Molecular proxies for climate maladaptation in a long-lived tree (Pinus pinaster Aiton, Pinaceae)

Genetics

Volumn 199, Issue 3, 2015, Pages 793-807

  Jaramillo Correa, Juan Pablo ^a,b   Rodríguez Quilón, Isabel ^a   Grivet, Delphine ^a   Lepoittevin, Camille ^c,d   Sebastiani, Federico ^e   Heuertz, Myriam ^a,c,d   Garnier Géré, Pauline H ^c,d   Alía, Ricardo ^a   Plomion, Christophe ^c,d   Vendramin, Giovanni G ^e   González Martínez, Santiago C ^a,f  

^a INIA   (Spain)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c UMR 1202 BIOGECO   (France)

^d UNIVERSITÉ DE BORDEAUX   (France)

^e Institute of Biosciences and BioResources   (Italy)

^f UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Climate adaptation; Environmental associations; Fitness estimates; Genetic lineages; Single nucleotide polymorphisms

Indexed keywords

AMINO ACID;

ALLELE; ARTICLE; BAYESIAN LEARNING; BIODIVERSITY; CLIMATE CHANGE; ENVIRONMENTAL CHANGE; FOREST; GENE FREQUENCY; GENE POOL; GENETIC ASSOCIATION; GENETIC MARKER; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; KEYSTONE SPECIES; MALADAPTATION; MALADJUSTMENT; MOLECULAR BIOLOGY; MOLECULAR PROXY; MORPHOLOGICAL ADAPTATION; NONHUMAN; OUTCROSSING; PINACEAE; PINUS PINASTER; PLANT GENE; POPULATION STRUCTURE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; SUMMER; SURVIVAL RATE; TEMPERATURE; TREE GROWTH; TROPIC CLIMATE; WINTER; ACCLIMATIZATION; GENETICS; PINE; PLANT GENOME;

PINACEAE; PINUS PINASTER;

ACCLIMATIZATION; CLIMATE CHANGE; GENOME, PLANT; PINUS; POLYMORPHISM, SINGLE NUCLEOTIDE; TEMPERATURE;

EID: 84925012830     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.173252     Document Type: Article

References (106)

