am. Nat. 106: 645–668.

    Google Scholar 

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

    Google Scholar 

  • Felsenstein, J. 1985a. Phylogenies and the comparative method. Am. Nat. 125: 1–15.

    Google Scholar 

  • Felsenstein, J. 1985b. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.

    Google Scholar 

  • Felsenstein, J. 1988. Phylogenies from molecular sequences: inference and reliability. Annu. Rev. Genet. 22: 521–565.

    Google Scholar 

  • Fins, L. and Seeb, L. W. 1986. Genetic variation in allozymes of western larch. Can. J. For. Res. 16: 1013–1018.

    Google Scholar 

  • Fitch, W. M. 1976. Molecular evolutionary clocks, pp. 160–178. In: Ayala, F. J. (Eds) Molecular evolution. Sinauer Associates, Inc., Publishers, Sunderland, Massachusetts.

    Google Scholar 

  • Fitch, W. M. 1977. On the problem of discovering the most parsimonious tree. Am. Nat. 111: 223–257.

    Google Scholar 

  • Fitch, W. M. and Margoliash, E. 1967. Construction of phylogenetic trees. Science 155: 279–284.

    Google Scholar 

  • Forde, M. B. and Blight, M. M. 1964. Geographical variation in the turpentine of Bishop pine. New Zeal. J. Bot. 2: 44–52

    Google Scholar 

  • Forrest, G.I. 1975. Polyphenol variation in Sitka spruce. Can. J. For. Res. 5: 26–37.

    Google Scholar 

  • Forrest, G.I. 1980. Genotypic variation among native Scots pine populations in Scotland based on monoterpene analysis. Forestry 53: 101–128.

    Google Scholar 

  • Forrest, G.I. 1982. Relationship of some European Scots pine populations to native Scottish woodlands based on monoterpene analysis. Forestry 55: 19–37.

    Google Scholar 

  • Fowler, D. P. and Morris, R. W. 1977. Genetic diversity in red pine: evidence for low genic heterozygosity. Can. J. For. Res. 7: 343–347.

    Google Scholar 

  • Furnier, G. R. and Adams, W. T. 1986. Geographic patterns of allozyme variation in Jeffrey pine. Am. J. Bot. 73: 1009–1015.

    Google Scholar 

  • Golenberg, E. M., Giannasi, D. E., Clegg, M. T., Smiley, C. J., Durbin, M., Henderson, D. and Zurawski, G. 1990. Chloroplast DNA sequence from a Miocene Magnolia species. Nature 344: 656–658.

    Google Scholar 

  • Gould, S. J. and Lewontin, R. C. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc. Roy. Soc. Lond. B 205: 581–598.

    Google Scholar 

  • Gullberg, U., Yazdani, R., Rudin, D. and Ryman, N. 1985. Allozyme variation in Scots pine (Pinus sylvestris L.) in Sweden. Silvae Genet. 34: 193–201.

    Google Scholar 

  • Guttman, S. I. and Weigt, L. A. 1989. Electrophoretic evidence of relationships among Quercus (oaks) of eastern North America. Can. J. Bot. 67: 339–351.

    Google Scholar 

  • Hanover, J. W. 1992. Tree fitness as a function of terpene composition. This issue, pp. 159–178.

  • Harry, D. E. 1984. Genetic structure of incense-cedar (Calocedrus decurrens) populations. Ph.D. thesis. Univ. of California, Berkeley, 163 pp.

    Google Scholar 

  • Holmquist, G. P. 1989. Evolution of chromosome bands: molecular ecology of noncoding DNA. J. Mol. Evol. 28: 469–486.

    Google Scholar 

  • Hopper, S. D. and Burgman, M. A. 1983. Cladistic and phenetic analyses of phylogenetic relationships among populations of Eucalyptus caesia. Aust. J. Bot. 31: 35–49.

    Google Scholar 

  • Jacobs, B. F., Werth, C. R. and Guttman, S. I. 1984. Genetic relationships in Abies (fir) of eastern United States: an electrophoretic study. Can. J. Bot. 62: 609–616.

    Google Scholar 

  • Jin, L. and Nei, M. 1990. Limitations of the evolutionary parsimony method of phylogenetic analysis. Mol. Biol. Evol. 7: 82–102.

