Genomic admixture analysis in European populus spp. reveals unexpected patterns of reproductive isolation and mating

Genetics

Volumn 186, Issue 2, 2010, Pages 699-712

  Lexer, Christian ^a,b   Joseph, Jeffrey A ^b   Van Loo, Marcela ^c   Barbará, Thelma ^a,b   Heinze, Berthold ^d   Bartha, Denes ^e   Castiglione, Stefano ^f   Fay, Michael F ^b   Buerkle, C Alex ^g  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

^b JODRELL LABORATORY   (United Kingdom)

^c UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^d FEDERAL RESEARCH AND TRAINING CENTRE FOR FORESTS   (Austria)

^e UNIVERSITY OF WEST HUNGARY   (Hungary)

^f UNIVERSITY OF SALERNO   (Italy)

^g UNIVERSITY OF WYOMING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ARTICLE; ASPEN; ASSORTATIVE MATING; EUROPE; GENE LOCUS; GENE MAPPING; GENETIC LINKAGE; GENETIC MARKER; GENETIC POLYMORPHISM; GENOME ANALYSIS; GENOTYPE; HYBRID; MICROSATELLITE MARKER; NONHUMAN; PLANT REPRODUCTION; POPULUS ALBA; POPULUS TREMULA; PRIORITY JOURNAL; TAXON; WILD SPECIES;

ADAPTATION, BIOLOGICAL; ALLELES; BASE SEQUENCE; BAYES THEOREM; BIOLOGICAL EVOLUTION; CHROMOSOME MAPPING; CROSSES, GENETIC; DATA INTERPRETATION, STATISTICAL; EPISTASIS, GENETIC; GENETIC DRIFT; GENETIC LINKAGE; GENETIC MARKERS; GENETIC SPECIATION; GENETIC VARIATION; GENOTYPE; HYBRIDIZATION, GENETIC; POLYMORPHISM, GENETIC; POPULUS; REPRODUCTION; SEQUENCE ANALYSIS, DNA;

POPULUS; POPULUS ALBA; POPULUS TREMULA;

EID: 78951472622     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.110.118828     Document Type: Article

References (74)