1. Aitken, S. N., S. Yeaman, J. A. Holliday, T. Wang, and S. Curtis- McLane, 2008 Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol. Appl. 1: 95–111.
2. Alberto, F. J., S. N. Aitken, R. Alía, S. C. González-Martínez, H. Hänninen et al., 2013a Potential for evolutionary responses to climate change: evidence from tree populations. Glob. Change Biol. 19: 1645–1661.
3. Alberto, F. J., J. Derory, C. Boury, J. M. Frigerio, N. E. Zimmermann et al., 2013b Imprints of natural selection along environmental gradients in phenology-related genes of Quercus petraea. Genetics 195: 495–512.
4. Alía, R., S. Martín, J. de-Miguel, R. Galera, D. Agúndez et al., 1996 Las regiones de procedencia de Pinus pinaster Aiton. Organismo Autónomo de Parques Nacionales, Madrid.
5. Anderson, J. T., J. H. Willis, and T. Mitchell-Olds, 2011 Evolutionary genetics of plant adaptation. Trends Genet. 27: 258–266.
6. Bellard, C., C. Bertelsmeier, P. Leadley, W. Thuiller, and F. Courchamp, 2012 Impacts of climate change on the future of biodiversity. Ecol. Lett. 15: 365–377.
7. Benito Garzón, M., R. Alía, T. M. Robson, and M. A. Zavala, 2011 Intra-specific variability and plasticity influence potential tree species distributions under climate change. Glob. Ecol. Biogeogr. 20: 766–778.
8. Benjamini, Y., 2010 Discovering the false discovery rate. J. R. Stat. Soc. B 72: 405–416.
9. Berg, J. J., and G. Coop, 2014 A population genetic signal of polygenic adaptation. PLoS Genet. 10: e1004412.
10. Bigham, A., M. Bauchet, D. Pinto, X. Mao, J. M. Akey et al., 2010 Identifying signatures of natural selection in Tibetan and Andean populations using dense genome scan data. PLoS Genet. 6: e1001116.
11. Bigras, F., and S. J. Colombo, 2001 Conifer Cold Hardiness. Kluwer, Dordrchet, The Netherlands.
12. Birol, I., A. Raymond, S. D. Jackman, S. Pleasance, R. Coope et al., 2013 Assembling the 20Gb white spruce (Picea glauca) genome from whole-genome shotgun sequencing data. Bioinformatics 29: 1492–1497.
13. Blödner, C., T. Skroppa, Ø. Johnsen, and A. Polle, 2005 Freezing tolerance in two Norway spruce (Picea abies [L.] Karst.) progenies is physiologically correlated with drought. J. Plant Physiol. 162: 549–558.
14. Bouillé, M., and J. Bousquet, 2005 Trans-species shared polymorphisms at orthologous gene loci among distant species in the conifer Picea (Pinaceae): implications for the long-term maintenance of genetic diversity in trees. Am. J. Bot. 92: 63–73.
15. Brown, G. R., G. P. Gill, R. J. Kuntz, C. H. Langley, and D. B. Neale, 2004 Nucleotide diversity and linkage disequilibrium in loblolly pine. Proc. Natl. Acad. Sci. USA 101: 15255–15260.
16. Bucci, G., S. C. González-Martínez, G. Le Provost, C. Plomion, M. M. Ribeiro et al., 2007 Range-wide phylogeography and gene zones in Pinus pinaster Ait. revealed by chloroplast microsatellite markers. Mol. Ecol. 16: 2137–2153.
17. Budde, K. B., M. Heuertz, A. Hernández-Serrano, J. G. Pausas, G. G. Vendramin et al., 2014 In situ genetic association for serotiny, a fire-related trait, in Mediterranean maritime pine (Pinus pinaster). New Phytol. 201: 230–241.
18. Calus, M. P. L., T. H. E. Meuwissen, A. P. W. de Roos, and R. F. Veerkamo, 2008 Accuracy of genomic selection using different methods to define haplotypes. Genetics 178: 553–561.
19. Carnicer, J., M. Coll, M. Ninyerola, X. Pons, G. Sánchez et al., 2011 Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. Proc. Natl. Acad. Sci. USA 108: 1474–1478.
20. Chancerel, E., C. Lepoittevin, G. Le Provost, Y. C. Lin, J. P. Jaramillo- Correa et al., 2011 Development and implementation of a highlymultiplexed SNP array for genetic mapping in maritime pine. BMC Genomics 12: 368.
21. Chancerel, E., J. B. Lamy, I. Lesur, C. Noirot, C. Klopp et al., 2013 High-density linkage mapping in a pine tree reveals a genomic region associated with inbreeding depression and provides clues to the extent and distribution of meiotic recombination. BMC Biol. 11: 50.