    Google Scholar 

  • Jukes, T. H. and Cantor, C. R. 1969. Evolution of protein molecules, pp. 121–132. In: Munro, H. N. (Ed) Mammalian Protein Metabolism. Academic Press, NY.

    Google Scholar 

  • Karalamangala, R. R. and Nickrent, D. L. 1989. An electrophoretic study of representatives of subgenus Diploxylon of Pinus. Can. J. Bot. 67: 1750–1759.

    Google Scholar 

  • Keim, P., Paige, K. N., Whitham, T. G. and Lark, K. G. 1989. Genetic analysis of an interspecific hybrid swarm of Populus: Occurrence of unidirectional introgression. Genetics 123: 557–565.

    Google Scholar 

  • Kimura, M. 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111–120.

    Google Scholar 

  • Kimura, M. 1983. The Neutral Theory of Molecular Evolution. Cambridge Univ. Press, Cambridge, England.

    Google Scholar 

  • Kinloch, B. B., Westfall, R. D. and Forrest, G. I. 1986. Caledonian Scots pine: origins and genetic structure. New Phytol. 104: 703–729.

    Google Scholar 

  • Lagercrantz, U. and Ryman, N. 1990. Genetic structure of Norway spruce (Picea abies): Concordance of morphological and allozymic variation. Evolution 44: 38–53.

    Google Scholar 

  • Lake, J. A. 1987. A rate-independent technique for analysis of nucleic acid sequences: evolutionary parsimony. Mol. Biol. Evol. 4: 167–191.

    Google Scholar 

  • Lebreton, P. 1990. La chimiotaxonomie des Gymnospermes. Bull. Soc. Bot. France 137, Lett. Bot. (1) 35–46.

    Google Scholar 

  • Ledig, F. T. 1988. The conservation of diversity in forest trees. BioScience 38: 471–479.

    Google Scholar 

  • Ledig, F. T. and Conkle, M. T. 1983. Gene diversity and genetic structure in a narrow endemic, Torrey pine (Pinus torreyana Parry ex Carr.). Evolution 37: 79–85.

    Google Scholar 

  • Lester, D. T. 1974. Geographic variation in leaf and twig monoterpenes of balsam fir. Can. J. For. Res. 4: 55–60.

    Google Scholar 

  • Lewontin, R. C. 1985. Population genetics. Annu. Rev. Genet. 19: 81–102.

    Google Scholar 

  • Li, P. and Adams, W. T. 1989. Range-wide patterns of allozyme variation in Douglas-fir (Pseudotsuga menziesii). Can. J. For. Res. 19: 149–161.

    Google Scholar 

  • Li, P. and Adams, W. T. 1981. Simple method for constructing phylogenetic trees from distance matrices. Proc. Natl. Acad. Sci. USA. 78: 1085–1089.

    Google Scholar 

  • Li, P. and Adams, W. T. 1989. A statistical test of phylogenies estimated from sequence data. Mol. Biol. Evol. 6: 424–435.

    Google Scholar 

  • Li, W.-H. and Tanimura, M. 1987. The molecular clock runs more slowly in man than in apes and monkeys. Nature 326: 93–96.

    Google Scholar 

  • Li, W. H., Wu, C.-I. and Luo, C.-C. 1985. A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol. Biol. Evol. 2: 150–174.

    Google Scholar 

  • Manos, P. S. and Fairbrothers, D. E. 1987. Allozyme variation in populations of six northeastern American red oaks (Fagaceae: Quercus subg. Erythrobalanus). Syst. Bot. 12: 365–373.

    Google Scholar 

  • Martin, P. G. and Dowd, J. M. 1984a. The study of plant phylogeny using amino acid sequences of ribulose-1,5-bisphosphate carboxylase. IV. Proteaceae and Fagaceae and the rate of evolution of the small subunit. Aust. J. Bot. 32:291–299.

    Google Scholar 

  • Martin, P. G. and Dowd, J. M. 1984b. The study of plant phylogeny using amino acid sequences of ribulose-1,5-bisphosphate carboxylase. V. Magnoliaceae, Polygonaceae and the concept of primitiveness. Aust. J. Bot. 32: 301–309.

    Google Scholar 

  • Martin, P. G. and Dowd, J. M. 1986. A phylogenetic tree for some monocotyledons and gymnosperms derived from protein sequences. Taxon 35: 469–475.

