Abstract
There is substantial interest in uncovering the genetic basis of the traits underlying adaptive responses in tree species, as this information will ultimately aid conservation and industrial endeavors across populations, generations, and environments. Fundamentally, the characterization of such genetic bases is within the context of a genetic architecture, which describes the mutlidimensional relationship between genotype and phenotype through the identification of causative variants, their relative location within a genome, expression, pleiotropic effect, environmental influence, and degree of dominance, epistasis, and additivity. Here, we review theory related to polygenic local adaptation and contextualize these expectations with methods often used to uncover the genetic basis of traits important to tree conservation and industry. A broad literature survey suggests that most tree traits generally exhibit considerable heritability, that underlying quantitative genetic variation (QST) is structured more so across populations than neutral expectations (FST) in 69% of comparisons across the literature, and that single-locus associations often exhibit small estimated per-locus effects. Together, these results suggest differential selection across populations often acts on tree phenotypes underlain by polygenic architectures consisting of numerous small to moderate effect loci. Using this synthesis, we highlight the limits of using solely single-locus approaches to describe underlying genetic architectures and close by addressing hurdles and promising alternatives towards such goals, remark upon the current state of tree genomics, and identify future directions for this field. Importantly, we argue, the success of future endeavors should not be predicated on the shortcomings of past studies and will instead be dependent upon the application of theory to empiricism, standardized reporting, centralized open-access databases, and continual input and review of the community’s research.
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References
Adams WT, Joly RJ (1980) Linkage relationships among twelve allozyme loci in loblolly pine. J Hered 71:199–202. https://doi.org/10.1093/oxfordjournals.jhered.a109347
Alberto FJ, Aitken SN, Alía R (2013) Potential for evolutionary responses to climate change–evidence from tree populations. Glob Chang Biol 19:1645–1661. https://doi.org/10.1111/gcb.12181
Ali OA, O’Rourke SM, Amish SJ, Meek MH, Luikart G, Jeffres C, Miller MR (2016) RAD capture (Rapture): flexible and efficient sequence-based genotyping. Genetics 202:389–400. https://doi.org/10.1534/genetics.115.183665
Álvarez-Castro JM, Carlborg O (2007) A unified model for functional and statistical epistasis and its application in quantitative trait loci analysis. Genetics 176:1151–1167. https://doi.org/10.1534/genetics.106.067348
Anderson JT, Lee C-R, Rushworth CA et al (2012) Genetic trade-offs and conditional neutrality contribute to local adaptation. Mol Ecol 22:699–708. https://doi.org/10.1111/j.1365-294X.2012.05522.x
Arnold SJ (1992) Constraints on phenotypic evolution. Am Nat 140:S85–S107. https://doi.org/10.1086/285398
Ashander J, Chevin L-M, Baskett ML (2016) Predicting evolutionary rescue via evolving plasticity in stochastic environments. Proc R Soc B Biol Sci 283:20161690–20161610. https://doi.org/10.1098/rspb.2016.1690
Ávila V, Pérez-Figueroa A, Caballero A et al (2014) The action of stabilizing selection, mutation, and drift on epistatic quantitative traits. Evolution 68:1974–1987. https://doi.org/10.1111/evo.12413
Bailey SF, Bataillon T (2016) Can the experimental evolution programme help us elucidate the genetic basis of adaptation in nature? Mol Ecol 25:203–218. https://doi.org/10.1111/mec.13378
Barrett R, Schluter D (2008) Adaptation from standing genetic variation. Trends Ecol Evol 23:38–44. https://doi.org/10.1016/j.tree.2007.09.008
Barton NH (1990) Pleiotropic models of quantitative variation. Genetics 124:773–782
Barton NH (1999) Clines in polygenic traits. Genet Res 74:223–236. https://doi.org/10.1017/S001667239900422X
Barton NH (2017) How does epistasis influence the response to selection? Heredity 118:96–109. https://doi.org/10.1038/hdy.2016.109
Barton NH, Etheridge AM, Véber A (2016) The infinitesimal model. bioRxiv 1–54. doi: https://doi.org/10.1101/039768
Beavis W (1994) The power and deceit of QTL experiments: lessons from comparative QTL studies. Proceedings of the forty-ninth annual corn and sorghum industry research conference. American Seed Trade Association, Chicago, pp 250–266
Bérénos C, Ellis PA, Pilkington JB, Pemberton JM (2014) Estimating quantitative genetic parameters in wild populations: a comparison of pedigree and genomic approaches. Mol Ecol 23:3434–3451. https://doi.org/10.1111/mec.12827
Berg JJ, Coop G (2014) A population genetic signal of polygenic adaptation. PLoS Genet 10:e1004412. https://doi.org/10.1371/journal.pgen.1004412
Bernardo R, Yu JM (2007) Prospects for genomewide selection for quantitative traits in maize. Crop Sci 47:1082–1090. https://doi.org/10.2135/cropsci2006.11.0690
Berry AJ, Ajioka JW, Kreitman M (1991) Lack of polymorphism on the Drosophila fourth chromosome resulting from selection. Genetics 129:1111–1117
Bessega C, Pometti C, Ewens M et al (2015) Evidences of local adaptation in quantitative traits in Prosopis alba (Leguminosae). Genetica 143:31. https://doi.org/10.1007/s10709-014-9810-5
Blanquart F, Kaltz O, Nuismer SL, Gandon S (2013) A practical guide to measuring local adaptation. Ecol Lett 16:1195–1205. https://doi.org/10.1111/ele.12150
Bontemps A, Lefèvre F, Davi H, Oddou-Muratorio S (2016) In situ marker-based assessment of leaf trait evolutionary potential in a marginal European beech population. J Evol Biol 29:514–527.https://doi.org/10.1111/jeb.12801
Boshier D, Broadhurst L, Cornelius J et al (2015) Is local best? Examining the evidence for local adaptation in trees and its scale. Environ Evid 4:1–10. https://doi.org/10.1186/s13750-015-0046-3
Bower AD, Aitken SN (2008) Ecological genetics and seed transfer guidelines for Pinus albicaulis (Pinaceae). Am J Bot 95:66–76
Boyle EA, Li YI, Pritchard JK (2017) An expanded view of complex traits: from polygenic to omnigenic. Cell 169:1177–1186. https://doi.org/10.1016/j.cell.2017.05.038
Brandvain Y, Wright SI (2016) The limits of natural selection in a non-equilibrium world. Trends Genet 32:201–210. https://doi.org/10.1016/j.tig.2016.01.004
Breiman L (2001) Random Forests. Mach Learn 45:5–32. https://doi.org/10.1023/A:1010933404324
Budde KB, Heuertz M, Hernandez-Serrano A et al (2014) In situ genetic association for serotiny, a fire-related trait, in Mediterranean maritime pine (Pinus pinaster). New Phytol 201:230–241. https://doi.org/10.1111/nph.12483
Bulmer MG (1980) The mathematical theory of quantitative genetics. Genet Res 19:17–25. https://doi.org/10.2307/2531982
Bürger R (1999) Evolution of genetic variability and the advantage of sex and recombination in changing environments. Genetics 153:1055–1069
Bürger R, Akerman A (2011) The effects of linkage and gene flow on local adaptation: a two-locus continent-island model. Theor Popul Biol 80:272–288. https://doi.org/10.1016/j.tpb.2011.07.002
Bürger R, Lynch M (1995) Evolution and extinction in a changing environment: a quantitative-genetic analysis. Evolution 49:151–163. https://doi.org/10.2307/2410301
Burghardt LT, Young ND, Tiffin P (2017) A guide to genome-wide association mapping in plants. Curr Protoc Plant Biol. https://doi.org/10.1002/cppb.20041
Caballero A, Tenesa A, Keightley PD (2015) The nature of genetic variation for complex traits revealed by GWAS and regional heritability mapping analyses. Genetics 201:1601–1613
Ćalić I, Bussotti F, Martínez-García PJ, Neale DB (2015) Recent landscape genomics studies in forest trees. Tree Genet Genomes 12:3. https://doi.org/10.1007/s11295-015-0960-0
Carlborg Ö, Haley CS (2004) Epistasis: too often neglected in complex trait studies? Nat Rev Genet 5:618–625. https://doi.org/10.1038/nrg1407
Carrasco A, Wegrzyn JL, Durán R, Fernández M, Donoso A, Rodriguez V, Neale DB, Valenzuela S (2017) Expression profiling in Pinus radiata infected with Fusarium circinatum. Tree Genet Genomes 13:1665. https://doi.org/10.1007/s11295-017-1125-0
Carter AJR, Hermisson J, Hansen TF (2005) The role of epistatic gene interactions in the response to selection and the evolution of evolvability. Theor Popul Biol 68:179–196. https://doi.org/10.1016/j.tpb.2005.05.002
Castellanos MC, González‐Martínez SC, Pausas JG (2015) Field heritability of a plant adaptation to fire in heterogeneous landscapes. Mol Ecol 24:5633-42. https://doi.org/10.1111/mec.13421
Catchen JM, Hohenlohe PA, Bernatchez L et al (2017) Unbroken: RADseq remains a powerful tool for understanding the genetics of adaptation in natural populations. Mol Ecol Resour 17:362–365. https://doi.org/10.1111/1755-0998.12669
Charlesworth B (2013) Background selection 20 years on: The Wilhelmine E. Key 2012 Invitational Lecture. J Hered 104:161–171
Charlesworth B, Charlesworth D (2010) Elements of evolutionary genetics. Roberts and Company Publishers, Greenwood Village 734 pp.
