Genetic evidence for hybridization in red oaks (Quercus sect. Lobatae, Fagaceae)

American Journal of Botany

Volumn 99, Issue 1, 2012, Pages 92-100

  Moran, Emily V ^b   Willis, John ^a   Clark, James S ^a  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Fagaceae; Gene flow; Genetic structure; Hybridization; Lobatae; Parentage; Quercus

Indexed keywords

ADULT; ALLELE; DECIDUOUS FOREST; DICOTYLEDON; ENVIRONMENTAL CHANGE; GENE FLOW; GENETIC ANALYSIS; GENETIC MARKER; GENETIC STRUCTURE; GENETIC VARIATION; HYBRIDIZATION; INTROGRESSION; LOCAL ADAPTATION; PARENTAGE; SEEDLING; TAXONOMY;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ARTICLE; GENE FLOW; GENETIC VARIABILITY; GENETICS; GENOTYPE; HISTOLOGY; HYBRIDIZATION; OAK; PHENOTYPE; PLANT GENOME; PLANT LEAF; POPULATION GENETICS; SEEDLING; SPECIES DIFFERENCE; TREE; UNITED STATES;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; GENE FLOW; GENETIC STRUCTURES; GENETICS, POPULATION; GENOME, PLANT; GENOTYPE; HYBRIDIZATION, GENETIC; NORTH CAROLINA; PHENOTYPE; PLANT LEAVES; QUERCUS; SEEDLING; SPECIES SPECIFICITY; TREES;

NORTH CAROLINA; UNITED STATES;

FAGACEAE; QUERCUS; QUERCUS RUBRA;

EID: 84858430878     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1100023     Document Type: Article

References (72)

