Divergent population structure and climate associations of a chromosomal inversion polymorphism across the Mimulus guttatus species complex

Molecular Ecology

Volumn 23, Issue 11, 2014, Pages 2844-2860

  Oneal, Elen ^a   Lowry, David B ^a,b,c   Wright, Kevin M ^a,d   Zhu, Zhirui ^a   Willis, John H ^a,b  

^a DUKE UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

^d HARVARD UNIVERSITY   (United States)

Author keywords

adaptation; chromosomal inversion; climate; cline; ecotypes; life history

Indexed keywords

PLANT DNA;

ADAPTATION; ARTICLE; CHROMOSOME INVERSION; CLIMATE; CLUSTER ANALYSIS; ECOTYPE; ECOTYPES; GENETIC MARKER; GENETIC POLYMORPHISM; GENETICS; LIFE HISTORY; MIMULUS; POPULATION GENETICS; REPRODUCTIVE ISOLATION;

ADAPTATION; CHROMOSOMAL INVERSION; CLIMATE; CLINE; ECOTYPES; LIFE HISTORY;

ADAPTATION, PHYSIOLOGICAL; CHROMOSOME INVERSION; CLUSTER ANALYSIS; DNA, PLANT; ECOTYPE; GENETIC MARKERS; GENETICS, POPULATION; MIMULUS; POLYMORPHISM, GENETIC; REPRODUCTIVE ISOLATION;

EID: 84901370405     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12778     Document Type: Article

References (80)