Chaves JA, Cooper EA, Hendry AP, Podos J, De León LF, Raeymaekers JAM, MacMillan WO, Uy JAC (2016) Genomic variation at the tips of the adaptive radiation of Darwin’s finches. Mol Ecol 25:5282–5295. https://doi.org/10.1111/mec.13743
Cheplick GP (2015) Approaches to plant evolutionary ecology. Oxford University Press, Oxford
Cheverud JM, Routman EJ (1995) Epistasis and its contribution to genetic variance components. Genetics 139:1455–1461
Chevin L-M (2012) Genetic constraints on adaptation to a changing environment. Evolution 67:708–721. https://doi.org/10.1111/j.1558-5646.2012.01809.x
Chevin L-M, Hoffmann AA (2017) Evolution of phenotypic plasticity in extreme environments. Philos Trans Roy Soc B: Biol Sci 372:20160138–20160112. https://doi.org/10.1098/rstb.2016.0138
Chevin L-M, Hospital F (2008) Selective sweep at a quantitative trait locus in the presence of background genetic variation. Genetics 180:1645–1660. https://doi.org/10.1534/genetics.108.093351
Chevin L-M, Lande R (2011) Adaptation to marginal habitats by evolution of increased phenotypic plasticity. J Evol Biol 24:1462–1476. https://doi.org/10.1111/j.1420-9101.2011.02279.x
Chevin L-M, Lande R, Mace GM (2010b) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol 8:e1000357. https://doi.org/10.1371/journal.pbio.1000357
Chevin L-M, Martin G, Lenormand T (2010a) Fisher’s model and the genomics of adaptation: restricted pleiotropy, heterogeneous mutation, and parallel evolution. Evolution 64:3213–3231. https://doi.org/10.1111/j.1558-5646.2010.01058.x
Civelek M, Lusis AJ (2014) Systems genetics approaches to understand complex traits. Nat Rev Genet 15:34–48. https://doi.org/10.1038/nrg3575
Cockerham CC (1954) An extension of the concept of partitioning hereditary variance for analysis of covariances among relatives when epistasis is present. Genetics 39:859–882
Cohen D, Bogeat-Triboulot M-B, Tisserant E, Balzergue S, Martin-Magniette M-L, Lelandais G, Ningre N, R, J-P, Tamby J-P, Le Thiec D, Hummel I (2010) Comparative transcriptomics of drought responses in Populus: a meta-analysis of genome-wide expression profiling in mature leaves and root apices across two genotypes. BMC Genomics 11:630. https://doi.org/10.1186/1471-2164-11-630
Collins S, de Meaux J, Acquisti C (2007) Adaptive walks toward a moving optimum. Genetics 176:1089–1099. https://doi.org/10.1534/genetics.107.072926
Comeault AA, Soria-Carrasco V, Gompert Z et al (2014) Genome-wide association mapping of phenotypic traits subject to a range of intensities of natural selection in Timema cristinae. Am Nat 183:711–727. https://doi.org/10.1086/675497
Comeault AA, Flaxman SM, Riesch R et al (2015) Selection on a genetic polymorphism counteracts ecological speciation in a stick insect. Curr Biol 25:1975–1981. https://doi.org/10.1016/j.cub.2015.05.058
Cornelius J (1994) Heritabilities and additive genetic coefficients of variation in forest trees. Can J For Res 24:372–379. https://doi.org/10.1139/x94-050
Costanza R, d’Arge R, De Groot R et al (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260. https://doi.org/10.1038/387253a0
Cowen L, Ideker T, Raphael BJ, Sharan R (2017) Network propagation: a universal amplifier of genetic associations. Nat Ecol Evol 18:551–562. https://doi.org/10.1038/nrg.2017.38
Crnokrak P, Merilä J (2002). Genetic population divergence: markers and traits. Trends Ecol Evol 17:501. https://doi.org/10.1016/S0169-5347(02)02602-2
Cronn R, Dolan PC, Jogdeo S, Wegrzyn JL, Neale DB, St. Clair JB, Denver DR (2017) Transcription through the eye of a needle: daily and annual cycles of gene expression variation in Douglas Fir needles. bioRxiv. https://doi.org/10.1101/117374
Crow JF (2008) Maintaining evolvability. J Genet 87:349–353. https://doi.org/10.1007/s12041-008-0057-8
Crow JF (2010) On epistasis: why it is unimportant in polygenic directional selection. Philos T Roy Soc B 365:1241–1244. https://doi.org/10.1098/rstb.2009.0275
Cruickshank TE, Hahn MW (2014) Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol Ecol 23:3133–3157. https://doi.org/10.1111/mec.12796
Csilléry K, Lalagüe H, Vendramin GG, González-Martínez SC, Fady B, Oddou-Muratorio S (2014) Detecting short spatial scale local adaptation and epistatic selection in climate-related candidate genes in European beech (Fagus sylvatica) populations. Mol Ecol 23:4696– 4708. https://doi.org/10.1111/mec.12902
De La Torre AR, Li Z, Van de Peer Y, Ingvarsson PK (2017) Contrasting rates of molecular evolution and patterns of selection among gymnosperms and flowering plants. Mol Biol Evol 34:1363–1377. https://doi.org/10.1093/molbev/msx069
De Mita S, Thuillet A-C, Gay L, Ahmadi N, Manel S, Ronfort J, Vigouroux Y (2013) Detecting selection along environmental gradients: analysis of eight methods and their effectiveness for outbreeding and selfing populations. Mol Ecol 22:1383–1399. https://doi.org/10.1111/mec.12182
de Villemereuil P, Gaggiotti OE, Mouterde M, Till-Bottraud I (2015) Common garden experiments in the genomic era: new perspectives and opportunities. Heredity 116:249–254. https://doi.org/10.1038/hdy.2015.93
de Visser JAGM, Cooper TF, Elena SF (2011) The causes of epistasis. P R Soc B-Biol Sci 278:3617–3624. https://doi.org/10.1098/rspb.2011.1537
de Vladar HP, Barton N (2014) Stability and response of polygenic traits to stabilizing selection and mutation. Genetics 197:749–767. https://doi.org/10.1534/genetics.113.159111/-/DC1
Devey ME, Fiddler TA, Liu BH, Knapp SJ, Neale DB (1994) An RFLP linkage map for loblolly pine based on a three-generation outbred pedigree. Theor Appl Genet 88:273–278. https://doi.org/10.1007/BF00223631
Devlin B, Roeder K (1999) Genomic control for association studies. Biometrics 55:997–1004
Dickson SP, Wang K, Krantz I, Hakonarson H, Goldstein DB (2010) Rare variants create synthetic genomewide associations. PLoS Biol 8:e1000294. https://doi.org/10.1371/journal.pbio.1000294
Dittmar EL, Oakley CG, Conner JK, Gould BA, Schemske DW (2016) Factors influencing the effect size distribution of adaptive substitutions. P R Soc B-Biol Sci 283:3065–3068. https://doi.org/10.1098/rspb.2015.3065
Donohue K, Rubio de Casas R, Burghardt L, Kovach K, Willis CG (2010) Germination, post-germination adaptation, and species ecological ranges. Annu Rev Ecol Evol Syst 41:293–319. https://doi.org/10.1146/annurev-ecolsys-102209-144715
Du J, Groover A (2010) Transcriptional regulation of secondary growth and wood formation. J Integr Plant Biol. 52:17–27. https://doi.org/10.1111/j.1744-7909.2010.00901.x
Dungey HS (2001) Pine hybrids—a review of their use performance and genetics. For Ecol Manag 148:243–258. https://doi.org/10.1016/S0378-1127(00)00539-9
East EM (1910) A Mendelian interpretation of variation that is apparently continuous. Am Nat 44:65–82. https://doi.org/10.1086/279117
Eckert AJ, Pande B, Ersoz ES, Wright MH, Rashbrook VK, Nicolet CM, Neale DB (2009) High-throughput genotyping and mapping of single nucleotide polymorphisms in loblolly pine (Pinus taeda L.) Tree Genet Genomes 5:225–234. https://doi.org/10.1007/s11295-008-0183-8
Eckert AJ, Wegrzyn JL, Cumbie WP et al (2012) Association genetics of the loblolly pine (Pinus taeda, Pinaceae) metabolome. New Phytol 193:890–902. https://doi.org/10.1111/j.1469-8137.2011.03976.x
Eckert AJ, Bower AD, Jermstad KD, Wegrzyn JL, Knaus BJ, Syring JV, Neale DB (2013b) Multilocus analyses reveal little evidence for lineage-wide adaptive evolution within major clades of soft pines (Pinus subgenus Strobus). Mol Ecol 22:5635–5650. https://doi.org/10.1111/mec.12514
Eckert AJ, Wegryzn JL, Liechty JD, Lee JM, Cumbie WP, Davis JM, Goldfarb B, Loopstra CA, Palle SR, Quesada T, Langley CH, Neale DB (2013a) The evolutionary genetics of the genes underlying phenotypic associations for loblolly pine (Pinus taeda, Pinaceae). Genetics 195:1353–1372. https://doi.org/10.1534/genetics.113.157198/-/DC1
Eckert AJ, Maloney PE, Vogler DR et al (2015) Local adaptation at fine spatial scales: an example from sugar pine (Pinus lambertiana, Pinaceae). Tree Genet Genomes 11:1–17. https://doi.org/10.1007/s11295-015-0863-0
Ehret GB, Lamparter D, Hoggart CJ, Whittaker JC, Beckmann JS, Kutalik Z, Genetic Investigation of Anthropometric Traits Consortium (2012) A multi-SNP locus-association method reveals a substantial fraction of the missing heritability. Am J Hum Genet 91:863–871. https://doi.org/10.1016/j.ajhg.2012.09.013
Ersoz ES, Wright MH, González-Martínez SC, Langley CH, Neale DB (2010) Evolution of disease response genes in loblolly pine: insights from candidate genes. PLoS ONE 5:e14234. https://doi.org/10.1371/journal.pone.0014234
Evans LM, Kaluthota S, Pearce DW, Allan GJ, Floate K, Rood SB, Whitham TG (2016) Bud phenology and growth are subject to divergent selection across a latitudinal gradient in Populus angustifolia and impact adaptation across the distributional range and associated arthropods. Ecol Evol 6:4565–4581. https://doi.org/10.1002/ece3.2222
