Cross-species outlier detection reveals different evolutionary pressures between sister species

New Phytologist

Volumn 204, Issue 1, 2014, Pages 215-229

  Cullingham, Catherine I ^a   Cooke, Janice E K ^a   Coltman, David W ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Adaptive variation; Environmental correlation; Jack pine (Pinus banksiana); Lodgepole pine (Pinus contorta var. latifolia); Outlier detection; Selection

Indexed keywords

ADAPTATION; BEETLE; CONIFEROUS TREE; EVOLUTIONARY BIOLOGY; GENETIC VARIATION; HYBRIDIZATION; NATURAL SELECTION; PEST OUTBREAK; RANGE EXPANSION;

CANADA;

COLEOPTERA; PINUS BANKSIANA; PINUS CONTORTA; PINUS MUGO;

ADAPTATION; BIOLOGICAL MODEL; CANADA; ECOSYSTEM; ENVIRONMENT; EVOLUTION; GENETIC SELECTION; GENETIC VARIATION; GENETICS; HETEROZYGOTE; HYBRIDIZATION; PHYSIOLOGY; PINE; POPULATION GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM;

ADAPTATION, BIOLOGICAL; BIOLOGICAL EVOLUTION; CANADA; ECOSYSTEM; ENVIRONMENT; GENETIC VARIATION; GENETICS, POPULATION; HETEROZYGOTE; HYBRIDIZATION, GENETIC; MODELS, GENETIC; PINUS; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC;

EID: 84906940759     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12896     Document Type: Article

References (121)