    Google Scholar 

  • Martin, P. G. and Dowd, J. M. 1988. A molecular evolutionary clock for angiosperms. Taxon 37: 364–377.

    Google Scholar 

  • Merkle, S. A. and Adams, W. T. 1987. Patterns of allozyme variation within and among Douglas-fir breeding zones in southwest Oregon. Can. J. For. Res. 17: 402–407.

    Google Scholar 

  • Merkle, S. A., Adams, W. T. and Campbell, R K. 1988. Multivariate analysis of allozyme variation patterns in coastal Douglas-fir from southwest Oregon. Can. J. For. Res. 18: 181–187.

    Google Scholar 

  • Millar, C. I. 1983. A steep cline in Pinus muricata. Evolution 37: 311–319.

    Google Scholar 

  • Millar, C. I. 1989. Allozyme variation of bishop pine associated with pygmy-forest soils in northern California. Can. J. For. Res. 19: 870–879.

    Google Scholar 

  • Millar, C. I. and Marshall, K. A. 1990. Allozyme variation of Port-Orford-Cedar (Chamaecyparis lawsoniana): implications for genetic conservation. For. Sci. (in press)

  • Millar, C. I. and Westfall, R. D. 1992. Allozyme markers in forest genetic conservation. This issue, pp. 347–371.

  • Millar, C. I., Strauss, S. H., Conkle, M. T. and Westfall, R. D. 1988. Allozyme differentiation and biosystematics of the Californian closed-cone pines (Pinus subsect. Oocarpae). Syst. Bot. 13: 351–370.

    Google Scholar 

  • Mirov, N. T., Zavarin, E., Snajberk, K. and Costello, K. 1966. Further studies of turpentine composition of Pinus muricata in relation to its taxonomy. Phytochemistry 5: 343–355.

    Google Scholar 

  • Moore, N. J. and Moran, G. F. 1989. Microgiographical patterns of allozyme variation in Casuarina cunninghamiana Miq. within and between the Murrumbidgee and coastal drainage systems. Aust. J. Bot. 37: 181–192.

    Google Scholar 

  • Moran, G. F. and Adams, W. T. 1989. Microgeographical patterns of allozyme differentiation in Douglas-fir from southwest Oregon. For. Sci. 35: 3–15.

    Google Scholar 

  • Moran, G. F. and Bell, J. C. 1987. The origin and genetic diversity of Pinus radiata in Australia. Theor. Appl. Genet. 73: 616–622.

    Google Scholar 

  • Moran, G. F., Bell, J. C. and Eldridge, K. G. 1988. The genetic structure and the conservation of the five natural populations of Pinus radiata. Can. J. For. Res. 18: 506–514.

    Google Scholar 

  • Moran, G. F., Bell, J. C. and Turnbull, J. W. 1989. A chne in genetic diversity in river she-oak Casuarina cunninghamiana. Aust. J. Bot. 37: 169–180.

    Google Scholar 

  • Moran, G. F. and Hopper, S. D. 1983. Genetic diversity and the insular population structure of the rare granite rock species, Eucalyptus caesia Benth. Aust. J. Bot. 31: 161–172.

    Google Scholar 

  • Mueller, L. D. and Ayala, F. J. 1982. Estimation and interpretation of genetic distance in empirical studies. Genet. Res. Camb. 40: 127–137.

    Google Scholar 

  • Neale, D. B. 1992. Potential for marker assisted selection in forest trees. This issue, pp. 391–407.

  • Neale, D. B. and Sederoff, R. R. 1989. Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine. Theor. Appl. Genet. 77: 212–216.

    Google Scholar 

  • Nei, M. 1972. Genetic distance between populations. Am. Nat. 196: 283–292.

    Google Scholar 

  • Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583–590.

    Google Scholar 

  • Nei, M. 1987. Molecular Evolutionary Genetics. Columbia Univ. Press, New York. 512 pp.

    Google Scholar 

  • Nei, M. and Li, W.-H. 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl. Acad. Sci. USA. 76: 5269–5273.

    Google Scholar 

  • Nei, M. and Tajima, F. 1983. Maximum likelihood estimation of the number of nucleotide substitutions from restriction site data. Genetics 105: 207–217.