22. Chen, J., T. Källman, X. Ma, N. Gyllenstrand, G. Zaina et al., 2012 Disentangling the roles of history and local selection in shaping clinal variation of allele frequencies and gene expression in Norway spruce (Picea abies). Genetics 191: 865–881.
23. Chen, J., Y. Tsuda, M. Stocks, T. Källman, N. Xu et al., 2014 Clinal variation at phenology-related genes in spruce: Parallel evolution in FTL2 and Gigantea? Genetics 197: 1025–1038.
24. Choat, B., S. Jansen, T. J. Brodribb, H. Cochard, S. Delzon et al., 2012 Global convergence in the vulnerability of forests to drought. Nature 491: 752–755.
25. Chu, B., D. P. Snustad, and J. V. Carter, 1993 Alteration of b-tubulin gene expression during low-temperature exposure in leaves of Arabidopsis thaliana. Plant Physiol. 103: 371–377.
26. Condit, R., S. P. Hubbell, and R. B. Foster, 1995 Mortality rates of 205 neotropical tree and shrub species and the impact of a severe drought. Ecol. Monogr. 65: 419–439.
27. Cooke, J. E. K., M. E. Eriksson, and O. Junttila, 2012 The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant Cell Environ. 35: 1707–1728.
28. Coop, G., J. K. Pickrell, J. Novembre, S. Kudaravalli, J. Li et al., 2009 The role of geography in human adaptation. PLoS Genet. 5: e1000500.
29. Crawford, N. G., 2010 SMOGD: software for the measurement of genetic diversity. Mol. Ecol. Res. 10: 556–557.
30. De La Torre, A. R., D. R. Roberts, and S. N. Aitken, 2014 Genomewide admixture and ecological niche modelling reveal the maintenance of species boundaries despite long history of interspecific gene flow. Mol. Ecol. 23: 2046–2059.
31. de-Lucas, A. I., J. J. Robledo-Arnuncio, E. Hidalgo, and S. C. González-Martínez, 2008 Mating system and pollen gene flow in Mediterranean maritime pine. Heredity 100: 390–399.
32. de-Miguel, M., N. de-Maria, M. A. Guevara, L. Diaz, E. Sáez-Laguna et al., 2012 Annotated genetic linkage maps of Pinus pinaster Ait. from a central Spain population using microsatellite and gene based markers. BMC Genomics 13: 527.
33. De-Mita, S., A. C. Thuillet, L. Gay, N. Ahmadi, S. Manel et al., 2013 Detecting selection along environmental gradients: analysis of eight methods and their effectiveness for outbreeding and selfing populations. Mol. Ecol. 22: 1383–1399.
34. Deagle, B. E., F. C. Jones, Y. F. Chan, D. M. Absher, D. M. Kingsley et al., 2012 Population genomics of parallel phenotypic evolution in stickleback across stream-lake ecological transitions. Proc. R. Soc. B Biol. Sci. 279: 1277–1286.
35. Desta, Z. A., and R. Ortiz, 2014 Genome-selection: genome-wide prediction in plant improvement. Trends Plant Sci. 19: 592–601.
36. Eckert, A. J., H. Shahi, S. L. Datwyler, and D. B. Neale, 2012 Spatially variable natural selection and the divergence between parapatric subspecies of lodgepole pine (Pinus contorta, Pinaceae). Am. J. Bot. 99: 1323–1334.
37. Eckert, A. J., J. van Heerwaarden, J. L. Wegrzyn, C. D. Nelson, J. Ross-Ibarra et al., 2010a Patterns of population structure and environmental associations to aridity across the range of loblolly pine (Pinus taeda L., Pinaceae). Genetics 185: 969–982.
38. Eckert, A. J., A. D. Bower, S. C. González-Martínez, J. L. Wegrzyn, G. Coop et al., 2010b Back to nature: ecological genomics of loblolly pine (Pinus taeda, Pinaceae). Mol. Ecol. 19: 3789–3805.
39. Evanno, G., S. Regnaut, and J. Goudet, 2005 Detecting the number of clusters of individuals using the software structure: a simulation study. Mol. Ecol. 14: 2611–2620.
40. Eveno, E., C. Collada, M. A. Guevara, V. Léger, A. Soto et al., 2008 Contrasting patterns of selection at Pinus pinaster Ait. drought stress candidate genes as revealed by genetic differentiation analyses. Mol. Biol. Evol. 25: 417–437.
41. Excoffier, L., and H. E. L. Lischer, 2010 Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Res. 10: 564–567.