1. Aitken SN, Yearman S, Holliday JA, Wang T, Curtis-McLane S. 2008. Adaptation, migration or extirpation: climate change outcomes for tree populations. Evolutionary Applications 1: 95-111.
2. Akashi H. 1999. Inferring the fitness effects of DNA mutations from polymorphism and divergence data: statistical power to detect directional selection under stationarity and recombination. Genetics 15: 221-238.
3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403-410.
4. Andolfatto P. 2005. Adaptive evolution of non-coding DNA in Drosophila. Nature 437: 1149-1152.
5. Arango-Velez A, Meents MJ, Galindo-Ganzález LM, El Kayal W, Cooke BJ, Linsky J, Lusebrink I, Cooke JEK. 2014. Influence of water deficit on the molecular responses of pines to infection by Grosmannia clabigera, a mountain pine beetle fungal associate. Tree Physiology. doi:10.1093/treephys/tpt101.
6. Balding DJ. 2003. Likelihood-based inference for genetic correlation coefficients. Theoretical Population Biology 63: 221-230.
7. Barton NH, Hewitt GM. 1985. Analysis of hybrid zones. Annual Review of Ecology and Systematics 16: 113-148.
8. Beaumont MA, Balding DJ. 2004. Identifying adaptive genetic divergence among populations from genome scans. Molecular Ecology 13: 969-980.
9. Beaumont MA, Nichols RA. 1996. Evaluating loci for use in genetic analysis of population structure. Proceedings of the Royal Society, Series B: Biological Sciences 263: 1619-1626.
10. Bentz BJ, Régnière J, Fettig CJ, Hansen EM, Hayes JL, Hicke JA, Kelsey RG, Negrón JF, Seybold SJ. 2010. Climate change and bark beetles of the western United States and Canada: direct and indirect effects. BioScience 60: 602-613.
11. Bierne N, Borsa P, Daguin C, Jollivet D, Viard F, Bonhomme F, David P. 2003. Introgression patterns in the mosaic hybrid zone between Mytilus edulis and M. galloprovincialis. Molecular Ecology 12: 447-461.
12. Bierne N, Roze D, Welch JJ. 2013. Pervasive selection or is it.? Why are Fst outliers sometimes so frequent? Molecular Ecology 22: 2061-2064.
13. Bierne N, Welch JJ, Loire E, Bonhomme F, David P. 2011. The coupling hypothesis: why genome scans may fail to map local adaptation genes. Molecular Ecology 20: 2044-2072.
14. Borcard D, Legendre P, Drapeau P. 1992. Partialling out the spatial component of ecological variation. Ecology 73: 1045-1055.
15. ter Braak CJF, Verdonschot PFM. 1995. Canonical correspondence analysis and related multivariate methods in aquatic ecology. Aquatic Sciences 57: 256-289.
16. Bradbury IA, Hubert S, Higgens B, Borza T, Bowman S, Paterson IG, Snelgrove PVR, Morris CJ, Gregory RS, Hardie DC et al. 2010. Parallel adaptive evolution of Atlantic cod on both sides of the Atlantic Ocean in response to temperature. Proceedings of the Royal Society, Series B: Biological Sciences 277: 3725-3734.
17. Campbell LG, Snow AA, Sweeney PM. 2009. When divergent life histories hybridize: insights into adaptive live-history traits in an annual weed. New Phytologist 184: 806-818.
18. Carlson MR, Murphy JC, Berger VG, Ryrie LF. 1999. Genetics of elevational adaptations of lodgepole pine in the interior. Journal of Sustainable Forestry 10: 35-44.
19. Carmel L, Wolf YI, Rogozin IB, Koonin EV. 2007. Three distinct modes of intron dynamics in the evolution of eukaryotes. Genome Research 17: 1034-1044.
20. Chamary JV, Hurst LD. 2004. Similar rates but different modes of sequence evolution in introns and at exonic silent sites in rodents: evidence for selectively driven codon usage. Molecular Biology and Evolution 21: 1014-1023.
21. Christiansen E, Waring RH, Berryman AA. 1987. Resistance of conifers to bark beetle attack: searching for general relationships. Forest Ecology and Management 22: 89-106.
22. Conesa A, Götz JM, Garcia-Gomez J, Terol M, Talon M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
23. Coop G, Witonsky D, Di Rienzo A, Pritchard JK. 2010. Using environmental correlations to identify loci underlying local adaptation. Genetics 185: 1411-1423.