1. Aldrich, P. R., M. Jagtap, C. H. Michler, and J. Romero-Severson. 2003a. Amplification of North American red oak microsatellite markers in European white oaks and Chinese chestnut. Silvae Genetica 52: 176-179.
2. Aldrich, P. R., C. H. Michler, W. Sun, and J. Romero-Severson. 2002. Microsatellite markers for northern red oak (Fagaceae: Quercus rubra). Molecular Ecology Notes 2: 472-474.
3. Aldrich, P. R., G. R. Parker, C. H. Michler, and J. Romeroseverson. 2003b. Whole-tree silvic identifications and the microsatellite genetic structure of a red oak species complex in an Indiana old-growth forest. Canadian Journal of Forest Research 33: 2228-2237.
4. Allendorf, F. W., R. F. Leary, P. Spruell, and J. K. Wenburg. 2001. The problem with hybrids: Setting conservation guidelines. Trends in Ecology & Evolution 16: 613-622.
5. Anderson, E. 1948. Hybridization of the habitat. Evolution 2: 1-19.
6. Arnold, M. L. 1992. Natural hybridization as an evolutionary process. Annual Review of Ecology, Evolution and Systematics 23: 237-261.
7. Ashley, M. V. 2010. Plant parentage, pollination, and dispersal: How DNA microsatellites have altered the landscape. Critical Reviews in Plant Sciences 29: 148-161.
8. Bacilieri, R., A. Ducousso, R. J. Petit, and A. Kremer. 1996. Mating system and asymmetric hybridization in a mixed stand of European oaks. Evolution 50: 900-908.
9. Boecklen, W. J., and R. Spellenberg. 1990. Structure of herbivore communities in two oak (Quercus spp.) hybrid zones. Oecologia 85: 92-100.
10. Burgarella, C., Z. Lorenzo, R. Jabbour-Zahab, R. Lumaret, E. Guichoux, R. J. Petit, A. Soto, and L. Gil. 2009. Detection of hybrids in nature: Application to oaks (Quercus suber and Q. ilex). Heredity 102: 442-452.
11. Burger, W. C. 1975. The species concept in Quercus. Taxon 24: 45-50.
12. Cavender-Bares, J., and A. Pahlich. 2009. Molecular, morphological and ecological niche differentiation of sympatric sister oak species, Quercus virginiana Miller and Q. geminata Small. American Journal of Botany 96: 1690-1702.
13. Chapuis, M.-P., and A. Estoup. 2007. Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24: 621-631.
14. Clark, J. S., D. Bell, C. Chu, B. Courbaud, M. Dietze, M. Hersh, J. Hille Ris Lambers, et al. 2010. High dimensional coexistence based on individual variation: A synthesis of evidence. Ecological Monographs 80: 569-608.
15. Clark, J. S., S. Ladeau, and I. Ibanez. 2004. Fecundity of trees and the colonization competition hypothesis. Ecological Monographs 74: 415-442.
16. Cottam, W. P., J. M. Tucker, and F. S. Santamour. 1982. Oak hybridization at the University of Utah. State Arboretum of Utah, Salt Lake City, Utah, USA.
17. Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer, Sunderland, Massachusetts, USA.
18. Craft, K. J., and M. V. Ashley. 2006. Population differentiation among three species of white oak in northeastern Illinois. Canadian Journal of Forest Research 36: 206-215.
19. Craft, K. J., and M. V. Ashley. 2007. Landscape genetic structure of bur oak (Quercus macrocarpa) savannas in Illinois. Forest Ecology and Management 239: 13-20.
20. Craft, K. J., M. V. Ashley, and W. D. Koenig. 2002. Limited hybridization between Quercus lobata and Quercus douglasii (Fagaceae) in a mixed stand in central coastal California. American Journal of Botany 89: 1792-1798.
21. Crawford, N. G. 2010. SMOGD: Software for the measurement of genetic diversity. Molecular Ecology Resources 10: 556-557.
22. Curtu, A. L., O. Gailing, and R. Finkeldey. 2007. Evidence for hybridization and introgression within a species-rich oak (Quercus spp.) community. BMC Evolutionary Biology 7: 218. doi:10.1186/1471-2148-7-218
23. Dodd, R. S., and Z. Afzal-Rafii. 2004. Selection and dispersal in a multispecies oak hybrid zone. Evolution 58: 261-269.
24. Ducousso, A., H. Michaud, and R. Lumaret. 1993. Reproduction and gene flow in the genus Quercus L. Annales des Sciences Forestieres 50: 91s-106s.
25. Elena-Rossello, J. A., I. R. Lumaretz, E. Cabrera, and H. Michaud. 1992. Evidence for hybridization between sympatric holm-oak and cork-oak in Spain based on diagnostic enzyme markers. Vegetatio 99-100: 115-118.