1. Ayala D, Fontaine MC, Cohuet A, et al,. (2011) Chromosomal inversions, natural selection and adaptation in the malaria vector Anopheles funestus. Molecular Biology and Evolution, 28, 745-758.
2. Ayala D, Guerrero RF, Kirkpatrick M, (2013) Reproductive isolation and local adaptation quantified for a chromosome inversion in a malaria mosquito. Evolution, 67, 946-958.
3. Beardsley PM, Olmstead RG, (2002) Redefining Phrymaceae: the placement of Mimulus, tribe Mimuleae, and Phryma. American Journal of Botany, 89, 1093-1102.
4. Brandvain Y, Kenney AM, Flagel L, Coop G, Sweigart AL, (2013) Speciation and introgression between Mimulus nasutus and Mimulus guttatus. PLoS Genetics, in press. arXiv preprint arXiv:1310.7131.
5. Campbell GR, (1950) Mimulus guttatus and related species. El Aliso, 2, 319-337.
6. Cheng C, White BJ, Kamdem C, et al,. (2012) Ecological genomics of Anopheles gambiae along a latitudinal cline: a population-resequencing approach. Genetics, 190, 1417-1432.
7. Chikhi L, Sousa VC, Luisi P, Goossens B, Beaumont MA, (2010) The confounding effects of population structure, genetic diversity and the sampling scheme on the detection and quantification of population size changes. Genetics, 186, 983-995.
8. Dobzhansky T, (1951) Genetics and the Origin of Species, 3rd edn. Columbia University Press, New York City, New York.
9. Dobzhansky T, (1970) Genetics of the Evolutionary Process. Columbia University Press, New York City, New York.
10. Dole JA, (1992) Reproductive assurance mechanisms in three taxa of the Mimulus guttatus complex (Scrophulariaceae). American Journal of Botany, 1992, 650-659.
11. Dudash MR, Carr DE, (1998) Genetics underlying inbreeding depression in Mimulus with contrasting mating systems. Nature, 393, 682-684.
12. Earl DA, von Holdt BM, (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359-361.
13. Eckert AJ, Carstens BC, (2008) Does gene flow destroy phylogenetic signal? The performance of three methods for estimating species phylogenies in the presence of gene flow. Molecular Phylogenetics and Evolution, 49, 832-842.
14. ESRI (2011) ArcGIS Desktop: Release 10. Environmental Systems Research Institute, Redlands, California.
15. Evanno G, Regnaut S, Goudet J, (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular ecology, 14, 2611-2620.
16. Excoffier L, Lischer HEL, (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567.
17. Fang Z, Pyhäjärvi T, Weber AL, et al,. (2012) Megabase-scale inversion polymorphism in the wild ancestor of maize. Genetics, 191, 883-894.
18. Feder JL, Nosil P, (2009) Chromosomal inversions and species differences: when are genes affecting adaptive divergence and reproductive isolation expected to reside within inversions? Evolution, 63, 3061-3075.
19. Fenster CB, Ritland K, (1994) Evidence for natural selection on mating system in Mimulus (Scrophulaiaceae). International Journal of Plant Sciences, 155, 588-596.
20. Fishman L, Willis JH, Wu CA, Lee Y-W, (2014) Comparative linkage maps suggest that fission, not polyploidy, underlies near-doubling of chromosome number within monkeyflowers (Mimulus; Phrymaceae). Heredity, 112, 562-568.
21. Gardner M, Macnair M, (2000) Factors affecting the co-existence of the serpentine endemic Mimulus nudatus Curran and its presumed progenitor, Mimulus guttatus Fischer ex DC. Biological Journal of the Linnean Society, 69, 443-459.
22. Grant AL, (1924) A monograph of the genus Mimulus. Annals of the Missouri Botanical Garden, 11, 99-389.
23. Hair JF, Anderson RE, Tatham RL, Black WC, (1998) Canonical correlation analysis. In: Multivariate Data Analysis. pp. 442-465. Prentice Hall International, Englewood, New Jersey.
24. Hall MC, Willis JH, (2006) Divergent selection on flowering time contributes to local adaptation in Mimulus guttatus populations. Evolution, 60, 2466-2477.
25. Hall MC, Basten CJ, Willis JH, (2006) Pleiotropic quantitative trait loci contribute to population divergence in traits associated with life history variation in Mimulus guttatus. Genetics, 172, 1829-1844.
26. Hall MC, Lowry DB, Willis JH, (2010) Is local adaptation in Mimulus guttatus caused by trade-offs at individual loci? Molecular Ecology, 19, 2739-2753.
27. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A, (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965-1978.
28. Hitchcock CL, (1959) Vascular plants of the Pacific Northwest: Ericaceae through Campanulaceae (eds, Hitchcock CL, Cronquist A, Ownbey M,), vol. 17. University of Washington Press, Seattle, Washington.
29. Hoffmann AA, Rieseberg LH, (2008) Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation? Annual Review of Ecology and Systematics, 39, 21-42.
30. Jakobsson M, Rosenberg NA, (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23, 1801-1806.
31. Jones FC, Grabherr MG, Chan YF, et al,. (2012a) The genomic basis of adaptive evolution in threespine sticklebacks. Nature, 484, 55-61.
32. Jones RT, Salazar PA, ffrench-Constant RH, Jiggins CD, Joron M, (2012b) Evolution of a mimicry supergene from a multilocus architecture. Proceedings of the Royal Society of London. Series B, Biological Sciences, 279, 316-325.
33. Joron M, Frezal L, Jones RT, et al,. (2011) Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature, 477, 203-206.
34. Kalinowski ST, (2011) The computer program STRUCTURE does not reliably identify the main genetic clusters within species: simulations and implications for human population structure. Heredity, 106, 625-632.
35. Kelly AJ, Willis JH, (1998) Polymorphic microsatellite loci in Mimulus guttatus and related species. Molecular Ecology, 7, 769-774.
36. Kiang YT, Hamrick JL, (1978) Reproductive isolation in the Mimulus guttatus-M. nasutus complex. American Midland Naturalist, 100, 269-276.
37. King M, (1993) Species Evolution: The Role of Chromosomal Change. Cambridge University Press, Cambridge, UK.
38. Kirkpatrick M, (2010) How and why chromosome inversions evolve. PLoS Biology, 8, e1000501.