24. Cudmore TJ, Björklund N, Carroll AL, Lindgren BS. 2010. Climate change and range expansion of an aggressive bark beetle: evidence of higher beetle reproduction in naïve host tree populations. Journal of Applied Ecology 47: 1036-1043.
25. Cullingham CI, Cooke JEK, Coltman DW. 2013. Effects of introgression on the genetic population structure of two ecologically and economically important conifer species; lodgepole pine (Pinus contorta var. latifolia) and jack pine (Pinus banksiana). Genome 56: 577-585.
26. Cullingham CI, Cooke JEK, Dang S, Davis CS, Cooke BJ, Coltman DW. 2011. Mountain pine beetle host-range expansion threatens the boreal forest. Molecular Ecology 20: 2157-2171.
27. Cullingham CI, James PMA, Cooke JECK, Coltman DW. 2012. Characterizing the physical and genetic structure of the lodgepole pine × jack pine hybrid zone: mosaic structure and differential introgression. Evolutionary Applications 5: 879-891.
28. Dabney A, Storey JD, Warnes GR. 2013. Qvalue: Q-value estimation for false discovery rate control. [WWW document] URL http://www.bioconductor.org/packages/release/bioc/html/qvalue.html [accessed 7 June 2013].
29. 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. Molecular Ecology 22: 1383-1399.
30. Development Core Team R. 2011. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
31. Drake JA, Bird C, Nemesh J, Thomas DJ, Newton-Cheh C, Raymond A, Exoffier L, Altar H, Antonarakis SE, Dermitzakis ET et al. 2006. Conserved noncoding sequences are selectively constrained and not mutation cold spots. Nature Genetics 38: 223-227.
32. Eckert AJ, Bower AD, González-Martínez SC, Wegrzyn JL, Coop G, Neale DB. 2010a. Back to nature: ecological genomics of loblolly pine (Pinus taeda, Pinaceae). Molecular Ecology 19: 3789-3805.
33. Eckert AJ, Bower AD, Jermstad KD, Wegrzyn JL, Knaus BJ, Syring JV, Neale BD. 2013. Multilocus analysis reveal little evidence for lineage-wide adaptive evolution within major clades of soft pines (Pinus subgenus Strobus). Molecular Ecology 22: 5635-5650.
34. Eckert AJ, van Heerwaarden J, Wegrzyn JL, Nelson CD, Ross-Ibarra J, González-Martínez SC, Neal DB. 2010b. Patterns of population structure and environmental associations to aridity across the range of loblolly pine (Pinus taeda L., Pinaceae). Genetics 185: 969-982.
35. Ekblom R, Galindo J. 2011. Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity 107: 1-15.
36. Ellegren H. 2008. Comparative genomics and the study of evolution by natural selection. Molecular Ecology 17: 4586-4596.
37. Endler JA. 1986. Natural selection in the wild. Princeton, NJ, USA: Princeton University Press.
38. Excoffier L, Hofer T, Foll M. 2009. Detecting loci under selection in a hierarchically structured population. Heredity 103: 285-298.
39. Excoffier L, Lischer HEL. 2010. Arelquin suite ver 3.5: a new series of programs to perform population genetic analyses under Linux and Windows. Molecular Ecology Resources 10: 564-567.
40. Foll M, Gaggiotti O. 2008. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180: 977-993.
41. Frankham R. 2012. How closely does genetic diversity in finite populations conform to predictions of neutral theory? Large deficits in regions of low recombination. Heredity 108: 167-178.
42. Freedman AH, Thomassen HA, Buermann W, Smith TB. 2010. Genomic signals of diversification along ecological gradients in a tropical lizard. Molecular Ecology 19: 3773-3788.
43. Fulton TM, Van der Hoeven R, Eannetta NT, Tanksley SD. 2002. Identification, analysis and utilization of conserved ortholog set markers for comparative genomics in higher plants. Plant Cell 14: 1457-1467.
44. Gompert Z, Buerkle CA. 2009. A powerful regression-based method for admixture mapping of isolation across the genome of hybrids. Molecular Ecology 18: 1207-1224.
45. Gompert Z, Buerkle CA. 2010. introgress: a software package for mapping components of isolation in hybrids. Molecular Ecology Resources 10: 378-384.
46. Gosset CC, Bierne N. 2012. Differential introgression from a sister species explains high FST outlier loci within a mussel species. Journal of Evolutionary Biology 26: 14-26.