26. González-Rodríguez, A., D. M. Arias, S. Valencia, and K. Oyama. 2004. Morphological and RAPD analysis of hybridization between Quercus affinis and Q. laurina (Fagaceae), two Mexican red oaks. American Journal of Botany 91: 401-409.
27. Gregorius, H., B. Degen, and A. Konig. 2007. Problems in the analysis of genetic differentiation among populations - A case study in Quercus robur. Silvae Genetica 56: 190-199.
28. Guttman, S. I., and L. A. Weigt. 1989. Electophoretic evidence of relationships among Quercus (oaks) of eastern North America. Canadian Journal of Botany 67: 339-351.
29. Hedrick, P. 1999. Highly variable loci and their interpretation in evolution and conservation. Evolution 53: 313-318.
30. Hedrick, P. 2005. A standardized genetic differentiation measure. Evolution 59: 1633-1638.
31. HIPP, A. L., and J. A. Weber. 2008. Taxonomy of Hill's oak (Quercus ellipsoidalis: Fagaceae): Evidence from AFLP data. Systematic Botany 33: 148-158.
32. Ibáñez, I., J. S. Clark, S. Ladeau, and J. H. R. Lambers. 2007. Exploiting temporal variability to understand tree recruitment response to climate change. Ecological Monographs 77: 163-177.
33. IPCC [INTERGOVERNMENTAL PANEL ON CLIMATE CHANGE]. 2007. Summary for policymakers. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor, and H. L. Miller [eds.]. In IPCC Fourth Assessment Report, Climatic change 2007: The physical science basis. Available at http://www.ipcc.ch/pdf/assessment-report/ar4/wg1/ar4-wg1-spm.pdf. Cambridge University Press, New York, New York, USA.
34. Jakobsson, M., and N. A. Rosenberg. 2007. Clumpp: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23: 1801-1806.
35. Jensen, R. J. 1977. A preliminary numerical analysis of the red oak complex in Michigan and Wisconsin. Taxon 26: 399-407.
36. Jones, F. A., J. L. Hamrick, C. J. Peterson, and E. R. Squiers. 2006. Inferring colonization history from analyses of spatial genetic structure within populations of Pinus strobus and Quercus rubra. Molecular Ecology 15: 851-861.
37. ST and its relatives do not measure differentiation. Molecular Ecology 17: 4015-4026.
38. Kashani, N., and R. S. Dodd. 2002. Genetic differentiation of two California red oak species, Quercus parvula var. shreveii and Q. wislizeni, based on AFLP genetic markers. In R. B. Standiford et al. [eds.], Oaks in California's changing landscape, 417-426. Gen. Tech. Rep. PSW-GTR-184, Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture, Albany, California, USA. Available at http://www.treesearch.fs.fed.us/pubs/26142.
39. Kimball, S., D. R. Campbell, and C. Lessin. 2008. Differential performance of reciprocal hybrids in multiple environments. Journal of Ecology 96: 1306-1318.
40. Little, E. L. 1980. National Audubon Society field guide to trees, eastern region. Alfred A. Knopf, New York, New York, USA.
41. Lorenzo, Z., C. Burgarella, U. López de Heredia, R. Lumaret, R. J. Petit, A. Soto, and L. Gil. 2009. Relevance of genetics for conservation policies: The case of Minorcan cork oaks. Annals of Botany 104: 1069-1076.
42. Manos, P. S., and A. M. Stanford. 2001. The historical biogeography of Fagaceae: Tracking the tertiary history of temperate and subtropical forests of the Northern Hemisphere. International Journal of Plant Sciences 162: S77-S93.
43. Mimura, M., and S. N. Aitken. 2010. Local adaptation at range peripheries in Sitka spruce. Journal of Evolutionary Biology 23: 249-258.
44. Moran, E. V., and J. S. Clark. 2011. Estimating seed and pollen movement in a monoecious plant: A hierarchical Bayesian approach integrating genetic and ecological data. Molecular Ecology 20: 1248-1262.
45. Morand, M. E., S. Brachet, P. Rossignol, J. Dufour, and N. Frascaria-Lacoste. 2002. A generalized heterozygote deficiency assessed with microsatellites in French common ash populations. Molecular Biology 11: 377-385.
46. Muir, G., and C. Schlotterer. 2005. Evidence for shared ancestral polymorphism rather than recurrent gene flow at microsatellite loci differentiating two hybridizing oaks (Quercus spp.). Molecular Ecology 14: 549-561.
