Journal of Forestry Research

, Volume 30, Issue 4, pp 1311–1322 | Cite as

Environmental contribution to needle variation among natural populations of Pinus tabuliformis

  • Jingxiang Meng
  • Xinyu Chen
  • Yujie Huang
  • Liming Wang
  • Fangqian Xing
  • Yue LiEmail author
Original Paper


Variations in the phenotypic characteristics of conifer needles is a consequence of genetic evolution that has been widely used in geographic variation and ecological studies. Although many studies are based on an in situ sampling strategy and generally realize the contribution of environmental effects to variation in needle traits, it is still uncertain which needle traits are most influenced by genetic effects and which are most influenced by the environment. Using both a common garden experiment to eliminate environmental heterogeneity and an in situ sampling strategy, we compared 18 Pinus tabuliformis needle traits among 10 geographical populations. Using both sampling strategies, we found significant differences in needle traits among populations and among individuals within populations. Differences in the “among-population” variance component between the two sampling strategies revealed the environmental contribution among natural populations for each trait. The among-population variance in the following traits exceeded 8%: needle length, number of stomata within 2 mm (NS2), number of stomatal lines on the planar side, number of resin canals (RCN) and the resin canal area (RCA). For the stability of needle traits, NS2, RCN, RCA, ratio of the vascular bundle area to the RCA (VBA/RCA), and MA/RCA differed significantly in more than five provenance changes between the common garden populations and natural populations, which may be susceptible to environmental effects. Conversely, the cross-sectional area, mesophyll area (MA), MA/(VBA + RCA), and MA/VBA were phenotypically stable. Geographic variation patterns and systematic relation of needle traits differed between the two sampling strategies, suggesting that in situ sampling results may reflect environmental effects and deviate statistical parameters for genetic study. Future studies of genetic evolution in the context of geographic variation should be based on appropriate sampling strategies and stable phenotypic traits.


Environmental effect Genetic variation Geographical variation In situ sampling Needle traits Pinus tabuliformis 



We thank Xiaoru Wang (Professor in Umeå university, Sweden) for her valuable edits.

Supplementary material

11676_2018_722_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 16 kb)


