Evidence for extensive parallelism but divergent genomic architecture of adaptation along altitudinal and latitudinal gradients in Populus trichocarpa

New Phytologist

Volumn 209, Issue 3, 2016, Pages 1240-1251

  Holliday, Jason A ^a   Zhou, Lecong ^a   Bawa, Rajesh ^a   Zhang, Man ^a   Oubida, Regis W ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Populus trichocarpa; Genomic architecture; Local adaptation; Parallel adaptation; Sequence capture

Indexed keywords

ALLELE; DECIDUOUS TREE; GENE FLOW; GENOME; LOCAL ADAPTATION; PHENOTYPE;

POPULUS; POPULUS TRICHOCARPA;

ADAPTATION; ALTITUDE; CLUSTER ANALYSIS; CPG ISLAND; GENE LOCUS; GENE ONTOLOGY; GENETICS; PHYSIOLOGY; PLANT GENOME; POPULUS; SINGLE NUCLEOTIDE POLYMORPHISM;

ADAPTATION, PHYSIOLOGICAL; ALTITUDE; CLUSTER ANALYSIS; CPG ISLANDS; GENE ONTOLOGY; GENETIC LOCI; GENOME, PLANT; POLYMORPHISM, SINGLE NUCLEOTIDE; POPULUS;

EID: 84954362814     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13643     Document Type: Article

References (75)