Eyre-Walker A (2010) Genetic architecture of a complex trait and its implications for fitness and genomewide association studies. Proc Natl Acad Sci 1752-1756. https://doi.org/10.1073/pnas.0906182107
Eyre-Walker A, Keightley PD (2007) The distribution of fitness effects of new mutations. Nat Rev Genet 8:610–618. https://doi.org/10.1038/nrg2146
Falconer DS (1989) Introduction to quantitative genetics, 3d edn. Longman, New York
Feltus FA (2014) Systems genetics: a paradigm to improve discovery of candidate genes and mechanisms underlying complex traits. Plant Sci 223:45–48. https://doi.org/10.1016/j.plantsci.2014.03.003
Feder JL, Nosil P (2010) The efficacy of divergence hitchhiking in generating genomic islands during ecological speciation. Evolution 64:1729–1747. https://doi.org/10.1111/j.1558-5646.2009.00943.x
Feder JL, Egan SP, Nosil P (2012b) The genomics of speciation-with-gene-flow. Trends Genet 28:342–350. https://doi.org/10.1016/j.tig.2012.03.009
Feder JL, Gejji R, Yeaman S, Nosil P (2012) Establishment of new mutations under divergence and genome hitchhiking. Philos T Roy Soc B 367:461–474. https://doi.org/10.1038/nature08480
Feldman M, Lewontin R (1975) The heritability hang-up. Science 190:1163–1168. https://doi.org/10.1126/science.1198102
Felsenstein J (1976) The theoretical population genetics of variable selection and migration. Annu Rev Genet 10:253–280. https://doi.org/10.1146/annurev.ge.10.120176.001345
Fisher RA (1918) The correlation between relatives on the supposition of Mendelian inheritance. Trans Roy Soc Edinb 52:399–433
Fisher RA (1930) The genetical theory of natural selection: a complete variorum edition. Oxford University Press, Oxford
Forester BR, Lasky JR, Wagner HH, Urban DL (2017) Using genotype-environment associations to identify multilocus local adaptation. bioRxiv 1–24. doi: https://doi.org/10.1101/129460
Franks SJ, Weber JJ, Aitken SN (2013) Evolutionary and plastic responses to climate change in terrestrial plant populations. Evol Appl 7:123–139. https://doi.org/10.1111/eva.12112
Friedline CJ, Lind BM, Hobson EM, Harwood DE, Mix AD, Maloney PE, Eckert AJ (2015) The genetic architecture of local adaptation I: the genomic landscape of foxtail pine (Pinus balfouriana Grev. & Balf.) as revealed from a high-density linkage map. Tree Genet Genomes 11:49. https://doi.org/10.1007/s11295-015-0866-x
Gagnaire P-A, Gaggiotti OE (2016) Detecting polygenic selection in marine populations by combining population genomics and quantitative genetics approaches. Curr Zool 62:603–616. https://doi.org/10.1093/cz/zow088
Gazal S, Finucane HK, Furlotte NA, Loh P, Palamara PF, Liu X, Schoech A, Bulik-Sullivan B, Neale BM, Gusev A, Price A (2017) Linkage disequilibrium–dependent architecture of human complex traits shows action of negative selection. Nat Gen 49:1421-1427 https://doi.org/10.1038/ng.3954
Gibson G (2012) Rare and common variants: twenty arguments. Nat Rev Genet 13:135–145. https://doi.org/10.1038/nrg3118
Gilbert KJ, Whitlock MC (2015) Q ST–F ST comparisons with unbalanced half-sib designs. Mol Ecol Resour 15:262–267. https://doi.org/10.1111/1755-0998.12303
Goddard ME, Wray NR, Verbyla K, Visscher PM (2009) Estimating effects and making predictions from genome-wide marker data. Stat Sci 24:517–529. https://doi.org/10.1214/09-STS306
Gompert Z, Jahner JP, Scholl CF, Wilson JS, Lucas LK, Soria-Carrasco V, Fordyce JA, Nice CC, Buerkle CA, Forister ML (2015) The evolution of novel host use is unlikely to be constrained by trade-offs or a lack of genetic variation. Mol Ecol 24:2777–2793. https://doi.org/10.1111/mec.13199
Gompert Z, Egan SP, Barrett RDH, Feder JL, Nosil P (2016) Multilocus approaches for the measurement of selection on correlated genetic loci. Mol Ecol 26:1–18. https://doi.org/10.1111/mec.13867
Goodnight CJ (1988) Epistasis and the effect of founder events on the additive genetic variance. Evolution 42:441–454. https://doi.org/10.2307/2409030
Göring HHH, Terwilliger JD, Blangero J (2001) Large upward bias in estimation of locus-specific effects from genomewide scans. Am J Hum Genet 69:1357–1369. https://doi.org/10.1086/324471
Grandtner MM (2005) Elsevier’s dictionary of trees: Volume 1: North America. Elsevier
Grattapaglia D (2017) Status and perspectives of genomic selection in forest tree breeding. In: Sorrells ME (ed) Genomic selection for crop improvement. Springer, Cham, pp 199–257
Grattapaglia D, Resende MDV (2011) Genomic selection in forest tree breeding. Tree Genet Genomes 7:241–255. https://doi.org/10.1007/s11295-010-0328-4
Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-test cross: mapping strategy and RAPD markers. Genetics 137:1121–1137
Griswold CK (2015) Additive genetic variation and evolvability of a multivariate trait can be increased by epistatic gene action. J Theor Biol 387:241–257. https://doi.org/10.1016/j.jtbi.2015.09.023
Guan Y, Stephens M (2011) Bayesian variable selection regression for genome-wide association studies and other large-scale problems. Ann Appl Stat 5:1780–1815. https://doi.org/10.1214/11-AOAS455
Haldane JBS (1930) A mathematical theory of natural and artificial selection. (Part VI, Isolation.). 26:220–230
Hall D, Hallingbäck HR, Wu HX (2016) Estimation of number and size of QTL effects in forest tree traits. Tree Genet Genomes 12:1–17. https://doi.org/10.1007/s11295-016-1073-0
Hansen TF (2003) Is modularity necessary for evolvability? Biosystems 69:83–94. https://doi.org/10.1016/S0303-2647(02)00132-6
Hansen TF (2006) The evolution of genetic architecture. Annu Rev Ecol Evol Syst 37:123–157. https://doi.org/10.1146/annurev.ecolsys.37.091305.110224
Hansen TF (2013) Why epistasis is important for selection and adaptation. Evolution 67:3501–3511. https://doi.org/10.1111/evo.12214
Hansen TF, Wagner GP (2001) Modeling genetic architecture: a multilinear theory of gene interaction. Theor Popul Biol 59:61–86. https://doi.org/10.1006/tpbi.2000.1508
Hansen TF, Pelabon C, Houle D (2011) Heritability is not evolvability. Evol Biol 38:258–277
Heffner EL, Sorrells ME, Jannink JL (2009) Genomic selection for crop improvement. Crop Sci 49:1–12. https://doi.org/10.2135/cropsci2008.08.0512
Hemani G, Knott S, Haley C (2013) An evolutionary perspective on epistasis and the missing heritability. PLoS Genet 9:e1003295. https://doi.org/10.1371/journal.pgen.1003295
Henderson CR (1975) Best linear unbiased estimation and prediction under a selection model. Biometrics 31:423–447. https://doi.org/10.2307/2529430
Hendry AP (2002) < = ≠ > ?. Trends Ecol Evol 17:502–502. https://doi.org/10.1016/S0169-5347(02)02603-4
Hendry AP (2016) Key questions on the role of phenotypic plasticity in eco-evolutionary dynamics. J Hered 107:25–41. https://doi.org/10.1093/jhered/esv060
Hereford J (2009) A quantitative survey of local adaptation and fitness trade-offs. Am Nat 173:579–588. https://doi.org/10.1086/597611
Hermisson J (2009) Who believes in whole-genome scans for selection? Heredity 103:283–284. https://doi.org/10.1038/hdy.2009.101
Hermisson J, Pennings PS (2005) Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169:2335–2352. https://doi.org/10.1534/genetics.104.036947
Hermisson J, Pennings PS (2017) Soft sweeps and beyond: understanding the patterns and probabilities of selection footprints under rapid adaptation. Methods Ecol Evol 8:700–716. https://doi.org/10.1111/2041-210X.12808
Hermisson J, Hansen TF, Wagner GP (2003) Epistasis in polygenic traits and the evolution of genetic architecture under stabilizing selection. Am Nat 161:708–734. https://doi.org/10.1086/374204
Hill WG (2010) Understanding and using quantitative genetic variation. Philos T Roy Soc B 365:73–85
Hill WG, Goddard ME, Visscher PM (2008) Data and theory point to mainly additive genetic variance for complex traits. PLoS Genet 4:e1000008. https://doi.org/10.1371/journal.pgen.1000008
Hirschhorn JN, Daly MJ (2005) Genome-wide association studies for common diseases and complex traits. Nat Rev Genet 6:95–108. https://doi.org/10.1038/nrg1521
Hoban S, Kelley JL, Lotterhos KE et al (2016) Finding the genomic basis of local adaptation: Pitfalls, practical solutions, and future directions. Am Nat 188:379–397. https://doi.org/10.1086/688018
Hodgins KA, Yeaman S, Nurkowski KA et al (2016) Expression divergence is correlated with sequence evolution but not positive selection in conifers. Mol Biol Evol 33:1502–1516. https://doi.org/10.1093/molbev/msw032
Hoffmann AA, Rieseberg LH (2008) Revisiting the impact of inversions in evolution: From population genetic markers to drivers of adaptive shifts and speciation? Annu Rev Ecol Evol Syst 39:21–42. https://doi.org/10.1146/annurev.ecolsys.39.110707.173532
Holliday JA, Wang T, Aitken SN (2012) Predicting adaptive phenotypes from multilocus genotypes in Sitka spruce (Picea sitchensis) using random forest. G3-Genes Genom Genet 2:1085–1903. https://doi.org/10.1534/g3.112.002733/-/DC1
Holliday JA, Zhou L, Bawa R, Zhang M, Oubida RW (2016) Evidence for extensive parallelism but divergent genomic architecture of adaptation along altitudinal and latitudinal gradients in Populus trichocarpa. New Phytol 209:1240–1251. https://doi.org/10.1111/nph.13643