47. Grant BR, Grant PR. 2008. Fission and fusion of Darwin's finches populations. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 363: 2821-2829.
48. Grossmann TI, Song B-H, Windsor AJ, Mitchell-Olds T, Dixon CJ, Kapralov MV, Filatov DA, Eyre-Walker A. 2010. Genome wide analyses reveal little evidence for adaptive evolution in many plant species. Molecular Biology and Evolution 27: 1822-1832.
49. Hahn MW. 2008. Towards a selection theory of molecular evolution. Evolution 62: 255-265.
50. Hamilton JA, Lexer C, Aitken SN. 2013. Differential introgression reveals candidate genes for selection across a spruce (Picea sitchensis × P. glauca) hybrid zone. New Phytologist 197: 927-938.
51. Hancock AM, Alkorta-Aranburu G, Witonsky DB, Di Rienzo A. 2010. Adaptations to new environments in humans: the role of subtle allele frequency shifts. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365: 2459-2468.
52. Haudry A, Platts AE, Vello E, Hoen DR, Leclercq M, Williamson RJ, Forczek E, Joly-Lopez Z, Steffen JG, Hazzouri KM et al. 2013. An atlas of over 90 000 conserved noncoding sequences yields a detailed map of crucifer regulatory regions. Nature Genetics 45: 891-898.
53. Hoffman AA, Sgrò CM. 2011. Climate change and evolutionary adaptation. Nature 470: 479-485.
54. Hogg EH. 1994. Climate and southern limit of the western Canadian boreal forest. Canadian Journal of Forest Research 24: 1835-1845.
55. Holliday JA, Wang T, Aitken SN. 2012. Predicting adaptive phenotypes from multilocus genotypes in sitka spruce (Picea sitchensis) using random forest. G3: Genes, Genomes, Genetics 2: 1085-1093.
56. Holliday JA, Yuen M, Ritland K, Aitken SN. 2010. Postglacial history of a widespread conifer produces inverse clines in selective neutrality tests. Molecular Ecology 19: 3857-3864.
57. Hough J, Williamson RJ, Wright SI. 2013. Patterns of selection in plant genomes. Annual Review of Ecology, Evolution, and Systematics 44: 31-49.
58. 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. Canadian Journal of Botany 81: 1247-1266.
59. Hudson ME. 2008. Sequencing breakthroughs for genomic ecology and evolutionary biology. Molecular Ecology Resources 8: 3-17.
60. Hutchinson MF, Gessler PE. 1994. Splines - more than just a smooth interpolator. Geoderma 62: 45-67.
61. Jeffreys H. 1961. Theory of probability. Oxford, UK: Oxford University Press.
62. Joost S, Bonin A, Bruford MW, Després L, Conord C, Erhardt G, Taberlet P. 2007. A spatial analysis method (SAM) to detect candidate loci for selection: towards a landscape genomic approach to adaptation. Molecular Ecology 16: 3955-3969.
63. Joost S, Kalbermatten M, Bonin A. 2008. Spatial analysis method (SAM): a software tool combining molecular and environmental data to identify candidate loci for selection. Molecular Ecology Resources 8: 957-960.
64. Kimura M. 1968. Evolutionary rate at the molecular level. Nature 217: 624-626.
65. Kimura M. 1983. The neutral theory of molecular evolution. New York, NY, USA: Cambridge University Press.
66. Kimura M, Maruyama T. 1971. Pattern of neutral polymorphism in a geographically structured population. Genetical Research 18: 125-131.
67. Knobloch IW. 1972. Intergeneric hybridization in flowering plants. Taxon 21: 97-103.
68. Lamesch P, Baradini TZ, Li D, Swarbeck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M et al. 2012. The Arabidopsis information resource (TAIR): improved gene annotation and new tools. Nucleic Acids Research 40: D1202-D1210.
69. Larsson S, Oren R, Waring RH, Barrett JW. 1983. Attacks of mountain pine beetle as related to tree vigor of ponderosa pine. Forest Science 29: 395-402.
70. Legendre P, Gallagher ED. 2001. Ecologically meaningful transformations for ordination of species data. Oecologia 129: 271-280.
71. Lewontin RC, Birch LC. 1966. Hybridiation as a source of variation for adaptation to new environments. Evolution 20: 315-336.
72. Lewontin RC, Krakauer J. 1973. Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics 74: 175-195.