    Google Scholar 

  • Nei, M., Stephens, J. C. and Saitou, N. 1985. Methods for computing the standard errors of branching points in an evolutionary tree and their application to molecular data from humans and apes. Mol. Biol. Evol. 2: 66–85.

    Google Scholar 

  • Nei, M. and Gojobori, T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous substitutions. Mol. Biol. Evol. 3: 418–426.

    Google Scholar 

  • Nei, M. and Miller, J. C. 1990. A simple method for estimating average number of nucleotide substitutions within and between populations from restriction data. Genetics 125: 873–879.

    Google Scholar 

  • Niebling, C. R. and Conkle, M. T. 1990. Diversity of Washoe pine and comparisons with allozymes of ponderosa pine races. Can. J. For. Res. 20: 298–308.

    Google Scholar 

  • Nikolic, D. and Tucic, N. 1983. Isoenzyme variation within and among populations of European black pine (Pinus nigra Arnold). Silvae Genet. 32: 80–89.

    Google Scholar 

  • O'Reilly, G. J., Parker, W. H. and Cheliak, W. M. 1985. Isozyme differentiation of upland and lowland Picea mariana stands in northern Ontario. Silvae Genet. 34: 214–221.

    Google Scholar 

  • Pamilo, P. 1990. Statistical tests of phenograms based on genetic distances. Evolution 44: 689–697.

    Google Scholar 

  • Perry, D. J. and Knowles, P. 1989. Allozyme variation in sugar maple at the northern limit of its range in Ontario, Canada. Can. J. For. Res. 19: 509–514.

    Google Scholar 

  • Plessas, M. E. and Strauss, S. H. 1986. Allozyme differentiation among populations, stands, and cohorts in Monterey pine. Can. J. For. Res. 16: 1155–1164.

    Google Scholar 

  • Pollack, J. C. and Dancik, B. P. 1985. Monoterpene and morphological variation and hybridization of Pinus contorta and P. banksiana in Alberta. Can. J. For. Res. 63: 201–210.

    Google Scholar 

  • Price, R. A. and Lowenstein, J. M. 1989. An immunological comparison of the Sciadopityaceae, Taxodiaceae, and Cupressaceae. Syst. Bot. 14: 141–149.

    Google Scholar 

  • Price, R. A., Olsen-Stojkovich, J. and Lowenstein, J. M. 1987. Relationships among the genera of Pinaceae: an immunological comparison. Syst. Bot. 12: 91–97.

    Google Scholar 

  • Rajora, O. P. 1989. Genetic structure and identification of Populus deltoides clones based on allozymes. Genome 32: 440–448.

    Google Scholar 

  • Rajora, O. P. 1990. Marker allozyme genes and alleles for differentiation of Populus deltoides, P. nigra, P. maximowiczii, and their interspecific hybrids. Can. J. Bot. 68: 990–998.

    Google Scholar 

  • Rajora, O. P. and Zsuffa, L. 1989. Multilocus genetic structure, characterization, and relationships of Populus x canadensis cultivars. Genome 32: 99–108.

    Google Scholar 

  • Rehfeldt, J. 1984. Microevolution of conifers in the northern Rocky Mountains: a view from common gardens, pp. 132–146. In: Lanner, R. M. (Ed) Proc. 8th North American Forest Biology Workshop, Dept. of Forest Resources, Utah State Univ., Logan, UT.

    Google Scholar 

  • Ritland, K. and Clegg, M. T. 1987. Evolutionary analysis of plant DNA sequences. Am. Nat. 130: S74-S100.

    Google Scholar 

  • Rogers, J. S. 1972. Measures of genetic similarity and genetic distance, pp. 145–153. In: Studies in Genetics VII. Univ. of Texas Publication 7213. Austin, Texas.

    Google Scholar 

  • Rose, M. R. and Doolittle, W. F. 1983. Molecular biological mechanisms of speciation. Science 220: 157–162.

    Google Scholar 

  • Saitou, N. and Nei, M. 1987. The neighbor-joining method: a new method for constructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.

    Google Scholar 

  • Saitou, N. and Imanishi, T. 1989. Relative efficiencies of the Fitch-Margoliash, Maximum-Parsimony, Maximum-Likelihood, Minimum-Evolution, and Neighbor-joining methods of phylogenetic tree construction in obtaining the correct tree. Mol. Biol. Evol. 6: 514–525.