1. ANDERSON, E. C., and E. A. THOMPSON, 2002 A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160: 1217-1229.
2. BARTHA, D., 1991 Hybridization and introgression in Hungarian populations of white poplar (Populus alba L.). Mitt. Dtsch. Dendrol. Ges. 80: 177-180 (in German).
3. BARTON, N. H., 2001 The role of hybridization in evolution. Mol. Ecol. 10: 551-568.
4. BARTON, N. H., and K. S. GALE, 1993 Genetic analysis of hybrid zones, pp. 13-45 in Hybrid Zones and the Evolutionary Process, edited by R. G. Harrison and J. Price. Oxford University Press, Oxford.
5. BARTON, N. H., and G. M. HEWITT, 1985 Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16: 113-148.
6. BEAUMONT, M. A., 2005 Adaptation and speciation: What can FST tell us? Trends Ecol. Evol. 20: 435-440.
7. BEAUMONT, M. A., and D. J. BALDING, 2004 Identifying adaptive genetic divergence among populations from genome scans. Mol. Ecol. 13: 969-980.
8. BEAUMONT, M. A., and R. A. NICHOLS, 1996 Evaluating loci for use in the genetic analysis of population structure. Proc. R. Soc. Lond. Ser. B 263: 1619-1626.
9. BRISCOE, D., J. STEPHENS and S. O'BRIEN, 1994 Linkage disequilibrium in admixed populations: applications in gene mapping. J. Hered. 85: 59-63.
10. BUERKLE, C. A., and C. LEXER, 2008 Admixture as the basis for genetic mapping. Trends Ecol. Evol. 23: 686-694.
11. BUERKLE, C. A., R. J. MORRIS, M. A. ASMUSSEN and L. H. RIESEBERG, 2000 The likelihood of homoploid hybrid speciation. Heredity 84: 441-451.
12. CHAKRABORTY, R., and K. WEISS, 1988 Admixture as a tool for finding linked genes and detecting that difference from allelic association between loci. Proc. Natl. Acad Sci. USA 85: 9119-9123.
13. COYNE, J. A., and H. A. ORR, 2004 Speciation. Sinauer Associates, Sunderland, MA.
14. DE CARVALHO, D., P. K. INGVARSSON, J. JOSEPH, L. SUTER, C. SEDIVY et al., 2010 Admixture facilitates adaptation from standing variation in the European aspen (P. tremula L.), a widespread forest tree. Mol. Ecol. 19: 1638-1650.
15. EXCOFFIER, L., T. HOFER and M. FOLL, 2009a Detecting loci under selection in a hierarchically structured population. Heredity 103: 285-298.
16. EXCOFFIER, L., M. FOLL and R. J. PETIT, 2009b Genetic consequences of range expansions. Annu. Rev. Ecol. Evol. Syst. 40: 481-501.
17. FALUSH, D., M. STEPHENS and J. K. PRITCHARD, 2003 Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567-1587.
18. FALUSH, D., M. STEPHENS and J. K. PRITCHARD, 2007 Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol. Ecol. Notes 7: 574-578.
19. FAURE, M. F., P. DAVID, F. BONHOMME and N. BIERNE, 2008 Genetic hitchhiking in a subdivided population of Mytilus edulis. BMC Evol. Biol. 8: 14.
20. FISCHER, M. A., W. ADLER and K. OSWALD, 2005 Excursion flora for Austria, Liechtenstein and South Tyrol. Land Oberoesterreich, Landesmuseum, Linz, Austria (in German).
21. FOLL, M., and O. GAGGIOTTI, 2008 A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180: 977-993.
22. FOSSATI, T., G. PATRIGNANI, I. ZAPELLI, M. SABATTI, F. SALA et al., 2004 Development of molecular markers to assess the level of introgression of P. tremula into P. alba natural populations. Plant Breeding 123: 382-385.
23. FUSSI, B., C. LEXER and B. HEINZE, 2010 Phylogeography of Populus alba (L.) and Populus tremula (L.) in Central Europe: secondary contact and hybridisation during recolonisation from disconnected refugia. Tree Genet. Genomes 6: 439-450.
24. GAVRILETS, S., 1997 Hybrid zones with Dobzhansky-type epistatic selection. Evolution 51: 1027-1035.
25. GOMPERT, Z., and C. A. BUERKLE, 2009 A powerful regression-based method for admixture mapping of isolation across the genome of hybrids. Mol. Ecol. 18: 1207-1224.
26. GOMPERT, Z., and C. A. BUERKLE, 2010 INTROGRESS: a software package for mapping components of isolation in hybrids. Mol. Ecol. Resources 10: 378-384.
27. GOUDET, J., 1995 Fstat version 1.2: a computer program to calculate F-statistics. J. Hered. 86: 485-486.
28. HALL, D., V. LUQUEZ, V. M. GARCIA, K. R. STONGE, S. JANSSON et al., 2007 Adaptive population differentiation in phenology across a latitudinal gradient in European Aspen (Populus tremula, L.): a comparison of neutral markers, candidate genes and phenotypic traits. Evolution 61: 2849-2860.
29. HAMZEH, M., and S. DAYANANDAN, 2004 Phylogeny of Populus (Salicaceae) based on nucleotide sequences of chloroplast TRNT-TRNF region and nuclear rDNA. Am. J. Bot. 91: 1398-1408.
30. HEDRICK, P. W., 2005 A standardized genetic differentiation measure. Evolution 59: 1633-1638.
31. HOHENLOHE, P. A., S. BASSHAM, P.D. ETTER, N. STIFFLER, E. A. JOHNSON et al., 2010 Population genomics of parallel adaptation in threespine stickleback using sequenced RAD Tags. Plos Genet. 6: e1000862.
32. JIGGINS, C. D., C. SALAZAR, M. LINARES and J. MAVAREZ, 2008 Hybrid trait speciation and Heliconius butterflies. Philos. Trans. R. Soc. Lond. B 363: 3047-3054.
33. JOSEPH, J. A., and C. LEXER, 2008 A set of novel DNA polymorphisms within candidate genes potentially involved in ecological divergence between Populus alba and P. tremula, two hybridizing European forest trees. Mol. Ecol. Resour. 8: 188-192.