39. Kirkpatrick M, Barton N, (2006) Chromosome inversion, local adaptation and speciation. Genetics, 173, 419-434.
40. Kirkpatrick M, Kern A, (2012) Where's the money? Inversions, genes, and the hunt for genomic targets of selection. Genetics, 190, 1153-1155.
41. van Kleunen M, (2007) Adaptive genetic differentiation in life-history traits between populations of Mimulus guttatus with annual and perennial life-cycles. Evolutionary Ecology, 21, 185-199.
42. Kolaczkowski B, Kern AD, Holloway AK, Begun DJ, (2011) Genomic differentiation between temperate and tropical Australian populations of Drosophila melanogaster. Genetics, 187, 245-260.
43. Krimbas CB, Powell JR, (1992) Drosophila Inversion Polymorphism. CRC Press, Boca Raton, Florida.
44. Lasky JR, Des Marais DL, McKay JK, et al,. (2012) Characterizing genomic variation of Arabidopsis thaliana: the roles of geography and climate. Molecular Ecology, 21, 5512-5529.
45. Legendre P, Legendre L, (1998) Numerical Ecology, 2nd edn. Elsevier, New York City, New York.
46. Legendre P, Oksanen J, ter Braak CJF, (2011) Testing the significance of canonical axes in redundancy analysis. Methods in Ecology and Evolution, 2, 269-277.
47. Lewis H, (1953) The mechanism of evolution in the genus Clarkia. Evolution, 7, 1-20.
48. Liu L, Yu L, Kubatko L, Pearl DK, Edwards S, (2009) Coalescent methods for estimating phylogenetic trees. Molecular Phylogenetics and Evolution, 53, 320-328.
49. Lowry DB, Willis JH, (2010) A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. PLoS Biology, 8, e1000500.
50. Lowry DB, Rockwood RC, Willis JH, (2008) Ecological reproductive isolation of coast and inland races of Mimulus guttatus. Evolution, 62, 2196-2214.
51. Macnair M, (1989) A new species of Mimulus endemic to copper mines in California. Botanical Journal of the Linnean Society, 100, 1-14.
52. Martin NH, Willis JH, (2010) Geographical variation in postzygotic isolation and its genetic basis within and between two Mimulus species. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 365, 2469-2478.
53. Meng C, Kubatko LS, (2009) Detecting hybrid speciation in the presence of incomplete lineage sorting using gene tree incongruence: a model. Theoretical Population Biology, 75, 35-45.
54. Modliszewski JL, Willis JH, (2012) Allotetraploid Mimulus sookensis are highly interfertile despite independent origins. Molecular Ecology., 21, 5280-5298.
55. Nesom GL, (2012) Taxonomy of Erythranthe sect. Simiola (Phrymaceae) in the USA and Mexico. Phytoneuron, 40, 1-123.
56. Noor MA, Grams KL, Bertucci LA, Reiland J, (2001) Chromosomal inversions and the reproductive isolation of species. Proceedings of the National Academy of Sciences, 98, 12084-12088.
57. Nordborg M, Hu TT, Ishino Y, et al,. (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS biology, 3, e196.
58. Oksanen J, Blanchet FG, Kindt R, Oksanen MJ, Suggests MASS (2013) Package 'vegan'. Community ecology package Version, 2, 0-0.
59. Peakall R, Smouse PE, (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288-295.
60. Pennell FW, (1951) Mimulus. In: Illustrated Flora of the Pacific States (ed., Abrams L,), vol. 3, pp. 688-731. Stanford University Press, Palo Alto, California.
61. Pickrell JK, Pritchard JK, (2012) Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genetics, 8, e1002967.
62. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
63. Raymond M, Rousset F, (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248-249.
64. Rieseberg LH, (2001) Chromosomal rearrangements and speciation. Trends in Ecology and Evolution, 16, 351-358.
65. Ritland C, Ritland K, (1989) Variation of sex allocation among eight taxa of the Mimulus guttatus species complex (Scrophulariaceae). American Journal of Botany, 76, 1731-1739.
66. Rosenberg NA, (2004) Distruct: a program for the graphical display of population structure. Molecular Ecology Notes, 4, 137-138.
67. Rousset F, (2008) Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources, 8, 103-106.
68. Städler T, Haubold B, Merino C, Stephan W, Pfaffelhuber P, (2009) The impact of sampling schemes on the site frequency spectrum in nonequilibrium subdivided populations. Genetics, 182, 205-216.
69. Stebbins GL, (1958) The inviability, weakness, and sterility of interspecific hybrids. Advances in Genetics, 9, 147-215.
70. Sweigart AL, Willis JH, (2003) Patterns of nucleotide diversity in two species of Mimulus are affected by mating system and asymmetric introgression. Evolution, 57, 2490-2506.
71. Sweigart AL, Fishman L, Willis JH, (2006) A simple genetic incompatibility causes hybrid male sterility in Mimulus. Genetics, 172, 2465-2479.
72. Thompson DM, (1993) Mimulus. In: The Jepson Manual: Higher Plants of California (ed., Hickman JC,), pp. 1037-1046. University of California Press, Berkeley, California.
73. Umina PA, Weeks AR, Kearney MR, McKechnie SW, Hoffmann AA, (2005) A rapid shift in a classic clinal pattern in Drosophila reflecting climate change. Science, 308, 691-693.
74. Vickery RK Jr, (1974) Crossing barriers in the yellow monkey flowers in the genus Mimulus (Scrophulariaceae). Genetics Lectures, 3, 33-82.
75. Vickery RK, (1978) Case studies in the evolution of species complexes in Mimulus. Evolutionary Biology, 11, 405-507.
76. Waples RS, Gaggiotti O, (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Molecular Ecology, 15, 1419-1439.
77. White MJD, (1978) Modes of Speciation. W.H. Freeman, San Francisco, California.
78. Wright KM, Lloyd D, Lowry DB, Macnair MR, Willis JH, (2013) Indirect evolution of hybrid lethality due to linkage with a selected locus in Mimulus guttatus. PLoS Biology, 11, e1001497.
79. Wu CA, Lowry DB, Cooley AM, et al,. (2008) Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity, 100, 220-230.
80. Wu CA, Lowry DB, Nutter LI, Willis JH, (2010) Natural variation for drought response traits in the Mimulus guttatus species complex. Oecologia, 162, 23-33.