42. Fischer, I., L. Camus-Kulandaivelu, F. Allal, and W. Stephan, 2011 Adaptation to drought in two wild tomato species: the evolution of the Asr gene family. New Phytol. 190: 1032–1044.
43. Fournier-Level, A., A. Korte, M. D. Cooper, M. Nordborg, J. Schmitt et al., 2011 A map of local adaptation in Arabidopsis thaliana. Science 334: 86–89.
44. Franks, S. J., and A. A. Hoffmann, 2012 Genetics of climate change adaptation. Annu. Rev. Genet. 46: 185–208.
45. Frichot, E., S.D. Schoville, G. Bouchard, andO. François, 2013 Testing for associations between loci and environmental gradients using latent factor mixed models. Mol. Biol. Evol. 30: 1687–1699.
46. Gamache, I., and S. Payette, 2004 Height growth response of tree line black spruce to recent climate warming across the foresttundra of eastern Canada. J. Ecol. 92: 835–845.
47. González, J., K. Lenkov, M. Lipatov, J. M. MacPherson, and D. A. Petrov, 2008 High rate of recent transposable element-induced adaptation in Drosophila melanogaster. PLoS Biol. 6: e251.
48. González-Martínez, S. C., N. C. Wheeler, E. Ersoz, C. D. Nelson, and D. B. Neale, 2007 Association genetics in Pinus taeda L. I. Wood property traits. Genetics 175: 399–409.
49. González-Martínez, S. C., D. Huber, E. Ersoz, J. M. Davis, and D. B. Neale, 2008 Association genetics in Pinus taeda L. II. Water use efficiency. Heredity 101: 19–26.
50. Gonzalo, J., 2007 Phytoclimatic analysis of the Spanish Peninsula: update and geostatistical analysis. PhD Thesis, University of Valladolid, Palencia, Spain.
51. Grattapaglia, D., and M. D. V. Resende, 2011 Genome selection in forest tree breeding. Tree Genet. Genomes 7: 241–255.
52. Grivet, D., F. Sebastiani, R. Alía, and T. Bataillon, S. Torre et al., 2011 Molecular footprints of local adaptation in two Mediterranean conifers. Mol. Biol. Evol. 28: 101–116.
53. Günther, T., and G. Coop, 2013 Robust identification of local adaptation from allele frequencies. Genetics 195: 205–220.
54. Hancock, A. M., B. Brachi, N. Faure, M. W. Horton, L. B. Jarymowycz et al., 2011 Adaptation to climate across the Arabidopsis thaliana genome. Science 334: 83–86.
55. Hanikenne, M., J. Kroymann, A. Trampczynska, M. Bernal, P. Motte et al., 2013 Hard selective sweep and ectopic gene conversion in a gene cluster affording environmental adaptation. PLoS Genet. 9: e1003707.
56. Heuertz, M., E. De Paoli, T. Källman, H. Larsson, I. Jurman et al., 2006 Multilocus patterns of nucleotide diversity, linkage disequilibrium and demographic history of Norway spruce. [Picea abies (L.) Karst] Genetics 174: 2095–2105.
57. Hijmans, R. J., S. E. Cameron, J. L. Parra, P. G. Jones, and A. Jarvis, 2005 Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25: 1965–1978.
58. Hoffmann, A. A., and C. M. Sgrò, 2011 Climate change and evolutionary adaptation. Nature 470: 479–485.
59. Hughes, L., 2000 Biological consequences of global warming: Is the signal already apparent? Trends Ecol. Evol. 15: 56–61.
60. Ioannidis, J. P. A., G. Thomas, and M. J. Daly, 2009 Validating, augmenting and refining genome-wide association signals. Nat. Rev. Genet. 10: 318–329.
61. Jakobsson, M., and N. A. Rosenberg, 2007 CLUMPP: a software matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23: 1801–1806.
62. Kearney, M., W. P. Porter, C. Williams, S. Ritchie, and A. A. Hoffmann, 2009 Integrating biophysical models and evolutionary theory to predict climatic impacts on species’ ranges: the dengue mosquito Aedes aegypti in Australia. Funct. Ecol. 23: 528–538.
63. König, I. K., 2011 Validation in genetic association studies. Brief. Bioinform. 12: 253–258.
64. Kremer, A., and V. Le Corre, 2012 Decoupling of differentiation between traits and their underlying genes in response divergent selection. Heredity 108: 375–385.
65. Kremer, A., O. Ronce, J. J. Robledo-Arnuncio, F. Guillaume, G. Bohrer et al., 2012 Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecol. Lett. 15: 378–392.