1. Azeez A, Miskolczi P, Tylewicz S, Bhalerao RP. 2014. A tree ortholog of APETALA1 mediates photoperiodic control of seasonal growth. Current Biology 24: 717-724.
2. Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C. 2004. Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427: 164-167.
3. Bohlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O. 2006. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312: 1040-1043.
4. Buerger R, Akerman A. 2011. The effects of linkage and gene flow on local adaptation: a two-locus continent-island model. Theoretical Population Biology 80: 272-288.
5. Chan YF, Marks ME, Jones FC, Villarreal G Jr, Shapiro MD, Brady SD, Southwick AM, Absher DM, Grimwood J, Schmutz J et al. 2010. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327: 302-305.
6. Clague JJ, Mathewes RW. 1989. Early Holocene thermal maximum in western North America - new evidence from Castle Peak, British Columbia. Geology 17: 277-280.
7. Clague JJ, Mathewes RW, Guilbault JP, Hutchinson I, Ricketts BD. 1997. Pre-Younger Dryas resurgence of the southwestern margin of the Cordilleran ice sheet, British Columbia, Canada. Boreas 26: 261-277.
8. Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G Jr, Dickson M, Grimwood J, Schmutz J, Myers RM, Schluter D, Kingsley DM. 2005. Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307: 1928-1933.
9. Conte GL, Arnegard ME, Peichel CL, Schluter D. 2012. The probability of genetic parallelism and convergence in natural populations. Proceedings of the Royal Society B 279: 5039-5047.
10. Cooke JEK, Eriksson ME, Junttila O. 2012. The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant, Cell & Environment 35: 1707-1728.
11. Cruickshank TE, Hahn MW. 2014. Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Molecular Ecology 23: 3133-3157.
12. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST et al. 2011. The variant call format and VCFtools. Bioinformatics 27: 2156-2158.
13. Delmore KE, Hubner S, Kane NC, Schuster R, Andrew RL, Camara F, Guigo R, Irwin DE. 2015. Genomic analysis of a migratory divide reveals candidate genes for migration and implicates selective sweeps in generating islands of differentiation. Molecular Ecology 24: 1873-1888.
14. Ding Z, Millar AJ, Davis AM, Davis SJ. 2007. TIME FOR COFFEE encodes a nuclear regulator in the Arabidopsis thaliana circadian clock. Plant Cell 19: 1522-1536.
15. Emelianov I, Marec F, Mallet J. 2004. Genomic evidence for divergence with gene flow in host races of the larch budmoth. Proceedings of the Royal Society B: Biological Sciences 271: 97-105.
16. Evans LM, Slavov GT, Rodgers-Melnick E, Martin J, Ranjan P, Muchero W, Brunner AM, Schackwitz W, Gunter L, Chen J-G et al. 2014. Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations. Nature Genetics 46: 1089-1096.
17. Farre EM, Harmer SL, Harmon FG, Yanovsky MJ, Kay SA. 2005. Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Current Biology 15: 47-54.
18. Feder JL, Nosil P. 2010. The efficacy of divergence hitchhiking in generating genomic islands during ecological speciation. Evolution 64: 1729-1747.
19. Flaxman SM, Wacholder AC, Feder JL, Nosil P. 2014. Theoretical models of the influence of genomic architecture on the dynamics of speciation. Molecular Ecology 23: 4074-4088.
20. 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.
21. Fulton RJ. 1991. A conceptual model for growth and decay of the Cordilleran ice sheet. Géographie Physique et Quaternaire 45: 281-286.
22. Geraldes A, Farzaneh N, Grassa CJ, McKown AD, Guy RD, Mansfield SD, Douglas CJ, Cronk QCB. 2014. Landscape genomics of Populus trichocarpa: the role of hybridization, limited gene flow, and natural selection in shaping patterns of population structure. Evolution 68: 3260-3280.
23. Gornall JL, Guy RD. 2007. Geographic variation in ecophysiological traits of black cottonwood (Populus trichocarpa). Canadian Journal of Botany-Revue Canadienne De Botanique 85: 1202-1213.
24. Guo HW, Yang WY, Mockler TC, Lin CT. 1998. Regulations of flowering time by Arabidopsis photoreceptors. Science 279: 1360-1363.
25. Hazen SP, Schultz TF, Pruneda-Paz JL, Borevitz JO, Ecker JR, Kay SA. 2005. LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proceedings of the National Academy of Sciences, USA 102: 10 387-10 392.
26. He YH, Michaels SD, Amasino RM. 2003. Regulation of flowering time by histone acetylation in Arabidopsis. Science 302: 1751-1754.
27. 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-Revue Canadienne De Botanique 81: 1247-1266.
28. Hsu C-Y, Adams JP, Kim H, No K, Ma C, Strauss SH, Drnevich J, Vandervelde L, Ellis JD, Rice BM et al. 2011. FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. Proceedings of the National Academy of Sciences, USA 108: 10 756-10 761.
29. Hudson M, Ringli C, Boylan MT, Quail PH. 1999. The FAR1 locus encodes a novel nuclear protein specific to phytochrome A signaling. Genes & Development 13: 2017-2027.
30. Ibanez C, Kozarewa I, Johansson M, Ogren E, Rohde A, Eriksson ME. 2010. Circadian clock components regulate entry and affect exit of seasonal dormancy as well as winter hardiness in Populus trees. Plant Physiology 153: 1823-1833.
31. Ingvarsson PK. 2008. Multilocus patterns of nucleotide polymorphism and the demographic history of Populus tremula. Genetics 180: 329-340.
32. Ingvarsson PK, Garcia MV, Hall D, Luquez V, Jansson S. 2006. Clinal variation in phyB2, a candidate gene for day-length-induced growth cessation and bud set, across a latitudinal gradient in European aspen (Populus tremula). Genetics 172: 1845-1853.
33. James AC, Azevedo RBR, Partridge L. 1995. Cellular basis and developmental timing in a size cline of Drosophila melanogaster. Genetics 140: 659-666.
34. Keller SR, Levsen N, Ingvarsson PK, Olson MS, Tiffin P. 2011. Local selection across a latitudinal gradient shapes nucleotide diversity in balsam poplar, Populus balsamifera L. Genetics 188: 941-952.
35. Keller SR, Levsen N, Olson MS, Tiffin P. 2012. Local adaptation in the flowering-time gene network of balsam poplar, Populus balsamifera L. Molecular Biology and Evolution 29: 3143-3152.
36. Kovanen DJ, Easterbrook DJ. 2002. Timing and extent of Allerod and younger dryas age (ca. 12500-10000 C-14 yr B.P) oscillations of the Cordilleran Ice Sheet in the Fraser Lowland, western north America. Quaternary Research 57: 208-224.
37. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
38. Li H, Durbin R. 2011. Inference of human population history from individual whole-genome sequences. Nature 475: 493-496.
39. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data P. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078-2079.
40. st outlier tests. Molecular Ecology 23: 2178-2192.
41. Maynard-Smith J, Haigh J. 1974. Hitchhiking effect of a favorable gene. Genetics Research 23: 23-35.
42. Menounos B, Osborn G, Clague JJ, Luckman BH. 2009. Latest Pleistocene and Holocene glacier fluctuations in western Canada. Quaternary Science Reviews 28: 2049-2074.
43. Menounos BP. 2002. Climate, fine-sediment transport linkages, Coast Mountains, British Columbia. PhD thesis, University of British Columbia, Vancouver, BC, Canada.
44. Nadeau NJ, Whibley A, Jones RT, Davey JW, Dasmahapatra KK, Baxter SW, Quail MA, Joron M, Ffrench-Constant RH, Blaxter ML et al. 2012. Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing. Philosophical Transactions of the Royal Society B 367: 343-353.
45. Nosil P, Funk DJ, Ortiz-Barrientos D. 2009. Divergent selection and heterogeneous genomic divergence. Molecular Ecology 18: 375-402.
46. Olsen JE, Junttila O, Nilsen J, Eriksson ME, Martinussen I, Olsson O, Sandberg G, Moritz T. 1997. Ectopic expression of oat phytochrome A in hybrid aspen changes critical daylength for growth and prevents cold acclimatization. Plant Journal 12: 1339-1350.
47. Orr HA. 2005. The probability of parallel evolution. Evolution 59: 216-220.
48. Ostry ME, McNabb HS. 1985. Susceptibility of Poplulus species and hybrids to disease in the north central United States. Plant Disease 69: 755-757.
49. Oubida RW, Gantulga D, Zhang M, Zhou L, Bawa R, Holliday JA. 2015. Partitioning of multivariate phenotypes using regression trees reveals complex patterns of adaptation to climate across the range of black cottonwood (Populus trichocarpa). Frontiers in Plant Science 6: 181.
50. Renaut S, Grassa CJ, Yeaman S, Moyers BT, Lai Z, Kane NC, Bowers JE, Burke JM, Rieseberg LH. 2013. Genomic islands of divergence are not affected by geography of speciation in sunflowers. Nature Communications 4: 1827.
51. Renaut S, Owens GL, Rieseberg LH. 2014a. Shared selective pressure and local genomic landscape lead to repeatable patterns of genomic divergence in sunflowers. Molecular Ecology 23: 311-324.
52. Renaut S, Rowe HC, Ungerer MC, Rieseberg LH. 2014b. Genomics of homoploid hybrid speciation: diversity and transcriptional activity of long terminal repeat retrotransposons in hybrid sunflowers. Philosophical Transactions of the Royal Society B: Biological Sciences 369: 20130345.
53. Rogers SM, Bernatchez L. 2005. Integrating QTL mapping and genome scans towards the characterization of candidate loci under parallel selection in the lake whitefish (Coregonus clupeaformis). Molecular Ecology 14: 351-361.
54. Rokas A, Carroll SB. 2008. Frequent and widespread parallel evolution of protein sequences. Molecular Biology and Evolution 25: 1943-1953.
55. Ruonala R, Rinne PLH, Kangasjarvi J, van der Schoot C. 2008. CENL1 expression in the rib meristem affects stem elongation and the transition to dormancy in Populus. Plant Cell 20: 59-74.
56. Savolainen O, Lascoux M, Merila J. 2013. Ecological genomics of local adaptation. Nature Reviews Genetics 14: 807-820.
57. Savolainen O, Pyhajarvi T, Knurr T. 2007. Gene flow and local adaptation in tees. Annual Review of Ecology Evolution and Systematics 38: 595-619.
58. Scheet P, Stephens M. 2006. A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. American Journal of Human Genetics 78: 629-644.
59. Slavov GT, DiFazio SP, Martin J, Schackwitz W, Muchero W, Rodgers-Melnick E, Lipphardt MF, Pennacchio CP, Hellsten U, Pennacchio LA et al. 2012. Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa. New Phytologist 196: 713-725.
60. Smith J. 1977. Why the genome does not congeal. Nature 268: 693-696.
61. Somers DE, Devlin PF, Kay SA. 1998. Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science 282: 1488-1490.
62. Soolanayakanahally RY, Guy RD, Silim SN, Drewes EC, Schroeder WR. 2009. Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar (Populus balsamifera L.). Plant, Cell & Environment 32: 1821-1832.
63. Soria-Carrasco V, Gompert Z, Comeault AA, Farkas TE, Parchman TL, Johnston JS, Buerkle CA, Feder JL, Bast J, Schwander T et al. 2014. Stick insect genomes reveal natural selection's role in parallel speciation. Science 344: 738-742.
64. Staneloni RJ, Rodriguez-Batiller MJ, Legisa D, Scarpin MR, Agalou A, Cerdan PD, Meijer AH, Ouwerkerk PBF, Casal JJ. 2009. Bell-like homeodomain selectively regulates the high-irradiance response of phytochrome A. Proceedings of the National Academy of Sciences, USA 106: 13 624-13 629.
65. Steiner CC, Rompler H, Boettger LM, Schoneberg T, Hoekstra HE. 2009. The genetic basis of phenotypic convergence in beach mice: similar pigment patterns but different genes. Molecular Biology and Evolution 26: 35-45.
66. Turner TL, Hahn MW, Nuzhdin SV. 2005. Genomic islands of speciation in Anopheles gambiae. PLoS Biology 3: 1572-1578.
67. Via S. 2012. Divergence hitchhiking and the spread of genomic isolation during ecological speciation-with-gene-flow. Philosophical Transactions of the Royal Society B 367: 451-460.
68. Via S, West J. 2008. The genetic mosaic suggests a new role for hitchhiking in ecological speciation. Molecular Ecology 17: 4334-4345.
69. Weinreich DM, Delaney NF, DePristo MA, Hartl DL. 2006. Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312: 111-114.
70. Weinreich DM, Watson RA, Chao L, Harrison R. 2005. Perspective: sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59: 1165-1174.
71. Xie CY, Ying CC, Yanchuk AD, Holowachuk DL. 2009. Ecotypic mode of regional differentiation caused by restricted gene migration: a case in black cottonwood (Populus trichocarpa) along the Pacific Northwest coast. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 39: 519-526.
72. Yeaman S. 2013. Genomic rearrangements and the evolution of clusters of locally adaptive loci. Proceedings of the National Academy of Sciences, USA 110: E1743-E1751.
73. Yeaman S, Whitlock MC. 2011. The genetic architecture of adaptation under migration-selection balance. Evolution 65: 1897-1911.
74. Zhou L, Bawa R, Holliday JA. 2014. Exome resequencing reveals signatures of demographic and adaptive processes across the genome and range of black cottonwood (Populus trichocarpa). Molecular Ecology 23: 2486-2499.
75. Zwaan BJ, Azevedo RBR, James AC, Van 'T Land J, Partridge L. 2000. Cellular basis of wing size variation in Drosophila melanogaster: a comparison of latitudinal clines on two continents. Heredity 84: 338-347.