Holliday JA, Aitken SN, Cooke JEK, Fady B, González-Martínez SC, Heuertz M, Jaramillo-Correa JP, Lexer C, Staton M, Whetten RW, Plomion C (2017) Advances in ecological genomics in forest trees and applications to genetic resources conservation and breeding. Mol Ecol 26:706–717. https://doi.org/10.1111/mec.13963
Hornoy B, Pavy N, Gérardi S, Beaulieu J, Bousquet J (2015) Genetic adaptation to climate in white spruce involves small to moderate allele frequency shifts in functionally diverse genes. Genome Biol Evol 7:3269–3285. https://doi.org/10.1093/gbe/evv218
Howe GT, Aitken SN, Neale DB, Jermstad KD, Wheeler NC, Chen THH (2003) From genotype to phenotype: unraveling the complexities of cold adaptation in forest trees. Can J Bot 81:1247–1266. https://doi.org/10.1139/b03-141
Huang W, Mackay TFC (2016) The genetic architecture of quantitative traits cannot be inferred from variance component analysis. PLoS Genet 12:e1006421. https://doi.org/10.1371/journal.pgen.1006421
Huber CD, Durvasula A, Hancock AM, Lohmueller KE (2017). Gene expression drives the evolution of dominance. bioRxiv. https://doi.org/10.1101/182865
Ingvarsson PK, Hvidsten TR, Street NR (2016) Towards integration of population and comparative genomics in forest trees. New Phytol 212:338–344. https://doi.org/10.1111/nph.14153
Innan H, Kim Y (2004) Pattern of polymorphism after strong artificial selection in a domestication event. Proc Natl Acad Sci 101:10667–10672. https://doi.org/10.1073/pnas.0401720101
Isik F, Kumar S, Martínez-García PJ, Iwata H, Yamamoto T (2015) Acceleration of forest and fruit tree domestication by genomic selection. Adv Bot Res 74:93–124. https://doi.org/10.1016/bs.abr.2015.05.002
Iwata H et al (2011) Prospects for genomic selection in conifer breeding: a simulation study of Cryptomeria japonica. Tree Genet Genomes 7:747–758. https://doi.org/10.1007/s11295-011-0371-9
Jain K, Stephan W (2015) Response of polygenic traits under stabilizing selection and mutation when loci have unequal effects. G3-Genes Genom Genet 5:1065–1074. https://doi.org/10.1534/g3.115.017970
Jain K, Stephan W (2017) Rapid adaptation of a polygenic trait after a sudden environmental shift. Genetics 206:389–406. https://doi.org/10.1534/genetics.116.196972
Jansen RC, Tesson BM, Fu J, Yan Y, McIntyre LM (2009) Defining gene and QTL networks. Curr Opin Plant Biol 12:241–246. https://doi.org/10.1016/j.pbi.2009.01.003
Jensen JD (2014) On the unfounded enthusiasm for soft selective sweeps. Nat Commun 5:5281. https://doi.org/10.1038/ncomms6281
Jensen JD, Kim Y, DuMont VB, Aquadro CF, Bustamante CD (2005) Distinguishing between selective sweeps and demography using DNA polymorphism data. Genetics 170:1401–1410. https://doi.org/10.1534/genetics.104.038224
Jiao WB, Schneeberger K (2017) The impact of third generation genomic technologies on plant genome assembly. Curr Opin Plant Biol 36:64–70. https://doi.org/10.1016/j.pbi.2017.02.002
Johnson RC, Nelson GW, Troyer JL, Lautenberger JA, Kessing BD, Winkler CA, O’Brien SJ (2010) Accounting for multiple comparisons in a genome-wide association study (GWAS). BMC Genomics 11:724
Jones AG, Bürger R, Arnold SJ (2014) Epistasis and natural selection shape the mutational architecture of complex traits. Nat Commun 5:3709. https://doi.org/10.1038/ncomms4709
Joo JWJ, Hormozdiari F, Han B, Eskin E (2016) Multiple testing correction in linear mixed models. Genome Biol 17:62
Josephs EB, Lee YW, Stinchcombe JR, Wright SI (2015) Association mapping reveals the role of purifying selection in the maintenance of genomic variation in gene expression. Proc Natl Acad Sci 112:15390–15395. https://doi.org/10.1073/pnas.1503027112
Josephs EB, Wright SI, Stinchcombe JR, Schoen DJ (2017) The relationship between selection, network connectivity, and regulatory variation within a population of Capsella grandiflora. Genome Biol Evol 9:1099–1109. https://doi.org/10.1093/gbe/evx068
Josephs EB, Stinchcombe JR, Wright SI (2017a) What can genome-wide association studies tell us about the evolutionary forces maintaining genetic variation for quantitative traits? New Phytol 214:21–33. https://doi.org/10.1111/nph.14410
Kaplan NL, Hudson RR, Langley CH (1989) The “hitchhiking effect” revisited. Genetics 123:887–899
Kawecki TJ (2008) Adaptation to marginal habitats. Annu Rev Ecol Evol Syst 39:321–342. https://doi.org/10.1146/annurev.ecolsys.38.091206.095622
Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241. https://doi.org/10.1111/j.1461-0248.2004.00684.x
Keightley PD, Eyre-Walker A (2010) What can we learn about the distribution of fitness effects of new mutations from DNA sequence data? Philos T Roy Soc B 365:1187–1193. https://doi.org/10.1098/rstb.2009.0266
Kempthorne O (1954) The correlation between relatives in a random mating population. P Roy Soc B-Biol Sci 143:103–113. https://doi.org/10.1098/rspb.1954.0056
Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge
Kinloch BB Jr, Parks GK, Fowler CW (1970) White pine blister rust: simply inherited resistance in sugar pine. Science 167:193–195. https://doi.org/10.1126/science.167.3915.193
Kirkpatrick M, Barton NH (1997) Evolution of a species’ range. Am Nat 150:1–23. https://doi.org/10.1086/286054
Kirkpatrick M, Barton NH (2006) Chromosome inversions, local adaptation and speciation. Genetics 173:419–434. https://doi.org/10.1534/genetics.105.047985
Kopp M, Hermisson J (2009a) The genetic basis of phenotypic adaptation I: fixation of beneficial mutations in the moving optimum model. Genetics 182:233–249. https://doi.org/10.1534/genetics.108.099820
Kopp M, Hermisson J (2009b) The genetic basis of phenotypic adaptation II: the distribution of adaptive substitutions in the moving optimum model. Genetics 183:1453–1476. https://doi.org/10.1534/genetics.109.106195
Kopp M, Matuszewski S (2013) Rapid evolution of quantitative traits: theoretical perspectives. Evol Appl 7:169–191. https://doi.org/10.1111/eva.12127
Kremer A, Le Corre V (2012) Decoupling of differentiation between traits and their underlying genes in response to divergent selection. Heredity 108:375–385. https://doi.org/10.1038/hdy.2011.81
Kremer A, Ronce O, Robledo-Arnuncio JJ, Guillaume F, Bohrer G, Nathan R, Bridle JR, Gomulkiewicz KEK, Ritlan K, Kuparinen A, Gerber S, Schueler S (2012) Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecol Lett 15:378–392. https://doi.org/10.1111/j.1461-0248.2012.01746.x
Krutovsky KV, Neale DB (2005) Nucleotide diversity and linkage disequilibrium in cold-hardiness- and wood quality-related candidate genes in Douglas fir. Genetics 171:2029–2041. https://doi.org/10.1534/genetics.105.044420
Lamichhaney S, Berglund J, Almén MS, Maqbool K, Grabherr M, Martinez-Barrio A, Promerová M, Rubin CJ, Wang C, Zamani N, Grant BR, Grant PR, Webster MT, Andersson L (2015) Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518:371–375. https://doi.org/10.1038/nature14181
Lamy JB, Bouffier L, Burlett R, Plomion C, Cochard H, Delzon S (2011) Uniform selection as a primary force reducing population genetic differentiation of cavitation resistance across a species range. PLoS ONE 6:e23476. https://doi.org/10.1371/journal.pone.0023476
Lamy JB, Plomion C, Kremer A, Delzon S (2012) < as a signature of canalization. Mol Ecol 21:5646–5655. https://doi.org/10.1111/mec.12017
Lande R (1980) The genetic covariance between characters maintained by pleiotropic mutations. Genetics 94:203–215
Lande R (2009) Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J Evol Biol 22:1435–1446. https://doi.org/10.1111/j.1420-9101.2009.01754.x
Lande R, Arnold S (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226. https://doi.org/10.1111/j.1558-5646.1983.tb00236.x
Langlet O (1971) Two hundred years genecology. Taxon 20:653–721. https://doi.org/10.2307/1218596
Latta RG (1998) Differentiation of allelic frequencies at quantitative trait loci affecting locally adaptive traits. Am Nat 151:283–292. https://doi.org/10.1086/286119
Latta RG (2003) Gene flow, adaptive population divergence and comparative population structure across loci. New Phytol 161:51–58. https://doi.org/10.1046/j.1469-8137.2003.00920.x
Laurent S, Pfeifer SP, Settles ML, Hunter SS, Hardwick KM, Ormond L, Sousa VC, Jensen JD, Rosenblum EB (2016) The population genomics of rapid adaptation: disentangling signatures of selection and demography in white sands lizards. Mol Ecol 25:306–323. https://doi.org/10.1111/mec.13385
Lauteri M, Pliura A, Monteverdi MC, Brugnoli E, Villani F, Eriksson G (2004) Genetic variation in carbon isotope discrimination in six European populations of Castanea sativa Mill. originating from contrasting localities. J Evol Biol 17:1286–1296. https://doi.org/10.1111/j.1420-9101.2004.00765.x
Le Corre V, Kremer A (2012) The genetic differentiation at quantitative trait loci under local adaptation. Mol Ecol 21:1548–1566. https://doi.org/10.1111/j.1365-294X.2012.05479.x
Le Corre V, Kremer A (2003) Genetic variability at neutral markers, quantitative trait loci and trait in a subdivided population under selection. Genetics 164:1205–1219
