Single-locus versus multilocus patterns of local adaptation to climate in eastern white pine (Pinus strobus, Pinaceae)

PLoS ONE

Volumn 11, Issue 7, 2016, Pages

  Rajora, Om P ^a   Eckert, Andrew J ^b   Zinck, John W R ^a,c  

^a UNIVERSITY OF NEW BRUNSWICK   (Canada)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c Athletigen Technologies Inc   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CLIMATE; COVARIANCE; DIVERSIFYING SELECTION; GENE STRUCTURE; GENETIC DISTANCE; GENETIC MARKER; LOCAL ADAPTATION; MUTATION RATE; NATURAL POPULATION; POPULATION STRUCTURE; SINGLE NUCLEOTIDE POLYMORPHISM; WHITE PINE; ADAPTATION; GENETIC SELECTION; GENETIC VARIATION; GENETICS; GENOTYPE; GEOGRAPHY; MUTATION; ODDS RATIO; PINE; PLANT GENE; POPULATION GENETICS; QUANTITATIVE TRAIT LOCUS;

PLANT DNA;

ADAPTATION, PHYSIOLOGICAL; CLIMATE; DNA, PLANT; GENES, PLANT; GENETIC MARKERS; GENETIC VARIATION; GENETICS, POPULATION; GENOTYPE; GEOGRAPHY; MUTATION; ODDS RATIO; PINUS; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; SELECTION, GENETIC;

EID: 84978648840     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0158691     Document Type: Article

References (94)

