The evolutionary history of Nebraska deer mice: Local adaptation in the face of strong gene flow

Molecular Biology and Evolution

Volumn 35, Issue 4, 2018, Pages 792-806

  Pfeifer, Susanne P ^a,b   Laurent, Stefan ^a   Sousa, Vitor C ^c,d   Linnen, Catherine R ^e   Foll, Matthieu ^a   Excoffier, Laurent ^c   Hoekstra, Hopi E ^f   Jensen, Jeffrey D ^a,b  

^a EPFL   (Switzerland)

^b ARIZONA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF BERN   (Switzerland)

^d UNIVERSITY OF LISBON   (Portugal)

^e UNIVERSITY OF KENTUCKY   (United States)

^f HARVARD UNIVERSITY   (United States)

Author keywords

adaptation; cryptic coloration; population genetics

Indexed keywords

ADAPTATION; AGOUTI; ARTICLE; EVOLUTION; GENE FLOW; GENE LOCUS; GENOME ANALYSIS; GENOTYPE; GLACIAL PERIOD; NEBRASKA; NONHUMAN; PEROMYSCUS; PIGMENTATION; POPULATION MIGRATION; SINGLE NUCLEOTIDE POLYMORPHISM; ANIMAL; GENETICS; PHENOTYPE;

ADAPTATION, BIOLOGICAL; ANIMAL MIGRATION; ANIMALS; BIOLOGICAL EVOLUTION; GENE FLOW; PEROMYSCUS; PHENOTYPE; PIGMENTATION;

EID: 85044751455     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msy004     Document Type: Article

References (75)