  1. Androsiuk P, Kaczmarek Z, Urbaniak L (2011) The morphological traits of needles as markers of geographical differentiation in European Pinus sylvestris populations. Dendrobiology 65:3–6Google Scholar
  2. Bobowicz MA, Korczyk AF (1994) Interpopulational variability of Pinus sylvestris L. in eight Polish localities expressed in morphological and anatomical traits of needles. Acta Soc Bot Pol 63(1):67–76Google Scholar
  3. Bobowicz M, Krzakowa M (1986) Anatomical differences between Pinus mugo Turra populations from the Tatra Mts., expressed in needle traits and in needle and cone traits together. Acta Soc Bot Pol 55:275–290Google Scholar
  4. Boratyńska K, Bobowicz M (2001) Pinus uncinata Ramond taxonomy based on needle characters. Plant Syst Evol 227(3):183–194Google Scholar
  5. Boratyńska K, Boratyński A (2007) Taxonomic differences among closely related pines Pinus sylvestris, P. mugo, P. uncinata, P. rotundata and P. uliginosa as revealed in needle sclerenchyma cells. Flora Morphol Distrib Funct Ecol Plants 202(7):555–569Google Scholar
  6. Boratyńska K, Jasińska AK, Boratyński A (2015) Taxonomic and geographic differentiation of Pinus mugo complex on the needle characteristics. Syst Biodivers 13(6):581–595Google Scholar
  7. Chazot N, Panara S, Zilbermann N, Blandin P, Le Poul Y, Cornette R, Elias M, Debat V (2016) Morpho morphometrics: shared ancestry and selection drive the evolution of wing size and shape in Morpho butterflies. Evolution 70(1):181–194Google Scholar
  8. Chen K, Abbott RJ, Milne RI, Tian XM, Liu J (2008) Phylogeography of Pinus tabulaeformis Carr. (Pinaceae), a dominant species of coniferous forest in northern China. Mol Ecol 17(19):4276–4288Google Scholar
  9. Cole KL, Fisher J, Arundel ST, Cannella J, Swift S (2008) Geographical and climatic limits of needle types of one-and two-needled pinyon pines. J Biogeogr 35(2):257–269Google Scholar
  10. Deckert RJ, Hsiang T, Peterson RL (2002) Genetic relationships of endophytic Lophodermium nitens isolates from needles of Pinus strobus. Mycol Res 106(3):305–313Google Scholar
  11. Ding ST, Wu JY, Chen JL, Yang Y, Yan DF, Sun BN (2013) Needles and seed cones of Pinus premassoniana sp. nov., and associated pollen cone from the upper Miocene in East China. Rev Palaeobot Palynol 197:78–89Google Scholar
  12. Donnelly K, Cavers S, Cottrell JE, Ennos RA (2016) Genetic variation for needle traits in Scots pine (Pinus sylvestris L.). Tree Genet Genomes 12(3):1–10Google Scholar
  13. Du QZ, Xu BH, Gong CR, Yang XH, Pan W, Tian JX, Li BL, Zhang DQ (2014) Variation in growth, leaf, and wood property traits of Chinese white poplar (Populus tomentosa), a major industrial tree species in Northern China. Can J For Res 44(4):326–339Google Scholar
  14. Eguchi N, Fukatsu E, Funada R, Tobita H, Kitao M, Maruyama Y, Koike T (2004) Changes in morphology, anatomy, and photosynthetic capacity of needles of Japanese larch (Larix kaempferi) seedlings grown in high CO2 concentrations. Photosynthetica 42(2):173–178Google Scholar
  15. Ghimire B, Lee C, Heo K (2014) Leaf anatomy and its implications for phylogenetic relationships in Taxaceae sl. J Plant Res 127(3):373–388Google Scholar
  16. Guo LD, Huang GR, Wang Y (2008) Seasonal and tissue age influences on endophytic fungi of Pinus tabulaeformis (Pinaceae) in the Dongling Mountains, Beijing. J Integr Plant Biol 50(8):997–1003Google Scholar
  17. Herbin G, Sharma K (1969) Studies on plant cuticular waxes—V. The wax coatings of pine needles: a taxonomic survey. Phytochemistry 8(1):151–160Google Scholar
  18. Huang Y, Mao J, Chen Z, Meng J, Xu Y, Duan A, Li Y (2016) Genetic structure of needle morphological and anatomical traits of Pinus yunnanensis. J For Res 27(1):13–25Google Scholar
  19. Jasińska AK, Boratyńska K, Sobierajska K, Romo A, Ok T, Kharat MBD, Boratyński A (2013) Relationships among Cedrus libani, C. brevifolia and C. atlantica as revealed by the morphological and anatomical needle characters. Plant Syst Evol 299(1):35–48Google Scholar