1. Kawecki T.J., Ebert D. Conceptual issues in local adaptation. Ecology Letters 2004; 7:1225-1241
2. Panwell J.R., Fields P.D. Evolution in subdivided plant populations: concepts, recent advances and future directions. New Phytologist 2013; 201:417-432 10.1111/nph.12495 PMID: 24111698
3. Neale D.B., Kremer A. Forest tree genomics: growing resources and applications. Nature Reviews Genetics 2011; 12:111-122 10.1038/nrg2931 PMID: 21245829
4. Morgenstern E.K. Geographic variation in forest trees - Genetic basis and application of knowledge in silviculture. 1996; UBC Press, Canada.
5. Endler J.A. Natural selection in the wild. 1986; Princeton University Press, New Jersey
6. Latta R.G. Differentiation of allelic frequencies at quantitative trait loci affecting locally adaptive traits. The American Naturalist 1998; 151:283-292 10.1086/286119 PMID: 18811359
7. Latta R.G. Gene flow, adaptive population divergence and comparative population structure across loci. New Phytologist 2003; 161:51-58
8. Kremer A., Le Corre V. Decoupling of differentiation between traits and their underlying genes in response to divergent selection. Heredity 2012; 108:375-385 10.1038/hdy.2011.81 PMID: 21915150
9. Le Corre V, Kremer A. Genetic variability at neutral markers, quantitative trait loci and trait in a subdivided population under selection. Genetics 2003; 164:1205-1219 PMID: 12871925
10. Le Corre V., Kremer A. The genetic differentiation at quantitative trait loci under local adaptation. Molecular Ecology 2012; 21:1548-1566 10.1111/j.1365-294X.2012.05479.x PMID: 22332667
11. Ohta T. Linkage disequilibrium with the island model. Genetics 1982; 101:139-155 PMID: 17246079
12. Hall D., Luquez V., Garcia VM, St. Onge K.R., Jansson S., Ingvarsson P.K. Adaptive population differentiation in phenology across a latitudinal gradient in European aspen (Populus tremula, L.): A comparison of neutral markers, candidate genes and phenotypic traits. Evolution 2007; 61:2849-2860 PMID: 17908247
13. Howe G.T., Aitken S.N., Neale D.B., Jermstad K.D., Wheeler N.C., Chen T.H.H. From genotype to phenotype: unraveling the complexities of cold adaptation in forest trees. Canadian Journal of Botany 2003; 81:1247-1266
14. Lynch M., Walsh B. Genetics and analysis of quantitative traits. 1999; Sinauer Associates, Inc., Massachusetts
15. Bürger R., Gimelfarb A. Genetic variation maintained in multilocus models of additive quantitative traits under stabilizing selection. Genetics 1999; 152:807-820 PMID: 10353920
16. Barton N.H. A general model for the evolution of recombination. Genetical Research 1995; 65:123-145 PMID: 7605514
17. Beaumont M.A., Balding J.B. Identifying adaptive genetic divergence among populations from genome scans. Molecular Ecology 2004; 13:969-980 PMID: 15012769
18. Foll M., Gaggiotti O. A genome-scan method to identify selected loci appropriate for both dominant and codominant marker: a Bayesian perspective. Genetics 2008; 180:977-993 10.1534/genetics.108.092221 PMID: 18780740
19. Excoffier L., Hofer T., Foll M. Detecting loci under selection in a hierarchically structured population. Heredity 2009; 103:285-298 10.1038/hdy.2009.74 PMID: 19623208
20. Coop G., Witonsky D., Di Rienzo A., Pritchard J.K. Using environmental correlations to identify loci underlying local adaptation. Genetics 2010; 185:1411-1423 10.1534/genetics.110.114819 PMID: 20516501
21. Hancock A.M., Witonsky D.B., Ehler E., Alkorta-Aranburu G., Beall C., Gebremedhin A., et al. Human adaptations to diet, subsistence, and ecoregion are due to subtle shifts in allele frequency. Proceedings of the National Academy of Sciences USA 2010; 107:28924-28930
22. Hancock A.M., Witonsky D.B., Alkorta-Aranburu G., Beall C.M., Gebremedhin A., Sukernik R., et al. Adaptations to climate-mediated selective pressures in humans. PLoS Genetics 2011; 7:e1001375 10.1371/journal.pgen.1001375 PMID: 21533023
23. Neale D.B., Savolainen O. Association genetics of complex traits in conifers. Trends in Plant Science 2004; 9:325-330 PMID: 15231277
24. Ma X.M., Hall D, St. Onge K.R., Jansson S., Ingvarsson P. Genetic differentiation, clinal variation and phenotypic associations with growth cessation across the Populus tremula photoperiodic pathway. Genetics 2010; 186:1033-1044 10.1534/genetics.110.120873 PMID: 20805554