Le Rouzic A, Álvarez-Castro JM (2016) Epistasis-induced evolutionary plateaus in selection responses. Am Nat 188:E134–E150. https://doi.org/10.1086/688893
Leempoel K, Duruz S, Rochat E, Widmer I, OrozcoterWengel P, Joost S (2017) Simple rules for an efficient use of Geographic Information Systems in molecular ecology. Front Ecol Evol 5:33. https://doi.org/10.3389/fevo.2017.00033
Legendre P, Legendre LF (2012) Numerical ecology (Vol. 24). Elsevier
Leimu R, Fischer M (2008) A meta-analysis of local adaptation in plants. PLoS ONE 3:e4010. https://doi.org/10.1371/journal.pone.0004010.s001
Leinonen PH, Sandring S, Quilot B et al (2009) Local adaptation in European populations of Arabidopsis lyrata (Brassicaceae). Am J Bot 96:1129–1137. https://doi.org/10.3732/ajb.0800080
Leinonen T, McCairns RJS, O'Hara RB, Merilä J (2013) Comparisons: evolutionary and ecological insights from genomic heterogeneity. Nat Rev Genet 14:179–190. https://doi.org/10.1038/nrg3395
Leiserson M, Eldridge JV, Ramachandran S (2013) Network analysis of GWAS data. Curr Opin Genet Dev 23:602–610. https://doi.org/10.1016/j.gde.2013.09.003
Leitch AR, Leitch IJ (2012) Ecological and genetic factors linked to contrasting genome dynamics in seed plants. New Phytol 194:629–646. https://doi.org/10.1111/j.1469-8137.2012.04105.x
Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189. https://doi.org/10.1016/S0169-5347(02)02497-7
Lewontin RC, Krakauer J (1973) Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms
Li Y, Suontoma M, Burdon RD, Dungey HS (2017) Genotype by environment interactions in forest tree breeding: Review of methodology and perspectives on research and application. Tree Genet Genomes 13:60. https://doi.org/10.1007/s11295-017-1144-x
Lind BM, Friedline CJ, Wegrzyn JL, Maloney PE, Vogler DR, Neale DB, Eckert AJ (2017) Water availability drives signatures of local adaptation in whitebark pine (Pinus albicaulis Engelm.) across fine spatial scales of the Lake Tahoe Basin, USA. Mol Ecol 26:3168–3185. https://doi.org/10.1111/mec.14106
Liu J-J Williams H, Li XR, Schoettle AW, Sniezko RA, Murray M, Zamany A, Roke G, Chen H (2017) Profiling methyl jasmonate-responsive transcriptome for understanding induced systemic resistance in whitebark pine (Pinus albicaulis). Plant Mol Biol 95:359–374. https://doi.org/10.1007/s11103-017-0655-z&domain=pdf
Liu J-J, Schoettle AW, Sniezko RA et al (2016) Genetic mapping of Pinus flexilis major gene (Cr4) for resistance to white pine blister rust using transcriptome-based SNP genotyping. BMC Genomics 17:753. https://doi.org/10.1186/s12864-016-3079-2
Loehle C (1988) Tree life history strategies: the role of defenses. Can J For Res 18:209–222
Long AD, Langley CH (1999) The power of association studies to detect the contribution of candidate genetic loci to variation in complex traits. Genome Res 9:720–731
Lopez GA, Potts BM, Vaillancourt RE, Apiolaza LA (2003) Maternal and carryover effects on early growth of Eucalyptus globulus. Can J For Res 33(11):2108–2115. https://doi.org/10.1139/X03-132
Lotterhos KE, Whitlock MC (2014) Evaluation of demographic history and neutral parameterization on the performance of F ST outlier tests. Mol Ecol 23:2178–2192. https://doi.org/10.1111/mec.12725
Lotterhos KE, Whitlock MC (2015) The relative power of genome scans to detect local adaptation depends on sampling design and statistical method. Mol Ecol 24:1031–1046. https://doi.org/10.1111/mec.13100
Lotterhos KE, Hodges K, Yeaman S, Degner J, Aitken S (2017) Modular environmental pleiotropy of genes involved in local adaptation to climate despite physical linkage. bioRxiv. https://doi.org/10.1101/202481
Lowry DB, Hoban S, Kelley JL, Lotterhos KE, Reed LK, Antolin MF, Storfer A (2016) Breaking RAD: an evaluation of the utility of restriction site-associated DNA sequencing for genome scans of adaptation. Mol Ecol Resour 17:142–152. https://doi.org/10.1111/1755-0998.12635
Lowry DB, Hoban S, Kelley JL, Lotterhos KE, Reed LK, Antolin MF, Storfer A (2017) Responsible RAD: Striving for best practices in population genomic studies of adaptation. Mol Ecol Resour 17:366–369. https://doi.org/10.1111/1755-0998.12677
Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, Sunderland
Mackay T (2001) The genetic architecture of quantitative traits. Annu Rev Genet 35:303–339
Mackay TFC (2014) Epistasis and quantitative traits: using model organisms to study gene-gene interactions. Nat Rev Genet 15:22–33. https://doi.org/10.1038/nrg3627
Mackay TFC, Stone EA, Ayroles JF (2009) The genetics of quantitative traits: challenges and prospects. Nat Rev Genet 10:565–577. https://doi.org/10.1038/nrg2612
MacPherson A, Hohenlohe PA, Nuismer SL (2015) Trait dimensionality explains widespread variation in local adaptation. P Roy Soc B-Biol Sci 282:20141570. https://doi.org/10.1098/rspb.2014.1570
Mahalovich MF, Hipkins VD (2011) Molecular genetic variation in whitebark pine (Pinus albicaulis Engelm.) in the Inland West. In: Keane RE, Tomback DF, Murray MP, Smith CM (eds) The future of high-elevation, five-needle white pines in Western North America: Proceedings of the High Five Symposium. 28–30 June 2010; Missoula, MT. Proceedings RMRS-P-63. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fort Collins 376 p
Mähler N, Wang J, Terebieniec BK, Ingvarsson PK, Street NR, Hvidsten TR (2017) Gene co-expression network connectivity is an important determinant of selective constraint. PLoS Genet 13:e1006402. https://doi.org/10.1371/journal.pgen.1006402
Mahler DL, Weber MG, Wagner CE, Ingram T (2017) Pattern and process in the comparative study of convergent evolution. Am Nat 190:S13–S28. https://doi.org/10.1086/692648
Mäki-Tanila A, Hill WG (2014) Influence of gene interaction on complex trait variation with multilocus models. Genetics 198:355–367. https://doi.org/10.1534/genetics.114.165282
Martin G, Lenormand T (2006) A general multivariate extension of Fisher’s geometrical model and the distribution of mutation fitness effects across species. Evolution 60:893–816. https://doi.org/10.1554/05-412.1
Martin G, Lenormand T (2008) The distribution of beneficial and fixed mutation fitness effects close to an optimum. Genetics 179:907–916. https://doi.org/10.1534/genetics.108.087122
Matuszewski S, Hermisson J, Kopp M (2014) Fisher’s geometric model with a moving optimum. Evolution 68:2571–2588. https://doi.org/10.1111/evo.12465
Matuszewski S, Hermisson J, Kopp M (2015) Catch me if you can: Adaptation from standing genetic variation to a moving phenotypic optimum. Genetics 200:1255–1274. https://doi.org/10.1534/genetics.115.178574/-/DC1
Mátyás C (1996) Climatic adaptation of trees: rediscovering provenance tests. Euphytica 92:45–54
Maynard Smith JH, Haigh J (1974) The hitch-hiking effect of a favourable gene. Genet Res 23:23–35
McCandlish DM, Stoltzfus A (2014) Modeling evolution using the probability of fixation: history and implications. Q Rev Biol 89:225–252. https://doi.org/10.1086/677571
McKay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol 17:285–291. https://doi.org/10.1016/S0169-5347(02)02478-3
McKinney GJ, Larson WA, Seeb LW, Seeb JE (2017) RADseq provides unprecedented insights into molecular ecology and evolutionary genetics: comment on Breaking RAD by Lowry et al. (2016). Mol Ecol Resour 17:356–361. https://doi.org/10.1111/1755-0998.12649
Mei W, Stetter MG, Gates DJ, Stitzer MC, Ross-Ibarra J (2017) Adaptation in plant genomes: bigger is different. bioRxiv. https://doi.org/10.1101/196501
Meier JI, Sousa VC, Marques DA, Selz OM Wagner CE, Excoffier L, Seehausen O (2017) Demographic modelling with whole-genome data reveals parallel origin of similar Pundamilia cichlid species after hybridization. Mol Ecol 26:123–141. https://doi.org/10.1111/mec.13838
Messer PW, Petrov DA (2013) Population genomics of rapid adaptation by soft selective sweeps. Trends Ecol Evol 28:659–669. https://doi.org/10.1016/j.tree.2013.08.003
Meuwissen TH, Hayes BJ, Goddard ME (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157:1819–1829
Mitton JB, Williams CG (2006) Gene flow in conifers. In: Williams CG (ed) Landscapes, genomics, and tansgenic conifers. Springer Netherlands, Dordrecht, pp 147–168
Mitton JB, Grant MC, Yoshino AM (1998) Variation in allozymes and stomatal size in pinyon (Pinus edulis, Pinaceae), associated with soil moisture. Am J Bot 85:1262–1265. https://doi.org/10.2307/2446636
Mizrachi E, Verbeke L, Christie N et al (2017) Network-based integration of systems genetics data reveals pathways associated with lignocellulosic biomass accumulation and processing. Proc Natl Acad Sci 114:1195–1200. https://doi.org/10.1073/pnas.1620119114
Moreno G (1994) Genetic architecture, genetic behavior, and character evolution. Annu Rev Ecol Syst 25:31–44. https://doi.org/10.1146/annurev.es.25.110194.000335
Morgenstern EK (1996) Geographic variation in forest trees: genetic basis and application of knowledge in silviculture. UBC Press, Vancouver
