European Journal of Forest Research

, Volume 134, Issue 1, pp 139–151 | Cite as

Leaf morphological evidence of natural hybridization between two oak species (Quercusaustrocochinchinensis and Q. kerrii) and its implications for conservation management

  • Yigang Song
  • Min Deng
  • Andrew L. Hipp
  • Qiansheng Li
Original Paper

Abstract

Natural hybridization is known to be a potential threat to rare and endangered species due to the risk of extensive genetic swamping or assimilation. However, hybridization may also beneficial for rare species by increasing their genetic variation and adaptive potential. Quercus austrocochinchinensis is an endangered oak species that overlaps geographically with the common, widespread Q. kerrii. Morphological intermediates are common in contact zones between the species, suggesting interspecific hybridization. This phenomenon may lead to pure Q. austrocochinchinensis facing a larger threat. Given the importance of leaf morphology for hybrid identification in oaks, we characterized leaf morphological and anatomical features of pure populations of Q. kerrii and Q. austrocochinchinensis and a population of probable hybrids at the contact zone. The results demonstrate that (1) leaf morphological features of putative hybrids are stable and distinct from the parental taxa, and more similar to those of Q. kerrii; (2) anticlinal wall patterns of abaxial epidermal cells show the most significant differences between parental species and probable hybrids, providing an important character for species identification; and (3) putative hybrids were intermediate in leaf anatomical features between the two parental species. The leaf traits for identified Q. austrocochinchinensis, Q. kerrii and hybrids can be used to estimate the hybridization ratio at the contact zone. The morphological evidence, sympatry and phenology strongly suggest that the rare Q. austrocochinchinensis forms hybrids with the more widespread Q. kerrii. Natural hybridization might play an important future role in both migration and adaptation of the species to novel environments. Thus, the characters we identify here for diagnosing hybrids provide an important tool for conserving species and genetic diversity. We suggest that a management plan for Q. austrocochinchinensis should address the conservation of both of the pure species, investigation of gene flow dynamics in the hybrid zone and investigation of the impacts of gene flow on fitness of the two species.

Keywords

Conservation Endangered species Hybrid zone Leaf epidermis Leaf morphological variation 

Supplementary material

10342_2014_839_MOESM1_ESM.doc (30 kb)
Supplementary material 1 (DOC 29 kb)