    Google Scholar 

  • Saylor, L. C. and Smith, B. W. 1966. Meiotic irregularity in species and interspecific hybrids of Pinus. Am. J. Bot. 53: 453–468.

    Google Scholar 

  • Schiller, G., Conkle, M. T. and Grunwald, C. 1986. Local differentiation among Mediterranean populations of Aleppo pine in their isoenzymes. Silvae Genet. 35: 11–19.

    Google Scholar 

  • Schmid, C. W. and Jelinek, W. R. 1982. The Alu family of dispersed repetitive sequences. Science 216: 1065–1070.

    Google Scholar 

  • Schnabel, A. and Hamrick, J. L. 1990. Comparative analysis of population genetic structure in Quercus macrocarpa and Q. gambeld (Fagaceae). Syst. Bot. 15: 240–251.

    Google Scholar 

  • Selander, R. K. and Whittam, T. S. 1983. Protein polymorphism and the genetic structure of populations, pp. 89–114. In: Nei, M. and Koehn, R. K. (Eds) Evolution of Genes and Proteins. Sinauer Associates, Inc. Publishers, Sundlander, Massachusetts.

    Google Scholar 

  • Sessions, S. K. and Larson, A. 1987. Developmental correlates of genome size in plethodontid salamanders and their implications for genome evolution. Evolution 41: 1239–1251.

    Google Scholar 

  • Sidow, A. and Wilson, A. C. 1990. Compositional statistics: an improvement of evolutionary parsimony and its application to deep branches in the tree of life. J. Mol. Evol. 31: 51–68.

    Google Scholar 

  • Sigurgeirsson, A. and Szmidt, A. 1988. Chloroplast DNA variation among North-American Picea species, and its phylogenetic implications, pp. 49–65. In: Proc. of the Frans Kempe Symposium, Umea, Sweden.

    Google Scholar 

  • Smith, R. H. 1977. Monoterpenes of ponderosa pine xylem resin in western United States. USDA For. Serv., Pacific Southwest Forest and Range Exp. Sta., Berkeley, California. Tech. Bull. 1532.

    Google Scholar 

  • Smouse, P. E. and Neel, J. V. 1977. Multivariate analysis of gametic disequilibrium in the Yanomama. Genetics 85: 733–752.

    Google Scholar 

  • Sneath, P. H. A. and Sokal, R. R. 1973. Numerical Taxonomy. W.H. Freeman, San Francisco.

    Google Scholar 

  • Sorensen, F. C., Campbell, R. K. and Franklin, J. F. 1990. Geographic variation in growth and phenology of seedlings of the Abies proceral A. magnifica complex. Forest Ecol. Manage. 36: 205–232.

    Google Scholar 

  • Sourdis, J. and Nei, M. 1988. Relative efficiencies of the Maximum Parsimony and Distance-Matrix methods in obtaining the correct phylogenetic tree. Mol. Biol. Evol. 5: 298–311.

    Google Scholar 

  • Steinhoff, R. J., Joyce, D. G. and Fins, L. 1983. Isozyme variation in Pinus monticola. Can. J. For. Res. 13: 1122–1132.

    Google Scholar 

  • Strauss, S. H. and Doerksen, A. H. 1990. Restriction fragment analysis of pine phylogeny. Evolution 44: 1081–1096.

    Google Scholar 

  • Strauss, S. H., Doerksen, A. H. and Byrne, J. R. 1990. Evolutionary relationships of Douglas-fir and its relatives (genus Pseudotsuga) from DNA restriction fragment analysis. Can. J. Bot. 68: 1052–1510.

    Google Scholar 

  • Strauss, S. H., Neale, D. B. and Wagner, D. B. 1989. Genetics of the chloroplast in conifers. J. Forestry 87: 11–17.

    Google Scholar 

  • Surles, S. E., Hamrick, J. L. and Bongarten, B. C. 1989. Allozyme variation in black locust (Robinia pseudoacacia). Can. J. For. Res. 19: 471–479.

    Google Scholar 

  • Swofford, D. L. 1990. PAUP-Phylogenetic analysis using parsimony. Illinois Natural History Survey, Champaign, IL.