25. Csillery K., Lalague H., Vendramin G.G., Gonzalez-Martinez S.C., Fady B., Oddou-Muratorio S. Detecting short spatial scale local adaptation and epistatic selection in climate-related candidate genes in European beach (Fagus sylvatica) populations. Molecular Ecology 2014; 23:4696-4708 10.1111/mec.12902 PMID: 25156570
26. Storz J.F., Kelly J.K. Effects of spatially varying selection on nucleotide diversity and linkage disequilibrium: Insights from deer mouse globin genes. Genetics 2008; 180:367-379 10.1534/genetics.108.088732 PMID: 18716337
27. Mackay T.F.C. Epistasis and quantitative traits: using model organisms to study gene-gene interactions. Nature Reviews Genetics 2014; 15:22-33 10.1038/nrg3627 PMID: 24296533
28. Kremer A., Zanetto A., Ducousso A. Multilocus and multitrait measures of differentiation for gene markers and phenotypic traits. Genetics 1997; 148:1229-1241
29. Sork V.L., Aitken S.N., Dyer R.J., Eckert A.J., Legendre P., Neale D.B. Putting the landscape into the genomics of trees: approaches for understanding local adaptation and population responses to changing climate. Tree Genetics and Genomes 2013; 9:901-911
30. Savolainen O., Pyhäjärvi T, Kunurr T. Gene flow and local adaptation in forest trees. Annual Review of Ecology, Evolution, and Systematics 2007; 38:595-619
31. Kremer A., Ronce O., Robledo-Arnuncio J.J., Guillaume F., Bohrer G., Nathan R., et al. Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecology Letters 2012; 15:378-392 10.1111/j.1461-0248.2012.01746.x PMID: 22372546
32. Davis M.B., Shaw R.G. Range shifts and adaptive responses to Quaternary climate change. Science 2001; 292:673-679 PMID: 11326089
33. Aitken S.N., Yeaman S., Holliday J.A., Wang T., Curtis-McLane S. Adaptation, migration or extirpation: Climate change outcomes for tree populations. Evolutionary Applications 2008; 1:95-111 10.1111/j.1752-4571.2007.00013.x PMID: 25567494
34. Wendel G.W., Smith H.C. Pinus strobus L.: Eastern White Pine. Burns RM, Honkala BH editors. Silvics of North America, ume1, Conifers. USDA Agric. Handbook 654, Washington, DC. 1990; 476-488
35. Fowler D.P., Heimburger C. Geographic variation in eastern white pine, 7-year results in Ontario. Silvae Genetica 1969; 18:123-129
36. Maronek D.M., Flint H.L. Cold hardiness of needles of Pinus strobus L. as a function of geographic source. Forest Science 1974; 20:135-141
37. Genys J.B. Provenance variation among different populations of Pinus strobus from Canada and the United States. Canadian Journal of Forest Research 1987; 17:228-235
38. Li P., Beaulieu J., Daoust G., Plourde A. Patterns of adaptive genetic variation in eastern white pine (Pinus strobus) from Quebec.Canadian Journal of Forest Research 1997; 27:199-206
39. Joyce D.G., Rehfeldt G.E. Climate niche, ecological genetics, and impact of climate change on eastern white pine (Pinus strobus L.): Guidelines for land managers. Forest Ecology and Management 2013; 295:173-192
40. Buchert G.P., Rajora O.P., Hood J.V., Dancik B.P. Effects of harvesting on genetic diversity in old-growth eastern white pine (Pinus strobus L.) in Ontario, Canada. Conservation Biology. 1997; 11:747-758.
41. Rajora O.P., Rahman M.H., Buchert G.P., Dancik B.P. Microsatellite DNA analysis of genetic effects of harvesting in old-growth eastern white pine (Pinus strobus) in Ontario. Molecular Ecology 2000; 9:339-348 PMID: 10736031
42. Chhatre V.E., Rajora O.P. Genetic divergence and signatures of natural selection in marginal populations of a keystone, long-lived conifer, eastern white pine (Pinus strobus) from northern Ontario. PLoS ONE 2014; 9: e97291 10.1371/journal.pone.0097291 PMID: 24859159
43. Marquardt P.E., Epperson B.K. Spatial and population genetic structure of microsatellites in white pine. Molecular Ecology 2004; 13:3305-3315 PMID: 15487991
44. Marquardt P.E., Echt C.S., Epperson B.K., Pubanz D.M. Genetic structure, diversity, and inbreeding of eastern white pine under different management conditions. Canadian Journal of Forest Research 2007; 37:2652-2662
45. Rajora O.P., DeVerno L., Mosseler A., Innes D. Genetic diversity and population structure of disjunct Newfoundland and central Ontario populations of eastern white pine (Pinus strobus L. ).Canadian Journal of Botany 1998; 76:500-508
46. Mehes M., Nkongolo K.K., Michael P. Assessing genetic diversity and structure of fragmented populations of eastern white pine (Pinus strobus) and western white pine (P. monticola) for conservation management.Journal of Plant Ecology 2009; 2:143-151