1. Aeschbacher S, Burger R. 2014. The effect of linkage on establishment and survival of locally beneficial mutations. Genetics 197(1): 317-336.
2. Akaike H. 1974. New look at statistical-model identification. IEEE Trans Automat Contr. 19(6): 716-723.
3. Bagley RK, Sousa VC, NiemillerML, Linnen CR. 2017. History, geography, and host use shape genome-wide patterns of genetic variation in the redhead pine sawfly. Mol Ecol. 26(4): 1022-1044.
4. Barsh GS. 1996. The genetics of pigmentation: from fancy genes to complex traits. Trends Genet. 12(8): 299-305.
5. Browning SR, Browning BL. 2007. Rapid and accurate haplotype phasing andmissing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet. 81(5): 1084-1097.
6. Bulmer MG. 1972. The genetic variability of polygenic characters under optimizing selection, mutation and drift. Genet Res. 19(1): 17-25.
7. Bultman SJ, Klebig ML, Michaud EJ, Sweet HO, Davisson MT, Woychik RP. 1994. Molecular analysis of reverse mutations from nonagouti (a) to black-and-tan (a (t)) and white-bellied agouti (Aw) reveals alternative forms of agouti transcripts. Genes Dev. 8(4): 481-490.
8. Caye K, Deist TM, Martins H, Michel O, Francois O. 2016. TESS3: fast inference of spatial population structure and genome scans for selection. Mol Ecol Res. 16(2): 540-548.
9. Chaves JA, Cooper EA, Hendry AP, Podos J, De Leon LF, Raeymaekers JA, MacMillan WO, Uy JA. 2016. Genomic variation at the tips of the adaptive radiation of Darwin's finches. Mol Ecol. 25(21): 5282-5295.
10. Clarke B, Murray J. 1962. Changes of gene-frequency in Cepaea nemoralis: the estimation of selective values. Heredity 17(4): 467-476.
11. Comeault AA, Soria-Carrasco V, Gompert Z, Farkas TE, Buerkle CA, Parchman TL, Nosil P. 2014. Genome-wide association mapping of phenotypic traits subject to a range of intensities of natural selection in Timema cristinae. Am Nat. 183(5): 711-727.
12. Cook LM, Mani GS. 1980. A migration-selection model for the morph frequency variation in the peppered moth over England and Wales. Biol J Linn Soc. 13(3): 179-198.
13. Crisci J, Poh Y-P, Bean A, Simkin A, Jensen JD. 2012. Recent progress in polymorphism based population genetic inference. J Hered. 103(2): 287-296.
14. Crisci J, Poh Y-P, Mahajan S, Jensen JD. 2013. On the impact of equilibrium assumptions on tests of selection. Front Genet. 4:235.
15. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST. 2011. The variant call format and VCFtools. Bioinformatics 27(15): 2156-2158.
16. DeGiorgio M, Huber CD, Hubisz MJ, Hellmann I, Nielsen R. 2016. SweepFinder2: increased sensitivity, robustness and flexibility. Bioinformatics 32(12): 1895-1897.
17. DePristo M, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, et al. 2011. A framework for variation discovery and genotyping using nextgeneration DNA sequencing data. Nat Genet. 43(5): 491-498.
18. Dice LR. 1941. Variation of the deer-mouse (Peromyscusmaniculatus) on the Sand Hills of Nebraska and adjacent areas. Contrib Lab Vertebrate Biol Univ Michigan. 15:1-19.
19. Dice LR. 1947. Effectiveness of selection by owls of deer mice (Peromyscus maniculatus) which contrast in color with their background. Contrib Lab Vertebrate Biol Univ Michigan. 34:1-20.
20. Endler JA. 1977. Geographic variation, speciation, and clines. Princeton (NJ): Princeton University Press.
21. Excoffier L, Dupanloup I, Huerta-Sanchez E, Sousa VC, Foll M. 2013. Robust demographic inference from genomic and SNP data. PLoS Genet. 9(10): e1003905.
22. Excoffier L, Lischer HE. 2010. Arlequin suite ver 3. 5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 10(3): 564-567.
23. Fariello MI, Boitard S, Naya H, SanCristobal M, Servin B. 2013. Detecting signatures of selection through haplotype differentiation among hierarchically structured populations. Genetics 193(3): 929-941.
24. Feulner PGD, Chain FJJ, PanchalM, Huang Y, Eizaguirre C, KalbeM, Lenz TL, Samonte IE, Stoll M, Bornberg-Bauer E, et al. 2015. Genomics of divergence along a continuum of parapatrick population differentiation. PLoS Genet. 11(7): e1005414.
25. Frichot E, François O, O'Meara B. 2015. LEA: an R package for landscape and ecological association studies. Methods Ecol Evol. 6(8): 925-929.
26. Frichot E, Mathieu F, TrouillonT, BouchardG, François O. 2014. Fast and efficient estimation of individual ancestry coefficients. Genetics 196(4): 973-983.
27. Gompert Z, Lucas LK, Nice CC, Buerkle CA. 2013. Genome divergence and the genetic architecture of barriers to gene flow between Lycaeides and L. melissa. Evolution 67(9): 2498-2514.
28. Haldane JBS. 1930. Enzymes. London/New York: Longmans, Green and Co.
29. Haldane JBS. 1957. The cost of natural selection. J Genet. 55(3): 511-524.
30. Hoekstra HE, Drumm KE, Nachman MW. 2004. Ecological genetics of adaptive color polymorphism in pocket mice: geographic variation in selected and neutral genes. Evolution 58(6): 1329-1341.
31. Jackson IJ. 1994. Molecular and development genetics of mouse coat color. Annu Rev Genet. 28:189-217.
32. Jensen JD, FollM, Bernatchez L. 2016. Introduction: the past, present, and future of genomic scans for selection. Mol Ecol. 25(1): 1-4.
33. Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, Johnson J, Swofford R, Pirun M, Zody MC, White S, et al. 2012. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484(7392): 55-61.
34. Joost S, Vuilleumier S, Jensen JD, Schoville S, Leempoel K, Stucki S, Widmer I, Melodelima C, Rolland J, Manel S. 2013. Uncovering the genetic basis of adaptive change: on the intersection of landscape genomics and theoretical population genetics. Mol Ecol. 22(14): 3659-3665.
35. Kingsley SP, Manceau M, Wiley CD, Hoekstra HE. 2009. Melanism in Peromyscus is caused by independentmutations in Agouti. PLoS One 4(7): e6435.