References

  1. Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with image. Biophotonics Int 11:36–42Google Scholar
  2. Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622. doi:10.1016/S0169-5347(01)02290-X CrossRefGoogle Scholar
  3. Arnold ML (1992) Natural hybridization as an evolutionary process. Annu Rev Ecol Syst 23:237–261. doi:10.1146/annurev.es.23.110192.001321 CrossRefGoogle Scholar
  4. Arnold ML, Ballerini ES, Brothers AN (2012) Hybrid fitness, adaptation and evolutionary diversification: lessons learned from Louisiana Irises. Heredity 108:159–166. doi:10.1038/hdy.2011.65 PubMedCentralPubMedCrossRefGoogle Scholar
  5. Bacilieri R, Ducousso A, Kremer A (1996) Comparison of morphological characters and molecular markers for the analysis of hybridization in sessile and pedunculate oak. Ann For Sci 53:79–91. doi:10.1051/forest:19960106 CrossRefGoogle Scholar
  6. Barton NH (2001) The role of hybridization in evolution. Mol Ecol 10:551–568. doi:10.1046/j.1365-294x.2001.01216.x PubMedCrossRefGoogle Scholar
  7. Barton NH, Hewitt GM (1989) Adaptation, speciation, and hybrid zones. Nature 341:497–503. doi:10.1038/341497a0 PubMedCrossRefGoogle Scholar
  8. Burgess KS, Morgan M, Deverno L, Husband BC (2005) Asymmetrical introgression between two Morus species (M. alba, M. rubra) that differ in abundance. Mol Ecol 14:3471–3483. doi:10.1111/j.1365-294X.2005.02670.x PubMedCrossRefGoogle Scholar
  9. Bussotti F, Grossoni P (1997) European and Mediterranean oaks (Quercus L.; Fagaceae): SEM characterization of the micromorphology of the abaxial leaf surface. Bot J Linn Soc 124:183–199. doi:10.1111/j.1095-8339.1997.tb01789.x Google Scholar
  10. Carney SE, Gardner KA, Rieseberg LH (2000) Evolutionary changes over the fifty-year history of a hybrid population of sunflowers (Helianthus). Evolution 54:462–474. doi:10.1111/j.0014-3820.2000.tb00049.x PubMedCrossRefGoogle Scholar
  11. Cavender-Bares J, Pahlich A (2009) Molecular, morphological, and ecological niche differentiation of sympatric sister oak species, Quercus virginiana and Q. geminata (Fagaceae). Am J Bot 96:1690–1702. doi:10.3732/ajb.0800315 PubMedCrossRefGoogle Scholar
  12. Cozzolino S, Nardella AM, Impagliazzo S, Widmer A, Lexer C (2006) Hybridization and conservation of Mediterranean orchids: should we protect the orchid hybrids or the orchid hybrid zones? Biol Conserv 129:14–23. doi:10.1016/j.biocom.2005.09.043 CrossRefGoogle Scholar
  13. Craft KJ, Ashley MV, Koenig WD (2002) Limited hybridization between Quercus lobata and Quercus douglasii (Fagaceae) in a mixed stand in central coastal California. Am J Bot 89:1792–1798. doi:10.3732/ajb.89.11.1792 PubMedCrossRefGoogle Scholar
  14. de Heredia UL, Valbuena-Carabana M, Cordoba M, Gil L (2009) Variation components in leaf morphology of recruits of two hybridising oaks [Q. petraea (Matt.) Liebl. and Q. pyrenaica Willd.] at small spatial scale. Eur J For Res 128:543–554. doi:10.1007/s10342-009-0302-6 CrossRefGoogle Scholar
  15. Deng M (2007) Anatomy, taxonomy, distribution and phylogeny of Quercus subg. Cyclobalanopsis (Oersted) Schneid. (Fagaceae). Ph.D. dissertation, Graduate School of Chinese Academy of SciencesGoogle Scholar
  16. Deng M, Zhou ZK, Li QS (2013) Taxonomy and systematics of Quercus subgenus Cyclobalanopsis. Int Oaks 24:48–60Google Scholar
  17. Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Ann Rev Ecol Syst 24:217–242. doi:10.1146/annurev.es.24.110193.001245 CrossRefGoogle Scholar
  18. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050. doi:10.1073/pnas.97.13.7043 PubMedCentralPubMedCrossRefGoogle Scholar
  19. Estabrook GF, Gilad NL, Reznicek AA (1996) Hypothesizing hybrids and parents using character intermediacy, parental distance, and equality. Taxon 45:647–662. doi:10.2307/1224249 CrossRefGoogle Scholar