47. Zinck J.W.R., Rajora O.P. Post-glacial phylogeography and evolution of a wide-ranging highly-exploited keystone forest tree, eastern white pine (Pinus strobus) in North America: Single refugium, multiple routes. BMC Evolutionary Biology 2016; 16:56; 10.1186/s12862-016-0624-1 PMID: 26936598
48. Nadeau S., Godbout J., Lamothe M., Gros-Louis M.-C., Nathalie I., Ritland K. Contrasting patterns of genetic diversity across the ranges of Pinus monticola and P. strobus: A comparison between eastern and western North American postglacial colonization histories. American Journal of Botany 2015; 102:1342-1355 10.3732/ajb.1500160 PMID: 26290557
49. Doyle J.J., Doyle J.L. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 1987; 19:11-15
50. Hijmans R.J., Cameron S.E., Parra J.L., Jones P.G., Jarvis A. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 2005; 25:1965-1978
51. Watling J.I., Romanach S.S., Bucklin D.N., Speroterra C., Brandt L.A., Pearlstine L.G., Mazzotti F.J. Do bioclimatic variables improve performance of climate envelope models?Ecological Modelling 2012; 246:79-85
52. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2013; URL http://www.R-project.org/.
53. Echt C.S., May-Marquardt P., Hseih M., Zahorchak R. Characterization of microsatellite markers in eastern white pine. Genome 1996; 39:1102-1108 PMID: 8983182
54. Krutovsky K.V., Neale D.B. Nucleotide diversity and linkage disequilibrium in cold-hardiness- and wood quality-related candidate genes in Douglas fir. Genetics 2005; 171:2029-2041 PMID: 16157674
55. Namroud M.C., Beaulieu J., Juge N., Laroche J., Bousquet J. Scanning the genome for gene single nucleotide polymorphisms involved in adaptive population differentiation in white spruce. Molecular Ecology 2008; 17:3599-3613 10.1111/j.1365-294X.2008.03840.x PMID: 18662225
56. Wegrzyn J.L., Lee J.M., Tearse B.R., Neale D.B. TreeGenes: A forest tree database. International Journal of Plant Genomics 2008: 412875. 10.1155/2008/412875 PMID: 18725987
57. Wheeler N.C.,Jermstad K.D., Krutovsky K., Aitken S.N., Howe G.T., Krakowski J., Neale D.B. Mapping of quantitative trait loci controlling adaptive traits in costal Douglas fir. IV. Cold-hardiness QTL verification and candidate gene mapping. Molecular Breeding 2005; 5: 145-156
58. McCallum C.M., Comai L., Greene E.A., Henikoff S. Targeted screening for induced mutations. Nature Biotechnology 2000; 18:455-457 PMID: 10748531
59. ST. Nature Genetics 2009; 10:639-650
60. ST' and D do not replace FST . Molecular Ecology 2011; 20:1083-1091 10.1111/j.1365-294X.2010.04996.x PMID: 21375616
61. Dyer R.J., Nason J.D. Population Graphs: the graph theoretic shape of genetic structure. Molecular Ecology 2004; 13:1713-1727 PMID: 15189198
62. Goudet J. Hierfstat, a package for R to compute and test hierarchical F-statistics. Molecular Ecology Notes 2005; 5:184-186
63. Hedrick P.W. A standard genetic differentiation measure. Evolution 2005; 59:1633-1638 PMID: 16329237
64. Excoffier L., Smouse P.E., Quattro J.M. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics; 1992; 131:479-491. PMID: 1644282
65. Dyer R.J., Nason J.D., Garrick R.C. Landscape modeling of gene flow: improved power using conditional genetic distance derived from the topology of population networks. Molecular Ecology 2010; 19:3746-3759 10.1111/j.1365-294X.2010.04748.x PMID: 20723052
66. Dyer R.J. The evolution of genetic topologies. Theoretical Population Biology 2007; 71:71-79 PMID: 16919694
67. Dyer R.J. Population graphs and landscape genetics. Annual Review of Ecology, Evolution, and Systematics. 2015; 46, 327-342. 10.1146/annurev-ecolsys-112414-054150
68. Storey J.D., Tibshirani R. Statistical significance for genome-wide studies. Proceedings of the National Academy of Sciences USA 2003; 100:9440-9445
69. Legendre P., Legendre L. Numerical ecology. 2012; Elsevier, The Netherlands.
70. Legendre P., Lapointe F., Casgrain P. Modeling brain evolution from behavior: A permutational regression approach. Evolution 1994; 48:1487-1499
71. Hudson R.R. Generating samples under a Wright-Fisher neutral model. Bioinformatics 2002; 18:337-338 PMID: 11847089
72. Pidugu S.R., Schlötterer C. ms2ms.pl: a PERL script for generating microsatellite data. Molecular Ecology Notes 2006; 6:580-581