36. Kirkpatrick M, Barton N. 2006. Chromosome inversions, local adaptation, and speciation. Genetics 173(1): 419-434.
37. Lenormand T. 2002. Gene flow and the limits to natural selection. Cell 17(4): 183-189.
38. Lenormand T, Otto SP. 2000. The evolution of recombination in a heterogeneous environment. Genetics 156(1): 423-438.
39. Li H. 2011. Improving SNP discovery by base alignment quality. Bioinformatics 27(8): 1157-1158.
40. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25(16): 2078-2079.
41. Linnen CR, Hoekstra HE. 2009. Measuring natural selection on genotypes and phenotypes in the wild. Cold Spring Harb Symp Quant Biol. 74:155-168.
42. Linnen CR, Kingsley EP, Jensen JD, Hoekstra HE. 2009. On the origin and spread of an adaptive allele in Peromyscus mice. Science 325(5944): 1095-1098.
43. Linnen CR, Poh Y-P, Peterson BK, Barrett RDH, Larson JG, Jensen JD, Hoekstra HE. 2013. Adaptive evolution of multiple traits through multiple mutations at a single gene. Science 339(6125): 1312-1316.
44. Loope DB, Swinehart J. 2000. Thinking like a dune field. Gt Plains Res. 10:5.
45. Lunter G, Goodson M. 2011. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 21(6): 936-939.
46. Mallarino R, Linden TA, Linnen CR, Hoekstra HE. 2017. The role of isoforms in the evolution of cryptic coloration in Peromyscus mice. Mol Ecol. 26(1): 245-258.
47. Manceau M, Domingues VS, Linnen CR, Rosenblum EB, Hoekstra HE. 2010. Convergence in pigmentation at multiple levels: mutations, genes and function. Philos Trans R Soc Lond B Biol Sci. 365(1552): 2439-2450.
48. Manceau M, Domingues VS, Mallarino R, Hoekstra HE. 2011. The developmental role of Agouti in color pattern evolution. Science 331(6020): 1062-1065.
49. Martin M. 2011. Cutadapt removes adapter sequences from highthroughput sequencing reads. EMBnet. journal 17(1): 10-12.
50. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, et al. 2010. The Genome Analysis Toolkit: a MapReduce framework for analyzing nextgeneration DNA sequencing data. Genome Res. 20(9): 1297-1303.
51. Mills MG, Patterson LB. 1994. Not just black and white: pigment pattern development and evolution in vertebrates. Semin Cell Biol. 20:72-81.
52. Montgomerie R. 2006. Analyzing colours. In: Hill GE, McGraw KJ, editors. Bird coloration, Volume I: Mechanisms and measurements. Cambridge (MA): Harvard University Press. p. 90-147.
53. Montgomerie R. 2008. CLR. Version 1. 05. Kingston, Canada: Queens University.
54. Nielsen R, Williamson S, Kim Y, Hubisz MJ, Clark AG, Bustamante C. 2005. Genomic scans for selective sweeps using SNP data. Genome Res. 15(11): 1566-1575.
55. Pfeifer SP. 2017. From next-generation resequencing reads to a high quality variant dataset. Heredity 118(2): 111-124.
56. Pickrell JK, Pritchard JK. 2012. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 8(11): e1002967.
57. Poh Y-P, Domingues V, Hoekstra HE, Jensen JD. 2014. On the prospect of identifying adaptive loci in recently bottlenecked populations: a case study in beach mice. PLoS One 9:e110579.
58. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, de Bakker PIW, Daly MJ, et al. 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 81(3): 559-575.
59. Rafajlovic M, Kleinhans D, Gulliksson C, Fries J, Johansson D, Ardehed A, Sundqvist L, Pereyra RT, Mehlig B, Jonsson PR, et al. 2017. Neutral processes forming large clones during colonization of new areas. J Evol Biol. 30(8): 1544-1560.
60. Ross KG, Keller L. 1995. Joint influence of gene flow and selection on a reproductively important genetic polymorphism in the fire ant Solenopsis invicta. Am Nat. 146(3): 325-348.
61. Rousset F. 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145(4): 1219-1228.
62. Smit AFA, Hubley R, Green P. 2013-2015. RepeatMasker Open-4. 0. Available from: http://www. repeatmasker. org.
63. Smith JM. 1977. Why does the genome not congeal? Nature 268(5622): 693-696.
64. Smouse PE, Long JC, Sokal RR. 1986. Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool. 35(4): 627-632.
65. Sokal RR. 1979. Testing statistical significance of geographic variation patterns. Syst Zool. 28(2): 227-232.
66. Stinchcombe JR, Weinig C, UngererM, Olsen KM, Mays C, Halldorsdottir SS, Purugganan MD, Schmitt J. 2004. A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proc Natl Acad Sci U S A. 101(13): 4712-4717.
67. Tabachnick B, Fidell LS. 2001. Using multivariate statistics. 4th ed. Boston: Allyn and Bacon.
68. Tigano A, Friesen VL. 2016. Genomics of local adaptation with gene flow. Mol Ecol. 25(10): 2144-2164.
69. Van der Auwera GA, CarneiroMO, Hartl C, Poplin R, Del Angel G, Levy-Moonshine A, Jordan T, Shakir K, Roazen D, Thibault J. 2013. From FastQ data to high-confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr Protoc Bioinformatics. 43:11. 10. 1-11. 10. 33.
70. Vrieling H, Duhl DM, Millar SE, Miller KA, Barsh GS. 1994. Differences in dorsal and ventral pigmentation result from regional expression of themouse agouti gene. Proc Natl Acad Sci U S A. 91(12): 5667-5671.
71. Weir BS, Cockerham CC. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38(6): 1358-1370.
72. Yeaman S, Otto SP. 2011. Establishment and maintenance of adaptive genetic divergence under migration, selection, and drift. Evolution 65(7): 2123-2129.
73. Yeaman S, Whitlock MC. 2011. The genetic architecture of adaptation under migration-selection balance. Evolution 65(7): 1897-1911.
74. Zheng X, Levin D, Shen J, Gogarten SM, Laurie C, Weir BS. 2012. A highperformance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28(24): 3326-3328.
75. Zhou X, Carbonetto P, Stephens M. 2013. Polygenic modeling with Bayesian sparse linear mixed models. PLoS Genet. 9(2): e1003264.