    Google Scholar 

  • Sytsma, K. J. 1990. DNA and morphology: inference of plant phylogeny. Trends Ecol. Evol. 5: 104–110

    Google Scholar 

  • Sytsma, K. J. and Schaal, B. A. 1985a. Genetic variation, differentiation, and evolution in a species complex of tropical shrubs based on isozymic data. Evolution 39: 582–593.

    Google Scholar 

  • Sytsma, K. J. and Schaal, B. A. 1985b. Phylogenetics of the Lisianthius skinned (Gentianaceae) species complex in Panama utilizing DNA restriction fragment analysis. Evolution 39: 594–608.

    Google Scholar 

  • Szmidt, A. E., El-Kassaby, Y. A., Sigurgeirsson, A., Aldèn, T., Lindgren, D. and Hällgren, J.-E. 1988a. Classifying seedlots of Picea sitchensis and P. glauca in zones of introgression using restriction analysis of choloroplast DNA. Theor. Appl. Genet. 76: 841–845.

    Google Scholar 

  • Szmidt, A. E., Sigurgeirsson, A., Wang, X.-R., Hallgren, J. E. and Lindgren, D. 1988b. Genetic relationships among Pinus species based on chloroplast DNA polymorphism, pp. 33–47. In: Proc. of the Frans Kempe Symposium in Umea, Sweden.

    Google Scholar 

  • Tajima, F. and Nei, M. 1984. Estimation of evolutionary distance between nucleotide sequences. Mol. Biol. Evol. 1: 269–285.

    Google Scholar 

  • Thielges, B. A. 1969. A chromatographic investigation of interspecific relationships in Pinus (Subsection Sylvestres). Am. J. Bot. 56: 406–409.

    Google Scholar 

  • von Rudloff, E. and Lapp, M. S. 1987. Chemosystematic studies in the genus Pinus. VI. General survey of the leaf oil terpene composition in lodgepole pine. Can. J. For. Res. 17: 1013–1025.

    Google Scholar 

  • von Rudloff, E. and Rehfeldt, G. E. 1980. Chemosystematic studies in the genus Pseudotsuga. IV. Inheritance and geographical variation in the leaf oil terpenes of Douglas-fir from the Pacific Northwest. Can. J. Bot. 58: 546–556.

    Google Scholar 

  • Wagner, D. B. Furnier, G. R., Saghai-Maroof, M. A., Williams, S. M., Dancik, B. P. and Allard, R. W. 1987. Chloroplast DNA polymorphisms in lodgepole and jack pines and their hybrids. Proc. Natl. Acad. Sci. USA 84: 2097–2100.

    Google Scholar 

  • Wang, X.-R. and Szmidt, A. E. 1990. Evolutionary analysis of Pinus densata [Masters], a putative Tertiary hybrid. II. A study using species-specific chloroplast DNA markers. Theor. Appl. Genet. (in press).

  • Wang, X.-R., Szmidt, A. E., Lewandowski, A. and Wang, Z.-R. 1990. Evolutionary analysis of Pinus densata Masters, a putative Tertiary hybrid. 1. Allozyme variation. Theor. Appl. Genet. (in press).

  • Wanntorp, H.-E., Brooks, D. R., Nilsson, T., Nylin, S., Ronquist, F., Stearns, S. C. and Wedell, N. 1990. Phylogenetic approaches in ecology. Oikos 57: 119–132.

    Google Scholar 

  • Weber, J. C. and Stettler R. F. 1981. Isoenzyme variation among ten populations of Populus trichocarpa Torr. et Gray in the Pacific Northwest. Silvae Genet. 30: 82–87.

    Google Scholar 

  • Wellendorf, H. and Simonsen, V. 1979. A chemotaxonomic study in Picea with isoenzymes in the seed endosperm, pp. 182–197. In: Proceedings of the Conference on Biochemical Genetics of Forest Trees, Umea, Sweden.

    Google Scholar 

  • Wendel, J. F. and Parks, C. R. 1985. Genetic diversity and population structure in Camellia japonica L. (Theaceae). Am. J. Bot. 72: 52–65.

    Google Scholar 

  • Westfall, R D. 1992. Allozyme markers in breeding zone designation. This issue, pp. 279–300.

  • Wheeler, N. C. and Guries, R. P. 1982a. Population structure, genic diversity, and morphological variation in Pinus contorta Dougl. Can. J. For. Res. 12: 595–606.