73. Bourret V., Dionne M., Bernatchez L. Detecting genotypic changes associated with selective mortality at sea in Atlantic salmon: polygenic multilocus analysis surpasses genome scan. Molecular Ecology 2014; 23:4444-4457 10.1111/mec.12798 PMID: 24845361
74. Hamblin M.T., Warburton M.L., Buckler E.S. Empirical comparison of simple sequence repeats and single nucleotide polymorphisms in assessment of maize diversity and relatedness. PLoS One 2007; 2:e1367 PMID: 18159250
75. Willyard A., Syring J., Gernandt D.S., Liston A., Cronn R. Fossil calibration of molecular divergence infers a moderate mutation rate and recent radiations for Pinus. Molecular Biology and Evolution 2008; 24:90-101
76. Nielsen R. Molecular signatures of natural selection. Annual Review of Genetics 2005; 39:197-218 PMID: 16285858
77. Lewontin R.C., Krakauer J.C. Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics 1973; 74:175-195 PMID: 4711903
78. Martinoia E., Klein M., Geisler M., Bovet L., Forestier C., Kolukisaoglu U., et al. Multifunctionality of plant ABC transporters - More than just detoxifiers. Planta 2002; 214:345-355 PMID: 11855639
79. Eckert A.J., van Heerwaarden J, Wegrzyn JL, Nelson CD, Ross-Ibarra J, González-Martínez SC, Neale DB. Patterns of population structure and environmental associations to aridity across the range of loblolly pine (Pinus taeda L., Pinaceae). Genetics 2010; 185:969-982 10.1534/genetics.110.115543 PMID: 20439779
80. Leips J., Mackay T.F.C. Quantitative trait loci for lifespan in Drosophila melanogaster: interactions with genetic background and larval density. Genetics 2000; 155:1773-1788 PMID: 10924473
81. Hoffmann A.A., Willi Y. Detecting genetic response to environmental change. Nature Review Genetics 2008; 9:421-432
82. Keller S.R., Levsen N., Olson M.S., Tiffin P. Local adaptation in the flowering-time gene network of balsam poplar, Populus balsamifera L. Molecular Biology and Evolution. 2012; 29:3143-3152. PMID: 22513286
83. Prunier L., Gerardi S., Laroche J., Beaulieu J., Bousquet J. Parallel and lineage-specific molecular adaptation to climate in boreal black spruce. Molecular Ecology 2012; 21:4270-4286 10.1111/j.1365-294X.2012.05691.x PMID: 22805595
84. Holliday J.A., Wang T., Aitken S.N. Predicting adaptive phenotypes from multilocus genotypes in Sitka spruce (Picea sitchensis) using random forest. Genes, Genomes, and Genetics 2012; 2:1085-1083
85. Eckert A.J., Wegrzyn J.L., Liechty J.D., Lee J.M., Cumbie W.P., Davis J.M., et al. The evolutionary genetics of the genes underlying phenotypic associations for loblolly pine (Pinus taeda, Pinaceae)Genetics 2013; 195:1353-1372 10.1534/genetics.113.157198 PMID: 24121773
86. Gugger P.F., Ikegami M., Sork V.L. Influence of late Quaternary climate change on present patterns of genetic variation in valley oak, Quercus lobata Née. Molecular Ecology. 2013; 22:3598-3612. 10.1111/mec.12317 PMID: 23802553
87. Grattapaglia D., Resende M.D.V. Genomic selection in forest tree breeding. Tree Genetics and Genomes 2011; 7:241-255
88. Alberto F.J., Aitken S.N., Alia R., Gonzalez-Martinez S.C., Hanninen H., Kremer A., et al. Potential for evolutionary responses to climate change - Evidence from tree populations. Global Change Biology 2013; 19:1645-1661 10.1111/gcb.12181 PMID: 23505261
89. Wang T., O'Neill G.A., Aitken S.N. Integrating environmental and genetic effects to predict responses of tree populations to climate. Ecological Applications 2010; 20:153-163 PMID: 20349837
90. Berg J.J., Coop G. The population genetic signature of polygenic local adaptation. 2014; arXiv:1307.7759.
91. Slatkin M. Isolation by distance in equilibrium and non-equilibrium populations. Evolution 1993; 47:264-279
92. Klütsch C.F.C., Dyer R.J., Misof B. Combining multiple analytical approaches for the identification of population structure and genetic delineation of two subspecies of the endemic Arabian burnet moth Reissita simonyi (Zygaenidae; Lepidoptera). Conservation Genetics 2012; 13:21-37
93. Albert E.M., Fortuna M.A., Godoy J.A., Bascompte J. Assessing the robustness of networks of spatial genetic variation. Ecology Letters 2013; 16:86-93 10.1111/ele.12061 PMID: 23294521
94. Bradburd G.S., Ralph P.L., Coop G.M. Disentangling the effects of geographic and ecological isolation on genetic differentiation. Evolution 2013; 67:3258-3273 10.1111/evo.12193 PMID: 24102455