47. Muller, C. H. 1952. Ecological control of hybridization in Quercus: A factor in the mechanism of evolution. Evolution 6: 147-161.
48. Nei, M. 1973. Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences, USA 70: 3321-3323.
49. Nixon, K. C. 2006. Global and neotropical distribution and diversity of oak (genus Quercus) and oak forests. In M. Kappelle [ed.], Ecology and conservation of neotropical montane oak forests. Springer-Verlag, Berlin, Germany.
50. Oh, S. H., and P. S. Manos. 2008. Molecular phylogenetics and cupule evolution in Fagaceae as inferred from nuclear CRABS CLAW sequences. Taxon 57: 434-451.
51. PALMER, E. J. 1942. The red oak complex in the United States. American Midland Naturalist 27: 732-740.
52. Peakall, R., and P. E. Smouse. 2006. Genalex 6: Genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288-295.
53. Peñalóza-Ramírez, J. M., A. González-Rodríguez, L. Mendozacuenca, H. Caron, A. Kremer, and K. Oyama. 2010. Interspecific gene flow in a multispecies oak hybrid zone in the Sierra Tarahumara of Mexico. Annals of Botany 105: 389-399.
54. Petit, R. J., C. Bodenes, A. Ducousso, G. Roussel, and A. Kremer. 2003. Hybridization as a mechanism of invasion in oaks. New Phytologist 161: 151-164.
55. Pritchard, J. K., M. Stephens, and P. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
56. Rieseberg, L. H., and J. H. Willis. 2007. Plant speciation. Science 317: 910-914.
57. Rosenberg, N. A. 2004. Distruct: A program for the graphical display of population structure. Molecular Ecology Notes 4: 137-138.
58. Rushton, B. S. 1993. Natural hybridization within the genus Quercus L. Annales des Sciences Forestieres 50: 73s-90s.
59. Salvini, D., P. Bruschi, S. Fineschi, P. Grossoni, E. D. Kjaer, and G. G. Vendramin. 2009. Natural hybridization between Quercus petraea (Matt.) Liebl. and Quercus pubescens Willd. within an Italian stand as revealed by microsatellite fingerprinting. Plant Biology 11: 758-765.
60. Sato, T., Y. Isagi, H. Sakio, K. O Sumi, and S. Goto. 2006. Effect of gene flow on spatial genetic structure in the riparian canopy tree Cercidiphyllum japonicum revealed by microsatellite analysis. Heredity 96: 79-84.
61. Schwarzmann, J. F., and H. D. Gerhold. 1991. Genetic structure and mating system of northern red oak (Quercus rubra L.) in Pennsylvania. Forest Science 37: 1376-1389.
62. Slatkin, M. 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139: 1463.
63. Streiff, R., A. Ducousso, C. Lexer, H. Steinkellner, J. Gloessl, and A. Kremer. 1999. Pollen dispersal inferred from paternity analysis in a mixed oak stand of Quercus robur L. and Q. petraea (Matt.) Liebl. Molecular Ecology 8: 831-841.
64. Tomlinson, P. T., R. J. Jensen, and J. F. Hancock. 2000. Do whole tree silvic characters indicate hybridization in red oak (Quercus section Lobatae)? American Midland Naturalist 143: 154-168.
65. Tovar-Sánchez, E., and K. Oyama. 2004. Natural hybridization and hybrid zones between Quercus crassifolia and Quercus crassipes (Fagaceae) in Mexico: Morphological and molecular evidence. American Journal of Botany 91: 1352-1363.
66. Valbuena-Carabana, M., S. C. González-Martínez, O. J. Hardy, and L. Gil. 2007. Fine-scale spatial genetic structure in mixed oak stands with different levels of hybridization. Molecular Ecology 16: 1207-1219.
67. Weir, B. S. 1996. Genetic data analysis II. Sinauer, Sunderland, Massachusetts, USA.
68. Weir, B. S., and C. C. Cockerham. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
69. Whitham, T. G., P. A. Morrow, and B. M. Potts. 1994. Plant hybrid zones as centers of biodiversity: The herbivore community of two endemic Tasmanian eucalypts. Oecologia 97: 481-490.
70. Whittemore, A. T., and B. A. Schaal. 1991. Interspecific gene flow in sympatric oaks. Proceedings of the National Academy of Sciences, USA 88: 2540-2544.
71. Williams, J. H., W. J. Boecklen, and D. J. Howard. 2001. Reproductive processes in two oak (Quercus) contact zones with different levels of hybridization. Heredity 87: 680-690.
72. Wright, S. 1949. The genetical structure of populations. Annals of Eugenics 15: 323-354.