  20. Gitzendanner MA, Soltis PM (2000) Patterns of genetic variation in rare and widespread plant congeners. Am J Bot 87:783–792. doi:10.2307/2656886 PubMedCrossRefGoogle Scholar
  21. Gonzalez-Rodriguez A, Oyama K (2005) Leaf morphometric variation in Quercus affinis and Q. laurina (Fagaceae), two hybridizing Mexican red oaks. Bot J Linn Soc 147:427–435. doi:10.1111/j.1095-8339.2004.00394.x CrossRefGoogle Scholar
  22. Gonzalez-Rodriguez A, Arias DM, Valencia S, Oyama K (2004) Morphological and RAPD analysis of hybridization between Quercus affinis and Q. laurina (Fagaceae), two Mexican red oaks. Am J Bot 91:401–409. doi:10.3732/ajb.91.3.401 PubMedCrossRefGoogle Scholar
  23. Gottlieb L (1972) Leaves of confidence in the analysis of hybridization in plants. Ann Mo Bot Gard 59:435–446. doi:10.2307/2395153 CrossRefGoogle Scholar
  24. Hardin JW (1975) Hybridization and introgression in Quercus alba. J Arnold Arbor 56:336–363Google Scholar
  25. Harrison RG (1993) Hybrids and hybrid zones: historical perspective. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, Oxford, pp 3–12Google Scholar
  26. Hedrick PW (2004) Recent developments in conservation genetics. For Ecol Manag 197:3–19. doi:10.1016/j.foreco.2004.05.002 CrossRefGoogle Scholar
  27. Hipp AL, Weber JA (2008) Taxonomy of Hill’s oak (Quercus ellipsoidalis: Fagaceae): evidence from AFLP data. Syst Bot 33:148–158. doi:10.1600/036364408783887320 CrossRefGoogle Scholar
  28. Hokanson SC, Isebrands JG, Jensen RJ, Hancock JF (1993) Isozyme variation in oaks of the Apostle Islands in Wisconsin: genetic structure and levels of inbreeding in Quercus rubra and Q. ellipsoidalis (Fagaceae). Am J Bot 80:1349–1357. doi:10.2307/2445720 CrossRefGoogle Scholar
  29. Howard DJ, Preszler RW, Williams J, Fenchel S, Boecklen WJ (1997) How discrete are oak species? Insights from a hybrid zone between Quercus grisea and Quercus gambelii. Evolution 51:747–755. doi:10.2307/2411151 CrossRefGoogle Scholar
  30. Huang CJ, Chang YT, Bartholomew B (1999) Flora of China, Fagaceae. Science Press and Missouri Botanical Garden Press, Beijing and Missouri, Beijing and St. LouisGoogle Scholar
  31. Ishida TA, Hattori K, Sato H, Kimura MT (2003) Differentiation and hybridization between Quercus crispula and Q. dentata (Fagaceae): insights from morphological traits, amplified fragment length polymorphism markers, and leafminer composition. Am J Bot 90:769–776. doi:10.3732/ajb.90.5.769 PubMedCrossRefGoogle Scholar
  32. Jensen RJ (1977) A preliminary numerical analysis of the red oak complex in Michigan and Wisconsin. Taxon 26:399–407. doi:10.2307/1220040 CrossRefGoogle Scholar
  33. Jensen RJ (1990) Detecting shape variation in oak leaf morphology: a comparison of Rotational-Fit methods. Am J Bot 77:1279–1293. doi:10.2307/2444589 CrossRefGoogle Scholar
  34. Jensen RJ, Depiero R, Smith BK (1984) Vegetative characters, population variation and the hybrid origin of Quercus ellipsoidalis. Am Midl Nat 111:364–370. doi:10.2307/2425331 CrossRefGoogle Scholar
  35. Jensen RJ, Hokanson SC, Isebrands JG, Hancock JF (1993) Morphometric variation in oaks of the Apostle Islands in Wisconsin: evidence of hybridization between Quercus rubra and Q. ellipsoidalis (Fagaceae). Am J Bot 80:1358–1366. doi:10.2307/2445721 CrossRefGoogle Scholar
  36. Jones JH (1986) Evolution of the Fagaceae: the implications of foliar features. Ann Mo Bot Gard 73:228–275. doi:10.2307/2399112 CrossRefGoogle Scholar
  37. Kelleher CT, Hodkinson TR, Douglas GC, Kelly DL (2005) Species distinction in Irish populations of Quercus petraea and Q. robur: morphological versus molecular analyses. Ann Bot 96:1237–1246. doi:10.1093/aob/mci275 PubMedCentralPubMedCrossRefGoogle Scholar