66. Kuparinen, A., O. Savolainen, and F. M. Schurr, 2010 Increased mortality can promote evolutionary adaptation of forest trees to climate change. For. Ecol. Manage. 259: 1003–1008.
67. Lepoittevin, C., L. Harvengt, C. Plomion, and P. H. Garnier-Géré, 2012 Association mapping for growth, straightness and wood chemistry traits in the Pinus pinaster Aquitaine breeding population. Tree Genet. Genomes 8: 113–126.
68. Loarie, S. R., P. B. Duffy, H. Hamilton, G. P. Asner, C. B. Field et al., 2009 The velocity of climate change. Nature 462: 1052–1055.
69. Lorenz, W. W., R. Alba, Y. S. Yu, J. M. Bordeaux, M. Simões et al., 2011 Microarray analysis and scale-free gene networks identify candidate regulators in drought-stressed roots of loblolly pine (P. taeda L.). BMC Genomics 12: 264.
70. Lotterhos, K. E., and M. C. Whitlock, 2014 Evaluation of demographic history and neutral parameterization on the performance of Fst outlier tests. Mol. Ecol. 23: 2178–2192.
71. Lynch, M., and R. Lande, 1993 Evolution and extinction in response to environmental change, pp. 234–250 in Biotic Interactions and Global Change, edited by P. M. Kareiva, J. G. Kingsolver, and R. B. Huey. Sinauer Associates, Sunderland, MA.
72. Malcom, J. R., A. Markham, R. P. Neilson, and M. Garaci, 2011 Estimated migration rates under scenarios of global climate change. J. Biogeogr. 29: 835–849.
73. McLachlan, J. S., J. S. Clark, and P. S. Manos, 2005 Molecular indicators of tree migration capacity under rapid climate change. Ecology 86: 2088–2098.
74. McLeod, T. K., and G. MacDonald, 1997 Postglacial range expansion and population growth of Picea mariana, P. glauca and Pinus banksiana in the western interior of Canada. J. Biogeogr. 24: 865–881.
75. Morin, P. A., G. Luikart, and R. K. Wayne, and the SNP workshop Group, 2004 SNPs in ecology, evolution and conservation. Trends Ecol. Evol. 19: 208–216.
76. Mosca, E., A. J. Eckert, E. A. Di Pierro, D. Rocchini, N. La Porta et al., 2012 The geographical and environmental determinants of genetic diversity for four alpine conifers of the European Alps. Mol. Ecol. 21: 5530–5545.
77. Namroud, M. C., J. Beaulieu, N. Juge, J. Laroche, and J. Bousquet, 2008 Scanning the genome for gene single nucleotide polymorphisms involved in adaptive population differentiation in white spruce. Mol. Ecol. 17: 3599–3613.
78. Neale, D. B., and P. K. Ingvarsson, 2008 Population, quantitative and comparative genomics of adaptation in forest trees. Curr. Opin. Plant Biol. 11: 149–155.
79. Neale, D. B., and O. Savolainen, 2004 Association genetics of complex traits in conifers. Trends Plant Sci. 9: 325–330.
80. Neale, D. B., J. L. Wegrzyn, K. A. Stevens, A. V. Zimin, D. Puiu et al., 2014 Decoding the massive genome of loblolly pine using haploid DNA and novel assembly strategies. Genome Biol. 15: R59.
81. Nystedt, B., N. Street, A. Wetterbom, A. Zuccolo, Y. C. Lin et al., 2013 The Norway spruce genome sequence and conifer genome evolution. Nature 497: 579–584.
82. O’Connell, L. M., A. Mosseler, and O. P. Rajora, 2006 Impact of forest fragmentation on the mating system and genetic diversity of white spruce (Picea glauca) at the landscape level. Heredity 97: 418–426.
83. Perdiguero, P., M. C. Barbero, M. T. Cervera, C. Collada, and A. Soto, 2013 Molecular responses to water stress in two contrasting Mediterranean pines (Pinus pinaster and Pinus pinea). Plant Physiol. Biochem. 67: 199–208.
84. Petit, R. J., and A. Hampe, 2006 Some evolutionary consequences of being a tree. Annu. Rev. Ecol. Evol. Syst. 37: 187–214.
85. Pot, D., L. McMillan, C. Echt, G. Le Provost, P. H. Garnier-Géré et al., 2005 Nucleotide variation in genes involved in wood formation in two pine species. New Phytol. 167: 101–112.
86. Pritchard, J. K., M. Stephens, and P. Donnelly, 2000 Inference of population structure using multilocus genotype data. Genetics 155: 945–959.