  20. Jordan L, He R, Hall DB, Clark AI, Daniels RF (2007) Variation in loblolly pine ring microfibril angle in the southeastern United States. Wood Fiber Sci 39(2):352–363Google Scholar
  21. Kajimoto T (1990) Photosynthesis and respiration of Pinus pumila needles in relation to needle age and season. Ecol Res 5(3):333–340Google Scholar
  22. Larsen JB, Mekic F (1991) The geographic variation in European silver fir (Abies alba Mill.). Gas exchange and needle cast in relation to needle age, growth rate, dry matter partitioning and wood density by 15 different provenance at age 6. Silvae Genet 40:188–198Google Scholar
  23. Lexer C, Fay M (2005) Adaptation to environmental stress: a rare or frequent driver of speciation? J Evol Biol 18(4):893–900Google Scholar
  24. Li G, Liu Y, Ma L, Lv R, Yu H, Bai S, Kang Y (2009) Comparison of tree growth and undergrowth development in aerially seeded and planted Pinus tabulaeformis forests. Front For China 4(3):283–290Google Scholar
  25. Li W, Wang X, Li Y (2011) Stability in and correlation between factors influencing genetic quality of seed lots in seed orchard of Pinus tabuliformis Carr. over a 12-year span. PLoS ONE 6(8):e23544Google Scholar
  26. Liang D, Mao J, Zhao W, Zhou X, Yuan H, Wang L, Xing F, Wang X, Li Y (2013) Seedling performance of Pinus densata and its parental population in the habitat of P. tabuliformis. Chin J Plant Ecol 37(2):150–163Google Scholar
  27. Lin J, Jach M, Ceulemans R (2001) Stomatal density and needle anatomy of Scots pine (Pinus sylvestris) are affected by elevated CO2. New Phytol 150(3):665–674Google Scholar
  28. Liu X, Gao C, Su Q, Zhang Y, Song Y (2016) Altitudinal trends in d13C value, stomatal density and nitrogen content of Pinus tabuliformis needles on the southern slope of the middle Qinling Mountains, China. J Mt Sci 6(13):1066–1077Google Scholar
  29. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates Press, Sunderland, pp 107–127Google Scholar
  30. Maley ML, Parker WH (1993) Phenotypic variation in cone and needle characters of Pinus banksiana (Jack pine) in northwestern Ontario. Can J Bot 71(1):43–51Google Scholar
  31. Mao Q, Watanabe M, Imori M, Kim Y, Kita K, Koike T (2012) Photosynthesis and nitrogen allocation in needles in the sun and shade crowns of hybrid larch saplings: effect of nitrogen application. Photosynthetica 50(3):422–428Google Scholar
  32. McKown AD, Guy RD, Klápště J, Geraldes A, Friedmann M, Cronk QC, El-Kassaby YA, Mansfield SD, Douglas CJ (2014) Geographical and environmental gradients shape phenotypic trait variation and genetic structure in Populus trichocarpa. New Phytol 201(4):1263–1276Google Scholar
  33. Meng J, Mao JF, Zhao W, Xing F, Chen X, Liu H, Xing Z, Wang XR, Li Y (2015) Adaptive differentiation in seedling traits in a hybrid pine species complex, Pinus densata and its parental species, on the Tibetan Plateau. PLoS ONE 10(3):e0118501Google Scholar
  34. Morgenstern M (2011) Geographic variation in forest trees: genetic basis and application of knowledge in silviculture. University of British Columbia Press, Vancouver, pp 3–18Google Scholar
  35. Nikolić B, Bojović S, Marin P (2015) Variability of morpho-anatomical characteristics of the needles of Picea omorika from natural populations in Serbia. Plant Biosyst Int J Deal Asp Plant Biol 149(1):61–67Google Scholar
  36. Niu SH, Li W, Li Y (2013) Open pollinated progeny test and stability analysis of seedlot from clonal seed orchard of Pinus tabuliformis. J Northwest For Univ 2:013Google Scholar
  37. Oleksyn J, Modrzýnski J, Tjoelker M, Reich P, Karolewski P (1998) Growth and physiology of Picea abies populations from elevational transects: common garden evidence for altitudinal ecotypes and cold adaptation. Funct Ecol 12(4):573–590Google Scholar
  38. Osada N, Nabeshima E, Hiura T (2015) Geographic variation in shoot traits and branching intensity in relation to leaf size in Fagus crenata: a common garden experiment. Am J Bot 102(6):878–887Google Scholar
  39. Parrish JD (1995) Effects of needle architecture on warbler habitat selection in a coastal spruce forest. Ecology 76(6):1813–1820Google Scholar