73. Lindner M, Maroschek M, Netherer S, Kremer A, Barbati A, Garcia-Gonzalo J, Seidi R, Delzon S, Corona P, Kolstrom M et al. 2010. Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. Forest Ecology and Management 259: 698-709.
74. Lockton S, Gaut BS. 2005. Plant conserved non-coding sequences and paralogues evoluiont. Trends in Genetics 21: 60-65.
75. Logan JE, Régnière J, Powell JA. 2003. Assessing the impacts of global warming on forest pest dynamics. Frontiers in Ecology and the Environment 1: 130-137.
76. ST outlier tests. Molecular Ecology 23: 2178-2192.
77. Lovett GM, Canham CD, Arthur MA, Weathers KC, Fitzhugh RD. 2006. Forest ecosystem responses to exotic pests and pathogens in eastern North America. BioScience 56: 395-405.
78. Luikart G, England PR, Tallmna D, Jordan S, Taberlet P. 2003. The power and the promise of population genomics: from genotyping to genome typing. Nature Reviews Genetics 4: 981-994.
79. Lusebrink I, Evenden ML, Blanchet EG, Cooke JEK, Erbilgin N. 2011. Effect of water stress and fungal inoculation on monoterpene emission from an historical and a new pine host of the mountain pine beetle. Journal of Chemical Ecology 37: 1013-1026.
80. Luttikhuizen PC, Drent J, Peinjnenburg KTCA, van der Veer HW, Johannesson K. 2012. Genetic architecture in a marine hybrid zone: comparing outlier detection and genomic cline analysis in the bivalve Macoma balthica. Molecular Ecology 21: 3048-3061.
81. Mbogga MS, Hamann A, Wang T. 2009. Historical and projected climate data for natural resource management in western Canada. Agricultural and Forest Meteorology 149: 881-890.
82. McLachlan JS, Hellmann JJ, Schwartz MW. 2007. A framework for debate of assisted migration in an era of climate change. Conservation Biology 21: 297-302.
83. Namroud M-C, Beaulieu J, Juge N, Laroche J, Bousquet J. 2008. Scanning the genome for gene single nucleotide polymorphisms involved in adaptive population differentiation in white spruce. Molecular Ecology 17: 3599-3613.
84. Narum SR, Hess JE. 2011. Comparison of Fst outlier tests for SNP loci under selection. Molecular Ecology Resources 11: 184-194.
85. Neale DB, Savolainen O. 2004. Association genetics of complex traits in conifers. Trends in Plant Science 9: 1360-1385.
86. Nei M, Maruyama T. 1975. Letters to the editors: Lewontin-Krakauer test for neutral genes. Genetics 80: 395.
87. Nei M, Suzuki Y, Nozawa M. 2010. The neutral theory of molecular evolution in the genomic era. Annual Review of Genomics and Human Genetics 11: 265-289.
88. Nielsen EE, Hemmer-Hansen J, Poulsen NA, Loeschcke V, Moen T, Johansen T, Mittelholzer C, Taranger G-L, Ogden R, Carvalho GR. 2009. Genomic signatures of local directional selection in a high gene flow marine organism; the Atlantic cod (Gadus morhua). BMC Evolutionary Biology 9: 276.
89. Nunes VL, Beaumont MA, Butlin RK, Paulo OS. 2011. Multiple approaches to detect outliers in a genome scan for selection in ocellated lizards (Lacerta lepida) along an environmental gradient. Molecular Ecology 20: 193-205.
90. Oksanen J, Guillaume-Blanchet F, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Henry M, Stevens H et al. 2013. vegan:community ecology package. R package version 2.0-9. Vienna, Austria: R Foundation for Statistical Computing. URL http://www.R-project.org/.
91. ST approaches reveal singly nucleotide polymporphisms under selection in goat breeds of North-East Mediterranean. BMC Genetics 10: 7.
92. Parks M, Cronn R, Liston A. 2012. Separating the wehat from the chaff: mitigating the effects of noice ina plastome phylogenomic data set from Pinus L. (Pinaceae). BMC Evolutionary Biology 12: 100.
93. Peakall R, Smouse PE. 2012. GenAlEx 6.5: genetic analysis is Excel. Population genetic software for teaching and research - an update. Bioinformatics 28: 2537-2539.
94. Pelgas B, Bousquet J, Meirmans PG, Ritland K, Isabel N. 2011. QTL mapping in white spuce: gene maps and genomic regions underlying adaptive traits across pedigrees, years and environments. BMC Genomics 12: 145.
95. Pérez-Figueroa A, García-Pereira MJ, Saura M, Rolán-Alvarez E, Caballero A. 2010. Comparing three different methods to detect selective loci using dominant markers. Journal of Evolutionary Biology 23: 2267-2276.