Morse AM, Peterson DG, Islam-Faridi MN et al (2009) Evolution of genome size and complexity in Pinus. PLoS ONE 4:e4332. https://doi.org/10.1371/journal.pone.0004332
Moser G, Lee SH, Hayes BJ, Goddard ME, Wray NR, Visscher PM (2015) Simultaneous discovery, estimation and prediction analysis of complex traits using a Bayesian mixture model. PLoS Genet 11:e1004969. https://doi.org/10.1371/journal.pgen.1004969
Namkoong G (1979) Introduction to quantitative genetics in forestry. Technical Bulletin No. 1588. USDA Forest Service, Washington, D. C. 342 pp
Neale DB, Kremer A (2011) Forest tree genomics: growing resources and applications. Nat Rev Genet 12:111–122. https://doi.org/10.1038/nrg2931
Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9:325–330. https://doi.org/10.1016/j.tplants.2004.05.006
Neale DB, Langley CH, Salzberg SL, Wegrzyn JL (2013) Open access to tree genomes: the path to a better forest. Genome Biol 14(6):120. https://doi.org/10.1186/gb-2013-14-6-120
Neale DB, Martínez-García PJ, La Torre De AR, Montanari S, Wei X-X (2017) Novel in-sights into tree biology and genome evolution as revealed through genomics. Annu Rev Plant Biol 68:457–483. https://doi.org/10.1146/annurev-arplant-042916-041049
Nelson RM, Pettersson ME, Carlborg Ö (2013) A century after Fisher: time for a new paradigm in quantitative genetics. Trends Genet 29:669–676. https://doi.org/10.1016/j.tig.2013.09.006
Nilsson-Ehle H (1909) Kreuzungsuntersuchungen an Hafer und Weizen. Lunds Universitets Arsskrift 5:1–122
Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin Y-C, Scofield DG, Vezzi F, Delhomme N, Giacomello S, Alexeyenko A, Vicedomini R, Sahlin K, Sherwood E, Elfstrand M, Gramzow L, Holmberg K, Hällman J, Keech O, Klasson L, Koriabine M, Kucukoglu M, Käller, Luthman J, Lysholm F, Nittylä T, Olson Å, Rilakovic N, Ritland C, Rosselló, Sena J, Svensson T, Talavera-López C, Theißen G, Tuominen H, Vanneste K, Wu Z-Q, Zhang B, Zerbe P, Arvestad L, Bhalerao R, Bohlmann J, Bousquet J, Gil RG, Hvidsten TR, de Jong P, MacKay J, Morgante M, Ritland K, Sundberg B, Thompson SL, de Peer YV, Andersson B, Nilsson O, Ingvarsson PK, Lundeberg J, Jansson S (2013) The Norway spruce genome sequence and conifer genome evolution. Nature 497:570– 584. https://doi.org/10.1038/nature12211
Ohta T (1982) Linkage disequilibrium with the island model. Genetics 101:139–155
Ohta T (1992) The nearly neutral theory of molecular evolution. Annu Rev Ecol Syst 23:263–286. https://doi.org/10.1146/annurev.es.23.110192.001403
Ohta T (1996) The current significance and standing of neutral and nearly neutral theories. BioEssays 18:673–684
Oldfield S, Lusty C, MacKinven A (1998) The world list of threatened trees. World Conservation Press
Orr HA (1998) The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52:935. https://doi.org/10.2307/2411226
Orr HA (2000) Adaptation and the cost of complexity. Evolution 54:13–20. https://doi.org/10.1111/j.0014-3820.2000.tb00002.x
Orr HA (2001) The “sizes” of mutations fixed in phenotypic evolution: a response to Clarke and Arthur. Evol Dev 3:121–123. https://doi.org/10.1046/j.1525-142x.2001.003003121.x
Orr HA (2003) The distribution of fitness effects among beneficial mutations. Genetics 163:1519–1526. https://doi.org/10.1101/SQB.1951.016.01.026
Orr HA (2005) The genetic theory of adaptation: a brief history. Nat Rev Genet 6:119–127. https://doi.org/10.1038/nrg1523
Orr HA (2006) The distribution of fitness effects among beneficial mutations in Fisher's geometric model of adaptation. J Theor Biol 238:279–285. https://doi.org/10.1016/j.jtbi.2005.05.001
Ortiz-Barrientos D, Engelstädter J, Rieseberg LH (2016) Recombination rate evolution and the origin of species. Trends Ecol Evol 31:226–236. https://doi.org/10.1016/j.tree.2015.12.016
Ovaskainen O, Karhunen M, Zheng CH, Cano Arias JM, Merilä J (2011) A new method to uncover signatures of divergent and stabilizing selection in quantitative traits. Genetics 189:621–632
Paaby AB, Rockman MV (2013) The many faces of pleiotropy. Trends Genet 29:66–73. https://doi.org/10.1016/j.tig.2012.10.010
Paixão T, Barton NH (2016) The effect of gene interactions on the long-term response to selection. Proc Natl Acad Sci 113:4422–4427. https://doi.org/10.1073/pnas.1518830113
Palmé AE, Pyhajarvi T, Wachowiak W, Savolainen O (2009) Selection on nuclear genes in a Pinus phylogeny. Mol Biol Evol 26:893–905. https://doi.org/10.1093/molbev/msp010
Parchman TL, Gompert Z, Mudge J, Schilkey FD, Benkman CW, Buerkle CA (2012) Genome-wide association genetics of an adaptive trait in lodgepole pine. Mol Ecol 21:2991–3005. https://doi.org/10.1111/j.1365-294X.2012.05513.x
Parchman TL, Jahner JP, Uckele K, Galland LM (forthcoming) RADseq approaches and applications for forest tree genetics
Patterson HD, Thompson R (1971) Recovery of interblock information when block sizes are unequal. Biometrika 58:545–554
Pavlidis P, Metzler D, Stephan W (2012) Selective sweeps in multilocus models of quantitative traits. Genetics 192:225–239. https://doi.org/10.1534/genetics.112.142547
Pennings PS, Hermisson J (2006a) Soft sweeps III: the signature of positive selection from recurrent mutation. PLoS Genet 2:e186. https://doi.org/10.1371/journal.pgen
Pennings PS, Hermisson J (2006b) Soft sweeps II--Molecular population genetics of adaptation from recurrent mutation or migration. Mol Biol Evol 23:1076–1084. https://doi.org/10.1093/molbev/msj117
Petit RJ, Hampe A (2006) Some evolutionary consequences of being a tree. Annu Rev Ecol 37:187–214
Phillips PC (2008) Epistasis—the essential role of gene interactions in the structure and evolution of genetic systems. Nat Rev Genet 9:855–2527 867. https://doi.org/10.1038/nrg2452
Pickrell JK, Berisa T, Liu JZ, Ségurel L (2016) Detection and interpretation of shared genetic influences on 42 human traits. Nat Genet 48:709–717. https://doi.org/10.1038/ng.3570
Piepho HP, Möhring J, Melchinger AE, Büchse A (2008) BLUP for phenotypic selection in plant breeding and variety testing. 2533. Euphytica 161:209–228. https://doi.org/10.1007/s10681-007-9449-8
Platt A, Vilhjalmsson BJ, Nordborg M (2010) Conditions under which genome-wide association studies will be positively misleading. Genetics 186:1045–1052
Plomion C, Bastien C, Bogeat-Triboulot M-B, Bouffier L, Déjardin A, Duplessis S, Fady B, Geuertz M, Le Gac A-L, Le Provost G, Legué V, Lelu-Walter M-A, Leplé J-C, Maury S, Morel A, Oddou-Muratorio S, Pilate G, Sanchez L, Scotti I, Scotti-Saintagne C, Segura V, T J-F, Vacher C (2016) Forest tree genomics: 10 achievements from the past 10 years and future prospects. Ann For Sci 73:77–103. https://doi.org/10.1007/s13595-015-0488-3
Postma FM, Ågren J (2016) Early life stages contribute strongly to local adaptation in Arabidopsis thaliana. Proc Natl Acad Sci 113:7590–7595. https://doi.org/10.1073/pnas.1606303113
Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904–909. https://doi.org/10.1038/ng1847
Pritchard JK, Di Rienzo A (2010) Adaptation – not by sweeps alone. Nat Rev Genet 11:665–667. https://doi.org/10.1038/nrg2880
Prout T, Barker JSF (1993) F statistics in Drosophila buzzatii: selection, population size and inbreeding. Genetics 134:369–375
Prunier J, Laroche J, Beaulieu J, Bousquet J (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. https://doi.org/10.1111/j.1365-294X.2011.05045.x
Prunier J, Verta J-P, MacKay JJ (2015) Conifer genomics and adaptation: at the crossroads of genetic diversity and genome function. New Phytol 209:44–62. https://doi.org/10.1111/nph.13565
Quesada T, Li Z, Dervinis C, Bocock PN, Tuskan GA, Casella G, Davis JM, Kirst M (2008) Comparative analysis of the transcriptomes of Populus trichocarpa and Arabidopsis thaliana suggests extensive evolution of gene expression regulation in angiosperms. New Phytol 180:408–420. https://doi.org/10.1111/j.1469-8137.2008.02586.x
Ralph P, Coop G (2010) Parallel adaptation: one or many waves of advance of an advantageous allele? Genetics 186:647–668. https://doi.org/10.1534/genetics.110.119594
Rausher MD, Delph LF (2015) Commentary: When does understanding phenotypic evolution require identification of the underlying genes? Evolution 69:1655–1664. https://doi.org/10.1111/evo.12687
Rellstab C, Gugerli F, Eckert AJ, Hancock AM, Holdregger R (2015) A practical guide to environmental association analysis in landscape genomics. Mol Ecol 24:4348–4370. https://doi.org/10.1111/mec.13322
Remington DL (2015) Alleles versus mutations: Understanding the evolution of genetic architecture requires a molecular perspective on allelic origins. Evolution 69:3025–3038. https://doi.org/10.1111/evo.12775
Resende MFR Jr, Muñoz P, Acosta JJ, Peter GF, Davis JM, Grattapaglia D, Resende MDV, Kirst M (2012a) Accelerating the domestication of trees using genomic selection: accuracy of prediction models across ages and environments. New Phytol 193:617–624. https://doi.org/10.1111/j.1469-8137.2011.03895.x