  40. Pensa M, Aalto T, Jalkanen R (2004) Variation in needle-trace diameter in respect of needle morphology in five conifer species. Trees 18(3):307–311Google Scholar
  41. Qiang W, Wang X, Chen T, Feng H, An L, He Y, Wang G (2003) Variations of stomatal density and carbon isotope values of Picea crassifolia at different altitudes in the Qilian Mountains. Trees 17(3):258–262Google Scholar
  42. Qualls FJ, Shine R (1998) Geographic variation in lizard phenotypes: importance of the incubation environment. Biol J Lin Soc 64(4):477–491Google Scholar
  43. Razgour O, Juste J, Ibáñez C, Kiefer A, Rebelo H, Puechmaille SJ, Arlettaz R, Burke T, Dawson DA, Beaumont M, Jones G (2013) The shaping of genetic variation in edge-of-range populations under past and future climate change. Ecol Lett 10(16):1258–1266Google Scholar
  44. Reich PB, Oleksyn J, Modrzynski J, Tjoelker MG (1996) Evidence that longer needle retention of spruce and pine populations at high elevations and high latitudes is largely a phenotypic response. Tree Physiol 16(7):643–647Google Scholar
  45. Tobler M, Palacios M, Chapman LJ, Mitrofanov I, Bierbach D, Plath M, Arias-Rodriguez L, García de León FJ, Mateos M (2011) Evolution in extreme environments: replicated phenotypic differentiation in livebearing fish inhabiting sulfidic springs. Evolution 65(8):2213–2228Google Scholar
  46. Urbaniak L, Karlinski L, Popielarz R (2003) Variation of morphological needle characters of Scots pine [Pinus sylvestris L.] populations in different habitats. Acta Soc Bot Pol 72(1):37–44Google Scholar
  47. Wagner GP, Altenberg L (1996) Perspective: complex adaptations and the evolution of evolvability. Evolution 50(3):967–976Google Scholar
  48. Wang MB, Gao FQ (2009) Genetic variation in Chinese pine (Pinus tabulaeformis), a woody species endemic to China. Biochem Genet 47(1–2):154–164Google Scholar
  49. Wang T, O’Neill GA, Aitken SN (2010) Integrating environmental and genetic effects to predict responses of tree populations to climate. Ecol Appl 20(1):153–163Google Scholar
  50. White TL, Adams WT, Neale DB (2007) Forest genetics. CABI Publishing, Cambridge, pp 149–284Google Scholar
  51. Xiao Y (2003) Variation in needle longevity of Pinus tabulaeformis forests at different geographic scales. Tree Physiol 23(7):463–471Google Scholar
  52. Xing F, Mao JF, Meng J, Dai J, Zhao W, Liu H, Xing Z, Zhang H, Wang XR, Li Y (2014) Needle morphological evidence of the homoploid hybrid origin of Pinus densata based on analysis of artificial hybrids and the putative parents, Pinus tabuliformis and Pinus yunnanensis. Ecol Evol 4(10):1890–1902Google Scholar
  53. Xu B, Tao WX (2006) Application of a hand-held slicing method for wood species identification. China Wood Ind 20:41–43Google Scholar
  54. Yang L, Liu Z, Li J, Dyer RJ (2015) Genetic structure of Pinus henryi and Pinus tabuliformis: natural landscapes as significant barriers to gene flow among populations. Biochem Syst Ecol 61:124–132Google Scholar
  55. Yuan H, Li Z, Fang P, Li W, Li Y (2014) Variation and stability in female strobili production of a first-generation clonal seed orchard of Chinese Pine (Pinus tabuliformis). Silvae Genet 63(1–2):41–47Google Scholar

Copyright information

© Northeast Forestry University and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Jingxiang Meng
    • 1
    • 2
  • Xinyu Chen
    • 1
    • 2
  • Yujie Huang
    • 3
  • Liming Wang
    • 1
    • 2
  • Fangqian Xing
    • 1
    • 2
  • Yue Li
    • 1
    • 2
    Email author
  1. 1.National Engineering Laboratory for Forest Tree Breeding, Key Laboratory for Genetics and Breeding of Forest Trees and Ornamental Plants of Ministry of EducationBeijing Forestry UniversityBeijingPeople’s Republic of China
  2. 2.College of Biology Sciences and TechnologyBeijing Forestry UniversityBeijingPeople’s Republic of China
  3. 3.State Academy of Forestry AdministrationBeijingPeople’s Republic of China

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