96. Pritchard JK, Di Rienzo A. 2010. Adaptation - not by sweeps alone. Nature Reviews Genetics 11: 665-667.
97. Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
98. Rehfeldt GE, Ying CC, Spittlehouse DL, Hamilton DA Jr. 1999. Genetic responses to climate in Pinus contorta: niche breadth, climate change, and reforestation. Ecological Monographs 69: 375-407.
99. Rigault P, Boyle B, Lepage P, Cooke JEK, Bousquet J, MacKay JJ. 2011. A white spruce gene catalogue resource for conifer genome analyses. Plant Physiology 157: 14-28.
100. Robertson A. 1975. Gene frequency distributions as a test of selective neutrality. Genetics 81: 775-785.
101. Rousset F. 2008. genepop '007: a complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources 8: 103-106.
102. Rweyongeza DM, Dhir NK, Barnhardt LK, Hansen C, Yang R-C. 2007. Population differentiation of the lodgepole pine (Pinus contorta) and jack pine (Pinus banksiana) complex in Alberta: growth, survival, and responses to climate. Canadian Journal of Botany 85: 545-556.
103. Saenz-Romero C, Guries RP, Monk AI. 2001. Landscape genetic structure of Pinus banksiana: allozyme variation. Canadian Journal of Botany 79: 871-878.
104. Siol M, Wright WI, Barrett SCH. 2010. The population genomics of plant adaptation. New Phytologist 188: 313-332.
105. Stebbins GL. 1959. The role of hybridization in evolution. Proceedings of the American Philosophical Society 103: 231-251.
106. Stinchcombe JR, Hoekstra HE. 2007. Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100: 158-170.
107. Storey JD. 2002. A direct approach to false discovery rates. Journal of the Royal Statistical Society. Series B, Statistical Methodology 64: 479-498.
108. Sykes MT. 2001. Modelling the potential distribution and community dynamics of lodgepole pine (Pinus contorta Dougl. Ex Loud.) in Scandinavia. Forest Ecology and Management 141: 69-84.
109. Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BFN, Ferreira de Siquiera M, Grainger A, Hannah L et al. 2004. Extinction risk from climate change. Nature 427: 145-148.
110. Thornton KR, Jensen JD. 2007. Controlling the false-positive rate in multilocus genome scans for selection. Genetics 175: 737-750.
111. Tsumura Y, Ushiyama K, Moriguchi Y, Ueno S, Ihara-Ujino T. 2012. Genome scanning for detecting adaptive genes along environmental gradients in the Japanese conifer, Cryptomeria japonica. Heredity 109: 349-360.
112. Vasemägi A. 2006. The adaptive hypothesis of clinal variation revisited: single-locus clines as a result of spatially restricted gene flow. Genetics 173: 2411-2414.
113. Vasemägi A, Primmer CR. 2005. Challenges for identifying functionally important genetic variation: the promise of combining complementary research strategies. Molecular Ecology 14: 3623-3642.
114. Wakamiya I, Newton RJ, Joghnston JS, Price HJ. 1993. Genome size and environmental factors in the genus Pinus. American Journal of Botany 80: 1235-1241.
115. Wasserman WW, Sandelin A. 2004. Applied bioinformatics for the identification of regulatory elements. Nature Reviews Genetics 5: 276-287.
116. Wheeler NC, Guries RP, O'Malley DM. 1983. Biosystematics of the genus Pinus, subsection Contortae. Biochemical Systematics and Ecology 11: 333-340.
117. Wu TD, Nacu S. 2010. Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26: 873-881.
118. Wu TD, Watanabe CK. 2005. GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21: 1859-1875.
119. Yang R-C, Yeh FC, Yanchuk AD. 1996. A comparison of isozyme and quantitative genetic variation in Pinus contorta ssp. latifolia by FST. Genetics 142: 1045-1052.
120. Yang Z, Nielsen R. 2008. Mutation-selection models of codon substitution and their use to estimate selective strengths on codon usage. Molecular Biology and Evolution 25: 568-579.
121. Yeaman S, Jarvis A. 2006. Regional heterogeneity and gene flow maintain variance in a quantitative trait within populations of lodgepole pine. Proceedings. Biological Sciences/The Royal Society 273: 1587-1593.