    Google Scholar 

  • Wheeler, N. C. and Guries, R. P. 1982b. Biogeography of lodgepole pine. Can. J. Bot. 60: 1805–1814.

    Google Scholar 

  • Wheeler, N. C. and Guries, R. P. 1987. A quantitative measure of introgression between lodgepole and jack pines. Can. J. Bot. 65: 1876–1885.

    Google Scholar 

  • Wheeler, N. C., Guries, R. P. and O'Malley, D. M. 1983. Biosystematics of the genus Pinus, Subsection Contortae. Biochem. Syst. Ecol. 11: 333–340.

    Google Scholar 

  • Wiley, E. O. 1981. Phylogenetics: The Theory and Practice of Phylogenetic Systematics. John Wiley and Sons, New York, 305 pp.

    Google Scholar 

  • Williams, P. L. and Fitch, W. M. 1990. Phylogeny determination using dynamically weighted parsimony method. In: Doolittle, R. F. (Ed) Molecular Evolution: Computer Analysis of Protein and Nucleic Acid Sequences. Methods Enzymol. 183: 615–626.

  • Wilson, M. A., Gaut, B. and Clegg, M. T. 1990. Chloroplast DNA evolves slowly in the palm family (Arecaceae). Mol. Biol. Evol. 7: 303–314.

    Google Scholar 

  • Wu, C.-I. and Li, W.-H. 1985. Evidence for higher rates of nucleotide substitution in rodents than in man. Proc. Natl. Acad. Sci. USA. 82: 1741–1745.

    Google Scholar 

  • Yacine, A. and Lumaret, R. 1989. Genetic diversity in holm-oak (Querces ilex L.): insight from several enzyme markers. Silvae Genet. 38: 140–148.

    Google Scholar 

  • Yeh, F. C. 1988. Isozyme variation of Thuja plicata (Cupressaceae) in British Columbia. Biochem. Syst. Ecol. 16: 373–377.

    Google Scholar 

  • Yeh, F. C. and Arnott, J. T. 1986. Electrophoretic and morphological differentiation of Picea sitchensis, Picea glauca, and their hybrids. Can. J. For. Res. 16: 791–798.

    Google Scholar 

  • Yeh, F. C., Cheliak, W. M., Dancik, B. P., Illingworth, K., Trust, D. C. and Pryhitka, B. A. 1985. Population differentiation in lodgepole pine, Pinus contorta spp. latifolia: a discriminant analysis of allozyme variation. Can. J. Genet. Cytol. 27: 210–218.

    Google Scholar 

  • Yeh, F. C., Khalil, M. A. K., El-Kassaby, Y. A. and Trust, D. C. 1986. Allozyme variation in Picea mariana from Newfoundland: genetic diversity, population structure, and analysis of differentiation. Can. J. For. Res. 16: 713–720.

    Google Scholar 

  • Zavarin, E. and Snajberk, K. 1973. Geographic variability of monoterpenes from cortex of Pseudotsuga menziesii. Pure and Appl. Chem. 34: 411–434.

    Google Scholar 

  • Zimmer, E. A., Hamby, K. R., Arnold, M. L., Leblanc, D. A. and Theriot, E. C. 1989. Ribosomal RNA phylogenies and flowering plant evolution. In: Fernholm, B., Bremer, and Jörnvall, K. (Eds) The Hierarchy of Life. Elsevier, NY, pp. 205–214.

    Google Scholar 

  • Zinkel, D. F. 1977. Pine resin acids as chemotaxonomic and genetic indicators, pp. 53–56. In: TAPPI Conference Papers, Forest Biology Wood Chemistry Conference, Madison, WI.

    Google Scholar 

  • Zuckerkandl, E. 1986. Polite DNA: functional density and functional compatibility in genomes. J. Mol. Evol. 24: 12–27.

    Google Scholar 

  • Zuckerkandl, E. and Pauling, L. 1965. Molecules as documents of evolutionary history. J. Theor. Biol. 8: 357–366.

    Google Scholar 

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

    Google Scholar 

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This is paper 2708 of the Forest Research Laboratory, Oregon State University.

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Strauss, S.H., Bousquet, J., Hipkins, V.D. et al. Biochemical and molecular genetic markers in biosystematic studies of forest trees. New Forest 6, 125–158 (1992). https://doi.org/10.1007/BF00120642

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