Resende MDV, Resende MFR Jr, Sansaloni CP, Petroli CD, Missiaggia AA, Aguiar AM, Abad JM, Takahashi EK, Rosado AM, Faria DA, Pappas GJ Jr, Kilian A, Grattapaglia D (2012b) Genomic selection for growth and wood quality in Eucalyptus: capturing the missing heritability and accelerating breeding for complex traits in forest trees. New Phytol 194:116–128. https://doi.org/10.1111/j.1469-8137.2011.04038.x
Resende MFR, Muñoz P, Resende MDV, Garrick DJ, Fernando RL, Davis JM, Jokela EJ, Martin TA, Peter GF (2012c) Kirst M. Accuracy of genomic selection methods in a standard data set of loblolly pine (Pinus taeda L.) Genetics 190:1503–1510. https://doi.org/10.1534/genetics.111.137026
Riesch R, Muschick M, Lindtke D, Villoutreix R, Comeault AA, Farkas TE, Lucek K, Hellen E, Soria-Carrasco V, Dennis SR, de Carvalho CF, Safran RJ, Sandoval CP, Feder J, Gries R, Crespi BJ, Gries G, Gompert Z, Nosil P (2017) Transitions between phases of genomic differentiation during stick-insect speciation. Nat Ecol Evol 1:0082. https://doi.org/10.1038/s41559-017-0082
Ritland K, Ritland C (1996) Inferences about quantitative inheritance based on natural population structure in the yellow monkeyflower, Mimulus guttatus. Evolution 50:1074–1082. https://doi.org/10.1111/j.1558-5646.1996.tb02348.x
Ritland K, Krutovsky KV, Tsumura Y, Pelgas B, Isabel N, Bousquet J (2011) Genetic mapping in conifers. In: Genetics, genomics and breeding of conifers, pp. 196–238
Rockman MV (2012) The QTN program and the alleles that matter for evolution: All that’s gold does not glitter. Evolution 66:1–17. https://doi.org/10.1111/j.1558-5646.2011.01486.x
Rodíguez-Quilón I, Santos-del-Blanco L, Serra-Varela MJ, Koskela J, González-Martínez SC, Alía R (2016) Capturing neutral and adaptive genetic diversity for conservation in a highly structured tree species. Ecol Appl 26:2254–2266
Romero IG, Ruvinsky I, Gilad Y (2012) Comparative studies of gene expression and the evolution of gene regulation. Nat Rev Genet 13:505–516. https://doi.org/10.1038/nrg3229
Roschanski AM, Csilléry K, Liepelt S, Oddou-Muratorio S, Ziegenhagen B, Huard F, Ullrich KK, Postolache D, Vendramin GG, Fady B (2016) Evidence of divergent selection at landscape and local scales in Abies alba Mill. in the French Mediterranean Alps. Mol Ecol 25:776–794. https://doi.org/10.1111/mec.13516
Savolainen O, Pyhäjärvi T, Knürr T (2007) Gene flow and local adaptation in trees. Annu Rev Ecol Evol Syst 38:595–619. https://doi.org/10.1146/annurev.ecolsys.38.091206.095646
Savolainen O, Lascoux M, Merilä J (2013) Ecological genomics of local adaptation. Nat Rev Genet 14:807–820. https://doi.org/10.1038/nrg3522
Schoville SD, Bonin A, Francois O et al (2012) Adaptive genetic variation on the landscape: methods and cases. Annu Rev Ecol Evol Syst 43:23–43. https://doi.org/10.1146/annurev-ecolsys-110411-160248
Schrider DR, Kern AD (2016) S/HIC: Robust identification of soft and hard sweeps using machine learning. PLoS Genet 12:e1005928–e1005931. https://doi.org/10.1371/journal.pgen.1005928
Schrider DR, Mendes FK, Hahn MW, Kern AD (2015) Soft shoulders ahead: spurious signatures of soft and partial selective sweeps result from linked hard sweeps. Genetics 200:267–284. https://doi.org/10.1534/genetics.115.174912/-/DC1
Schrider DR, Shanku AG, Kern AD (2016) Effects of linked selective sweeps on demographic inference and model selection. Genetics 204:1207–1223. https://doi.org/10.1534/genetics.116.190223/-/DC1
Searle SR, Casella G, McCulloch CE (1992) Variance components. Wiley, New York 528 pp
Silva-Junior O, Faria DA, Grattapaglia D (2015) A flexible multi-species genome-wide 60K SNP chip developed from pooled resequencing of 240 Eucalyptus tree genomes across 12 species. New Phytol 206:1527–1540. https://doi.org/10.1111/nph.13322
Simons YB, Bullaughey K, Hudson RR, Sella G (2017) A model for the genetic architecture of quantitative traits under stabilizing selection. arXiv 1–76. https://arxiv.org/pdf/1704.06707.pdf
Siol M, Wright S, Barrett S (2010) The population genomics of plant adaptation. New Phytol 188:313–332. https://doi.org/10.1111/j.1469-8137.2010.03401.x
Slate J (2005) Quantitative trait locus mapping in natural populations: progress, caveats and future directions. Mol Ecol 14:363–379. https://doi.org/10.1111/j.1365-294X.2004.02378.x
Slatkin M (1975) Gene flow and selection in a two-locus system. Genetics 81:787–802
Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–793. https://doi.org/10.1126/science.3576198
Smith SD (2016) Pleiotropy and the evolution of floral integration. New Phytol 209:80–85. https://doi.org/10.1111/nph.13583
Sork VL, Aitken SN, Dyer RJ, Eckert AJ, Legendre P, Neale DB (2013) Putting the landscape into the genomics of trees: approaches for understanding local adaptation and population responses to changing climate. Tree Genet Genomes 9:901–911. https://doi.org/10.1007/s11295-013-0596-x
Sork VL, Squire K, Gugger PF, Steele SE, Levy ED, Eckert AJ (2016) Landscape genomic analysis of candidate genes for climate adaptation in a California endemic oak. https://doi.org/10.3732/ajb.1500162
Speed D, Balding DJ (2014) MultiBLUP: improved SNP-based predic- tion for complex traits. Genome Res 24:1550–1557. https://doi.org/10.1101/gr.169375.113
Spencer CCA, Su Z, Donnelly P, Marchini J (2009) Designing genome-wide association studies: sample size, power, imputation, and the choice of genotyping chip. PLoS Genet 5:e1000477. https://doi.org/10.1371/journal.pgen.1000477
Spitze K (1993) Population structure in Daphnia obtusa: quantitative genetic and allozyme variation. Genetics 135:367–374
St Clair JB, Mandel NL, Vance-Borland KW (2005) Genecology of Douglas fir in western Oregon and Washington. Ann Bot 96:1199–1214. https://doi.org/10.1093/aob/mci278
Stephan W (2010) Genetic hitchhiking versus background selection: the controversy and its implications. Philos T Roy Soc B 365:1245–1253. https://doi.org/10.1098/rstb.2009.0278
Stephan W (2015) Signatures of positive selection: from selective sweeps at individual loci to subtle allele frequency changes in polygenic adaptation. Mol Ecol 25:79–88. https://doi.org/10.1111/mec.13288
Stephens M, Balding DJ (2009) Bayesian statistical methods for genetic association studies. Nat Rev Genet 10:681–690. https://doi.org/10.1038/nrg2615
Stinchcombe JR, Hoekstra HE (2008) Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100:158–170. https://doi.org/10.1038/sj.hdy.6800937
Stölting KN, Paris M, Meier C, Heinze B, Castiglione S, Bartha D, Lexer C (2015) Genome-wide patters of differentiation and spatially varying selection between postglacial recolonization lineage of Populus alba (Salicaceae), a widespread forest tree. New Phytol 207:723–734. https://doi.org/10.1111/nph.13392
Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci 100:9440–9445. https://doi.org/10.1073/pnas.1530509100
Strickler SR, Bombarely A, Mueller LA (2012) Designing a transcriptome next-generation sequencing project for a nonmodel plant species. Am J Bot 99:257–266. https://doi.org/10.3732/ajb.1100292
Suren H, Hodgins KA, Yeaman S, Nurkowski KA, Smets P, Rieseberg LH, Aitken SN, Holliday JA (2016) Exome capture from the spruce and pine giga-genomes. Mol Ecol 16:1136–1146. https://doi.org/10.1111/1755-0998.12570
Tan B, Grattapaglia D, Wu HX, Ingvarsson PK (2017) Genomic prediction reveals significant non-additive effects for growth in hybrid Eucalyptus. bioRxiv, 1–35. https://doi.org/10.1101/178160
Temesgen B, Brown GR, Harry DE, Kinlaw CS, Sewell MM (2001) Neale DB. Genetic mapping of expressed sequence tag polymorphism (ESTP) markers in loblolly pine (Pinus taeda L.) Theor Appl Genet 102:664–675. https://doi.org/10.1007/s001220051695
Tenaillon O (2014) The utility of Fisher’s geometric model in evolutionary genetics. Annu Rev Ecol Evol Syst 45:179–201. https://doi.org/10.1146/annurev-ecolsys-120213-091846
Thavamanikumar S, Southerton SG, Bossinger G, Thumma BR (2013) Dissection of complex traits in forest trees—Opportunities for marker-assisted selection. Tree Genet Genomes 9:627–639. https://doi.org/10.1007/s11295-013-0594-z
Tiffin P, Ross-Ibarra J (2014) Advances and limits of using population genetics to understand local adaptation. Trends Ecol Evol 29:673–680. https://doi.org/10.1016/j.tree.2014.10.004
Tigano A, Friesen VL (2016) Genomics of local adaptation with gene flow. Mol Ecol 25:2144–2164. https://doi.org/10.1111/mec.13606
Timpson NJ, Greenwood CMT, Soranzo N, Soranzo Lawson DJ, Richars JB (2018) Genetic architecture: the shape of the genetic contribution to human traits and disease. Nature Rev Genet 19:110–124. https://doi.org/10.1038/nrg.2017.101
Turelli M, Barton NH (1994) Genetic and statistical analyses of strong selection on polygenic traits: what, me normal? Genetics 138:913–941
Vasquez-Gross HA, Yu JJ, Figueroa B, Gessler DD, Neale DB, Wegrzyn JL (2013) CartograTree: connecting tree genomes, phenotypes and environment. Mol Ecol Resour 13:528–537. https://doi.org/10.1111/1755-0998.12067
Via S, Lande R (1985) Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39:505–522. https://doi.org/10.1111/j.1558-5646.1985.tb00391.x