87. Prunier, J., J. Laroche, J. Beaulieu, and J. Bousquet, 2011 Scanning the genome for gene SNPs related to climate adaptation and estimating selection at the molecular level in boreal black spruce. Mol. Ecol. 20: 1702–1716.
88. Prunier, J., S. Gerardi, J. Beaulieu, and J. Bousquet, 2012 Parallel and lineage-specific molecular adaptation to climate in boreal black spruce. Mol. Ecol. 21: 4270–4286.
89. R Development Core Team, 2013 R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: http://www.R-project.org.
90. Rangel, T. F., J. A. F. Diniz-Filho, and L. M. Bini, 2010 SAM: a comprehensive application of spatial analysis in macroecology. Ecography 33: 46–50.
91. Rehfeldt, G. E., C. C. Ying, D. L. Spittlehouse, and D. A. Hamilton, 1999 Genetic responses to climate in Pinus contorta: nichebreadth, climate change, and reforestation. Ecol. Monogr. 69: 375–407.
92. Rubiales, J. M., I. García-Amorena, L. Hernández, M. Génova, F. Martínez et al., 2010 Late quaternary dynamics of pinewoods in the Iberian Mountains. Rev. Palaeobot. Palynol. 162: 476–491.
93. Santos-del-Blanco, L., J. Climent, S. C. González-Martínez, and J. R. Pannell, 2012 Genetic differentiation for size at first reproduction through male vs. female functions in the widespread Mediterranean tree Pinus pinaster. Ann. Bot. 110: 1449–1460.
94. Savolainen, O., T. Pyhäjärvi, and T. Knürr, 2007 Gene flow and local adaptation in trees. Annu. Rev. Ecol. Evol. Syst. 38: 595–619.
95. Savolainen, O., S. T. Kujala, C. Sokol, T. Pyhäjärvi, K. Avia et al., 2011 Adaptive potential of northernmost tree populations to climate change, with emphasis on Scots pine (Pinus sylvestris L.). J. Hered. 102: 526–536.
96. Seki, M., M. Narusaka, J. Ishida, T. Nanjo, M. Fujita et al., 2002 Monitoring the expression profile of 7000 Arabidopsis genes under drought, cold and high salinity stresses using a full-length cDNA microarray. Plant J. 31: 279–292.
97. Tanino, K. K., L. Kalcsits, S. Silim, E. Kendall, and G. R. Gray, 2010 Temperature-driven plasticity in growth cessation and dormancy development in deciduous woody plants: a working hypothesis suggesting how molecular and cellular function is affected by temperature during dormancy induction. Plant Mol. Biol. 73: 49–65.
98. Tenaillon, O., A. Rodríguez-Vergugo, R. L. Gaut, P. McDonald, A. F. Bennett et al., 2012 The molecular diversity of adaptive convergence. Science 335: 457–461.
99. Tiffin, P., and J. Ross-Ibarra, 2014 Advances and limits of using population genetics to understand local adaptation. Trends Ecol. Evol. 29: 673–680.
100. Urano, K., Y. Kurihara, M. Seki, and K. Shinozaki, 2010 “Omics” analyses of regulatory networks in plant abiotic stress responses. Curr. Opin. Plant Biol. 13: 132–138.
101. Wagner, A., L. Donaldson, H. Kim, L. Phillips, H. Flint et al., 2009 Suppression of 4-Coumarate-CoA ligase in the coniferous gymnosperm Pinus radiata. Plant Physiol. 149: 370–383.
102. Westbrook, J. W., M. F. Resende Jr., P. Munoz, A. R. Walker, J. L. Wegrzyn et al., 2013 Association genetics of oleoresin flow in loblolly pine: discovering genes and predicting phenotype for improved resistance to bark beetles and bioenergy potential. New Phytol. 199: 89–100.
103. Yakovlev, I. A., C. G. Fossdal, and Ø. Johnsen, 2010 MicroRNAs, the epigenetic memory and climate adaptation in Norway spruce. New Phytol. 187: 1154–1169.
104. Yeaman, S., and A. Jarvis, 2006 Regional heterogeneity and gene flow maintain variance in a quantitative trait within populations of lodgepole pine. Proc. R. Soc. B Biol. Sci. 273: 1587–1593.
105. Yun, M. S., W. J. Chen, F. Deng, and Y. Yogo, 2005 Selective growth suppression of five annual plant species by chalcone and naringenin correlates with the total amount of 4-coumarate: coenzyme A ligase. Weed Biol. Manage. 9: 27–37.
106. Zhu, K., C. W. Woodall, and J. S. Clark, 2011 Failure to migrate: lack of tree range expansion in response to climate change. Glob. Change Biol. 18: 1042–1052.