  38. Kleinschmit JR, Bacilieri GR, Kremer A, Roloff A (1995) Comparison of morphological and genetic traits of pedunculate oak (Q. robur L.) and sessile oak (Q. petraea (Matt.) Liebl.). Silvae Genet 44:256–269Google Scholar
  39. Kremer A, Dupouey JL, Deans JD et al (2002) Leaf morphological differentiation between Quercus robur and Quercus petraea is stable across western European mixed oak stands. Ann For Sci 59:777–787. doi:10.1051/forest:2002065 CrossRefGoogle Scholar
  40. Lexer C, Kremer A, Petit RJ (2006) Shared alleles in sympatric oaks: recurrent gene flow is a more parsimonious explanation than ancestral polymorphism. Mol Ecol 15:2007–2012. doi:10.1111/j.1365-294X.2006.02896.x PubMedCrossRefGoogle Scholar
  41. Liu WJ, Li QJ, Zhang GM et al (2000) The microclimatic differences between and within canopy gaps in the dry-hot season in Shorea chinensis forest. Acta Ecol Sin 20:932–937Google Scholar
  42. Llamas F, Perez-Morales C, Acedo C, Penas A (1995) Foliar trichomes of the evergreen and semi-deciduous species of the genus Quercus (Fagaceae) in the Iberian Peninsula. Bot J Linn Soc 117:47–57Google Scholar
  43. Long WX, Ding Y, Zang RG et al (2011) Environmental characteristics of tropical cloud forests in the rainy season in Bawangling National Nature Reserve on Hainan Island, South China. Chin J Plant Ecol 35:137–146CrossRefGoogle Scholar
  44. Lopez-Pujol J, Garcia-Jacas N, Susanna A, Vilatersana R (2012) Should we conserve pure species or hybrid species? Delimiting hybridization and introgression in the Iberian endemic Centaurea podospermifolia. Biol Conserv 152:271–279. doi:10.1016/j.biocon.2012.03.032 CrossRefGoogle Scholar
  45. Luo Y, Zhou ZK (2001) Leaf epidermis of Quercus subgen. Cyclobalanopsis (Oerst.) Schneid. (Fagaceae). J Syts Evol 39:489–501Google Scholar
  46. Mallet J (2007) Hybrid speciation. Nature 446:279–283. doi:10.1038/nature05706 PubMedCrossRefGoogle Scholar
  47. Marques I, Rosselló-Graell A, Draper D, Iriondo JM (2007) Pollination patterns limit hybridization between two sympatric species of Narcissus (Amaryllidaceae). Am J Bot 94:1352–1359. doi:10.3732/ajb.94.8.1352 PubMedCrossRefGoogle Scholar
  48. McKenzie RJ, Ward JM, Lovis JD, Breitwieser I (2004) Morphological evidence for natural intergeneric hybridization in the New Zealand Gnaphalieae (Compositae): Anaphalioides bellidioides × Ewartia sinclairii. Bot J Linn Soc 145:59–75. doi:10.1111/j.1095-8339.2003.00282.x CrossRefGoogle Scholar
  49. Muller CH (1952) Ecological control of hybridization in Quercus: a factor in the mechanism of evolution. Evolution 6:147–161. doi:10.2307/2405620 CrossRefGoogle Scholar
  50. Neophytou C, Aravanopoulos FA, Fink S, Dounavi A (2011) Interfertile oaks in an island environment. II. Limited hybridization between Quercus alnifolia Poech and Q. coccifera L. in a mixed stand. Eur J For Res 130:623–635. doi:10.1007/s10342-010-0454-4 CrossRefGoogle Scholar
  51. Penaloza-Ramirez JM, Gonzalez-Rodriguez A, Mendoza-Cuenca L, Caron H, Kremer A, Oyama K (2010) Interspecific gene flow in a multispecies oak hybrid zone in the Sierra Tarahumara of Mexico. Ann Bot 105:389–399. doi:10.1093/aob/mcp301 PubMedCentralPubMedCrossRefGoogle Scholar
  52. Peterson CA, Fetcher N, McGraw JB, Bennington CC (2012) Clinal variation in stomatal characteristics of an arctic sedge, Eriophorum vaginatum (Cyperaceae). Am J Bot 99:1562–1571. doi:10.3732/ajb.1100508 PubMedCrossRefGoogle Scholar
  53. Pu CX, Zhou ZK, Luo Y (2002) A cladistic analysis of Quercus (Fagaceae) in China based on leaf epidermis and architecture. Acta Bot Yunnan 24:689–698Google Scholar
  54. Rasband WS (1997–2012) ImageJ, US National Institutes of Health, Bethesda, MD, USA. http://imagej.nih.gov/ij/