Vialette-Guiraud ACM, Andres-Robin A, Chambrier P, Tavares R, Scutt CP (2016) The analysis of Gene Regulatory Networks in plant evo-devo. J Exp Bot 67:2549–2563. https://doi.org/10.1093/jxb/erw119
Vitezica ZG, Legarra A, Toro MA, Varona L (2017) Orthogonal estimates of variances for additive, dominance, and epistatic effects in populations. Genetics 206:1297–1307. https://doi.org/10.1534/genetics.116.199406
Vizcaíno-Palomar N, Revuelta-Eugercios B, Zavala MA, Alia R, González-Martínez SC (2014) The role of population origin and microenvironment in seedling emergence and early survival in Mediterranean maritime pine (Pinus pinaster Aiton). PLoS ONE 9:e109132. https://doi.org/10.1371/journal.pone.0109132
Wachowiak W, Trivedi U, Perry A, Cavers S (2015) Comparative transcriptomics of a complex of four European pine species. BMC Genomics 16:234. https://doi.org/10.1186/s12864-015-1401-z
Wadgymar SM, Lowry DB, Gould BA, Byron CN, Mactavish RM, Anderson JT (2017) Identifying targets and agents of selection: innovative methods to evaluate the processes that contribute to local adaptation. Methods Ecol Evol 8:738–749. https://doi.org/10.1111/2041-210X.12777
Wagner GP, Altenberg L (1996) Perspective: complex adaptations and the evolution of evolvability. Evolution 50:967. https://doi.org/10.2307/2410639
Wagner GP, Zhang J (2011) The pleiotropic structure of the genotype–phenotype map: the evolvability of complex organisms. Nat Rev Genet 12:204–213. https://doi.org/10.1038/nrg2949
Wagner GP, Pavlicev M, Cheverud JM (2007) The road to modularity. Nat Rev Genet 8:921–931. https://doi.org/10.1038/nrg2267
Wagner GP, Kenney-Hunt JP, Pavlicev M, Peck JR, Waxman D, Cheverud JM (2008) Pleiotropic scaling of gene effects and the ‘cost of complexity’. Nature 452:470–472. https://doi.org/10.1038/nature06756
Wang Z, Liao BY, Zhang J (2010) Genomic patterns of pleiotropy and the evolution of complexity. Proc Natl Acad Sci 107:18034–18039. https://doi.org/10.1073/pnas.1004666107
Wang L, Beissinger TM, Lorant A, Ross-Ibarra C, Ross-Ibarra J, Hufford M (2017) The interplay of demography and selection during maize domestication and expansion. bioRxiv. https://doi.org/10.1101/114579
Wegrzyn JL, Lee JM, Tearse BR, Neale DB (2008) TreeGenes: a forest tree genome database. Int J Plant Genomics 2008:1–7. https://doi.org/10.1155/2008/412875
Wegrzyn JL, Main D, Figueroa B, Choi M, Yu J, Neale DB, Jung S, Lee T, Stanton M, Zheng P, Ficklin S, Cho I, Peace C, Evans K, Volk G (2012) Uniform standards for genome databases in forest and fruit trees. Tree Genet Genomes 8:549–557. https://doi.org/10.1007/s11295-012-0494-7
Welch JJ, Waxman D (2003) Modularity and the cost of complexity. Evolution 57:1723–1713. https://doi.org/10.1554/02-673
Wellenreuther M, Hansson B (2016) Detecting polygenic evolution: problems, pitfalls, and promises. Trends Genet 32:155–164. https://doi.org/10.1016/j.tig.2015.12.004
Whitlock MC (1999) Neutral additive genetic variance in a metapopulation. Genet Res 74:215–221. https://doi.org/10.1017/S0016672399004127
Whitlock MC (2003) Fixation probability and time in subdivided populations. Genetics 164:767–779
Whitlock MC, Gilbert KJ (2012) QST in a hierarchically structured population. Mol Ecol Resour 12:481–483. https://doi.org/10.1111/j.1755-0998.2012.03122.x
Whitlock MC, Guillaume F (2009) Testing for spatially divergent selection: comparing Q ST to F ST. Genetics 183:1055–1063. https://doi.org/10.1534/genetics.108.099812
Whitlock MC, Lotterhos KE (2015) Reliable detection of loci responsible for local adaptation: Inference of a null model through trimming the distribution of F ST. Am Nat 186:S24–S36. https://doi.org/10.1086/682949
Whitlock MC, Phillips PC, Moore FB, Tonsor SJ (1995) Multiple fitness peaks and epistasis. Annu Rev Ecol Syst 26:601–629. https://doi.org/10.1146/annurev.es.26.110195.003125
Wong CK, Bernardo R (2008) Genomewide selection in oil palm: increasing selection gain per unit time and cost with small populations. Theor Appl Genet 116:815–824. https://doi.org/10.1007/s00122-008-0715-5
Wortley AH, Scotland RW (2004) Synonymy, sampling and seed plant numbers. Taxon 53(2):478–480. https://doi.org/10.2307/4135625
Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159
Wright S (1932) The roles of mutation, inbreeding, crossbreeding, and selection in evolution. Proceedings of the Sixth International Congress on Genetics 1:356–366.
Xu S (2003) Theoretical basis of the beavis effect. Genetics 165:2259–2268. https://doi.org/10.1038/hdy.1992.131
Yang J, Benyamin B, McEvoy BP et al (2010) Common SNPs explain a large proportion of the heritability for human height. Nat Genet 42:565–569. https://doi.org/10.1038/ng.608
Yang J, Mezmouk S, Baumgarten A, Buckler ES, Guill KE, McMullen MD, Ross-Ibarra J (2017) Incomplete dominance of deleterious alleles contribute substantially to trait variation and heterosis in maize. bioRxiv. https://doi.org/10.1101/086132
Yeaman S (2013) Genomic rearrangements and the evolution of clusters of locally adaptive loci. Proc Natl Acad Sci 110:E1743–E1751. https://doi.org/10.1073/pnas.1219381110
Yeaman S (2015) Local adaptation by alleles of small effect. Am Nat 186:S74–S89. https://doi.org/10.1086/682405
Yeaman S, Jarvis A (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. https://doi.org/10.1534/genetics.166.2.1053
Yeaman S, Otto SP (2011) Establishment and maintenance of adaptive genetic divergence under migration, selection, and drift. Evolution 65:2123–2129. https://doi.org/10.1111/j.1558-5646.2011.01277.x
Yeaman S, Whitlock MC (2011) The genetic architecture of adaptation under migration-selection balance. Evolution 65:1897–1911. https://doi.org/10.1111/j.1558-5646.2011.01269.x
Yeaman S, Hodgins KA, Lotterhos KE et al (2016) Convergent local adaptation to climate in distantly related conifers. Science 353:1431–1433. https://doi.org/10.1126/science.aaf7812
Yoder JB, Tiffin P (2017) Effects of gene action, marker density, and timing of selection on the performance of landscape genomic scans of local adaptation. J Hered 109:16–28. https://doi.org/10.1093/jhered/esx042
Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2005) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208. https://doi.org/10.1038/ng1702
Zhang X-S (2012) Fisher’s geometric model of fitness landscape and variance in fitness within a changing environment. Evolution 66:2350–2368. https://doi.org/10.1111/j.1558-5646.2012.01610.x
Zhang M, Zhou L, Bawa R, Suren H, Holliday JA (2016) Recombination rate variation, hitchhiking, and demographic history shape deleterious load in poplar. Mol Biol Evol 33:2899–2910. https://doi.org/10.1093/molbev/msw169
Zhong S, Dekkers JC, Fernando RL, Jannink JL (2009) Factors affecting accuracy from genomic selection in populations derived from multiple inbred lines: a barley case study. Genetics 182:355–364. https://doi.org/10.1534/genetics.108.098277
Zhou X, Carbonetto P, Stephens M (2013) Polygenic modeling with Bayesian sparse linear mixed models. PLoS Genet 9(2):e1003264. https://doi.org/10.1371/journal.pgen.1003264
Zinkgraf M, Liu L, Groover A, Filkov V (2017) Identifying gene coexpression networks underlying the dynamic regulation of wood-forming tissues in Populus under diverse environmental conditions. New Phytol 214:1464–1478. https://doi.org/10.1111/nph.14492
Zöllner S, Pritchard JK (2007) Overcoming the Winner’s curse: estimating penetrance parameters from case-control data. Am J Hum Genet 80:605–615. https://doi.org/10.1086/512821
Zuk O, Hechter E, Sunyaev SR (2012) The mystery of missing heritability: genetic interactions create phantom heritability. Proc Natl Acad Sci 109:1193–1198. https://doi.org/10.1073/pnas.1119675109/-/DCSupplemental
Acknowledgements
The authors would like to thank S. González-Martínez for inviting this review, Chris Friedline for stimulating conversations when developing content, and Justin Bagley, Jill Wegrzyn, and two anonymous reviewers for providing helpful comments to earlier versions of this manuscript. Brandon Lind is supported through a Dissertation Fellowship provided by the Graduate School of Virginia Commonwealth University. Andrew Eckert is supported through the National Science Foundation (EF-1442486) and the United States Department of Agriculture (USDA 2016-67013-24469).
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BML and AJE conceived the review, with contributions from MM, CEB, and TMF. BML, MM, CEB, and TMF contributed to the literature search and survey which was analyzed by BML. CEB summarized QST and FST comparisons. BML wrote the manuscript with contributions from MM and AJE. All authors contributed to the editing of the manuscript.
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Lind, B.M., Menon, M., Bolte, C.E. et al. The genomics of local adaptation in trees: are we out of the woods yet?. Tree Genetics & Genomes 14, 29 (2018). https://doi.org/10.1007/s11295-017-1224-y
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DOI: https://doi.org/10.1007/s11295-017-1224-y