  55. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Ann Rev Ecol Syst 27:83–109. doi:10.1146/annurev.ecolsys.27.1.83 CrossRefGoogle Scholar
  56. Rieseberg LH, Ellstrand NC (1993) What can molecular and morphological markers tell us about plant hybridization? Crit Rev Plant Sci 12:213–241. doi:10.1080/713608045 Google Scholar
  57. Rieseberg LH, Willis JH (2007) Plant speciation. Science 317:910–914. doi:10.1126/science.1137729 PubMedCentralPubMedCrossRefGoogle Scholar
  58. Rieseberg LH, Archer MA, Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity 83:363–372. doi:10.1038/sj.hdy.6886170 PubMedCrossRefGoogle Scholar
  59. Rushton BS (1993) Natural hybridization within the genus Quercus L. Ann For Sci 50:73–90CrossRefGoogle Scholar
  60. Scareli-Santos C, Herrera-Arroyo ML, Sanchez-Mondragon ML, Gonzalez-Rodriguez A, Bacon J, Oyama K (2007) Comparative analysis of micromorphological characters in two distantly related Mexican oaks, Quercus conzattii and Q. eduardii (Fagaceae), and their hybrids. Brittonia 59:37–48. doi:10.1663/0007-196X(2007)59[37:CAOMCI]2.0.CO;2
  61. Schwarzbach AE, Donovan LA, Rieseberg LH (2001) Transgressive character expression in a hybrid sunflower species. Am J Bot 88:270–277. doi:10.2307/2657018 PubMedCrossRefGoogle Scholar
  62. Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207. doi:10.1016/j.tree.2004.01.003 PubMedCrossRefGoogle Scholar
  63. Spellenberg R, Bacon JR (1996) Taxonomy and distribution of a natural group of black oaks of Mexico (Quercus, Section Lobatae, Subsection Racemiflorae). Syst Bot 21:85–99. doi:10.2307/2419565 CrossRefGoogle Scholar
  64. Stebbins GL, Matzke EB, Epling C (1947) Hybridization in a population of Quercus marilandica and Quercus ilicifolia. Evolution 1:79–88. doi:10.2307/2405406 CrossRefGoogle Scholar
  65. Thompson JD, Gaudeul M, Debussche M (2010) Conservation value of sites of hybridization in peripheral populations of rare plant species. Conserv Biol 24:236–245. doi:10.1111/j.1523-1739.2009.01304.x PubMedCrossRefGoogle Scholar
  66. Tomlinson PT, Jensen RJ, Hancock JF (2000) Do whole tree silvic characters indicate hybridization in red oak (Quercus Section Lobatae)? Am Midl Nat 143:154–168. doi:10.1674/0003-0031(2000)143[0154:DWTSCI]2.0.CO;2
  67. Tovar-Sanchez E, Oyama K (2004) Natural hybridization and hybrid zones between Quercus crassifolia and Quercus crassipes (Fagaceae) in Mexico: morphological and molecular evidence. Am J Bot 91:1352–1363. doi:10.3732/ajb.91.9.1352 PubMedCrossRefGoogle Scholar
  68. Tucker JM, Cottam WP, Drobnick R (1961) Studies in the Quercus undulata complex. II. The contribution of Quercus turbinella. Am J Bot 48:329–339CrossRefGoogle Scholar
  69. Wang S, Xie Y (2004) China species red list. Higher Education Press, Beijing, p 313Google Scholar
  70. Whittemore AT, Schaal BA (1991) Interspecific gene flow in sympatric oaks. Pro Natl Acad Sci USA 88:2540–2544. doi:10.1073/pnas.88.6.2540 CrossRefGoogle Scholar
  71. Wiegand KM (1935) A taxonomist’s experience with hybrids in the wild. Science 81:161–166. doi:10.1126/science.81.2094.161 PubMedCrossRefGoogle Scholar
  72. Woodward FI, Lake JA, Quick WP (2002) Stomatal development and CO2: ecological consequences. New Phytol 153:477–484. doi:10.1046/j.0028-646X.2001.00338.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Yigang Song
    • 1
  • Min Deng
    • 1
  • Andrew L. Hipp
    • 2
  • Qiansheng Li
    • 3
  1. 1.Shanghai Chenshan Plant Science Research CenterChinese Academy of Sciences/Shanghai Chenshan Botanical GardenShanghaiChina
  2. 2.The Morton ArboretumLisleUSA
  3. 3.School of EcologyShanghai Institute of TechnologyShanghaiChina

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