34. KIM, S.-C., and L. H. RIESEBERG, 1999 Genetic architecture of species differences in annual sunflowers: implications for adaptive trait introgression. Genetics 153: 965-977.
35. ST and its relatives do not measure differentiation. Mol. Ecol. 17: 4015-4026.
36. LEXER, C., B. HEINZE, R. ALIA and L. H. RIESEBERG, 2004 Hybrid zones as a tool for identifying adaptive genetic variation in out-breeding forest trees: lessons from wild annual sunflowers (Helianthus spp.). Forest Ecol. Manag. 197: 49-64.
37. LEXER, C., M. FAY, J. JOSEPH, M.-S. NICA and B. HEINZE, 2005 Barrier to gene flow between two ecologically divergent Populus species, P. alba (white poplar) and P. tremula (European aspen): the role of ecology and life history in gene introgression. Mol. Ecol. 14: 1045-1057.
38. LEXER, C., C. A. BUERKLE, J. JOSEPH, B. HEINZE and M. FAY, 2007 Admixture in European Populus hybrid zones makes feasible the mapping of loci that contribute to reproductive isolation and trait differences. Heredity 98: 74-84.
39. LEXER, C., J. JOSEPH, M. VAN LOO, G. PRENNER, B. HEINZE et al., 2009 The use of digital image-based morphometrics to study the phenotypic mosaic in taxa with porous genomes. Taxon 58: 349-364.
40. MARTIN, N. H., A. C. BOUCK and M. L. ARNOLD, 2006 Detecting adaptive trait introgression between Iris fulva and I. brevicaulis in highly selective field conditions. Genetics 172: 2481-2489.
41. Martinsen, G. D., T. G. Whitham, R. J. Turek and P. KEIM, 2001 Hybrid populations selectively filter gene introgression between species. Evolution 55: 1325-1335.
42. MILNE, R. I., S. TERZIOGLU and R. J. ABBOTT, 2003 A hybrid zone dominated by fertile F(1)s: maintenance of species barriers in Rhododendron. Mol. Ecol. 12: 2719-2729.
43. MINDER, A. M., C. ROTHENBUEHLER and A. WIDMER, 2007 Genetic structure of hybrid zones between Silene latifolia and Silene dioica (Caryophyllaceae): evidence for introgressive hybridization. Mol. Ecol. 16: 2504-2516.
44. NIELSEN, R., 2005 Molecular signatures of natural selection. Annu. Rev. Genet. 39: 197-218.
45. NOLTE, A. W., and D. TAUTZ, 2010 The onset of hybrid speciation. Trends Genet. 26: 54-58.
46. NOLTE, A. W., Z. GOMPERT and C. A. BUERKLE, 2009 Variable patterns of introgression in two sculpin hybrid zones suggest that genomic isolation differs among populations. Mol. Ecol. 18: 2615-2627.
47. PAYSEUR, B. A., J. G. KRENZ and M. W. NACHMAN, 2004 Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mice. Evolution 58: 2064-2078.
48. PIALEK, J., and N. H. BARTON, 1997 The spread of an advantageous allele across a barrier: the effects of random drift and selection against heterozygotes. Genetics 145: 493-504.
49. RAJORA, O. P., and B. P. DANCIK, 1992 Genetic characterization and relationships of Populus alba, P. tremula, and P. x canescens, and their clones. Theor. Appl. Genet. 84: 291-298.
50. REICH, D., N. PATTERSON, P. DE JAGER, G. MCDONALD, A. WALISZEWSKA et al., 2005 A whole-genome admixture scan finds a candidate locus for multiple sclerosis susceptibility. Nat. Genet. 37: 1113-1118.
51. RIESEBERG, L. H., and C. A. BUERKLE, 2002 Genetic mapping in hybrid zones. Am. Nat. 159: S36-S50.
52. RIESEBERG, L. H., J. WHITTON and K. GARDNER, 1999 Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152: 713-727.
53. RIESEBERG, L. H., O. RAYMOND, D. M. ROSENTHAL, Z. LAI, K. LIVINGSTONE et al., 2003 Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301: 1211-1216.
54. ROGERS, S., D. CAMPBELL, S. BAIRD, R. DANZMANN and L. BERNATCHEZ, 2001 Combining the analyses of introgressive hybridisation and linkage mapping to investigate the genetic architecture of population divergence in the lake whitefish (Coregonus clupaeformis,Mitchell). Genetica 111: 25-41.
55. SCOTTI-SAINTAGNE, C., S. MARIETTE, I. PORTH, P. G. GOICOECHEA, T. Barreneche et al., 2004 Genome scanning for interspecific differentiation between two closely related oak species. [Quercus robur L. and Q. petraea (Matt.) Liebl.] Genetics 168: 1615-1626.
56. SLATE, J., 2005 Quantitative trait locus mapping in natural populations: progress, caveats and future directions. Mol. Ecol. 14: 363-379.
57. SMULDERS, M. J. M., J. VAN DER SCHOOT, P. ARENS and B. VOSMAN, 2001 Trinucleotide repeat microsatellite markers for black poplar (Populus nigra L.). Mol. Ecol. Notes 1: 188-190.
58. STETTLER, R. F., H. D. BRADSHAW, P.E. HEILMAN and T. M. HINCKLEY, 1996 Biology of Populus and Its Implications for Management and Conservation. NRC Research Press, Ottawa.
59. TEETER, K. C., L. M. THIBODEAU, Z. GOMPERT, C. A. BUERKLE, M. W. NACHMAN et al., 2010 The variable genomic architecture of isolation between hybridizing species of house mice. Evolution 64: 472-485.
60. TURELLI, M., and L. C. MOYLE, 2007 Asymmetric postmating isolation: Darwin's corollary to Haldane's rule. Genetics 176: 1059-1088.
61. TURNER, T. L., E. C. BOURNE, E. J. VON WETTBERG, T. T. HU and S. V. NUZHDIN, 2010 Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nat. Genet. 42: 260-263.
62. TUSKAN, G. A., L. E. GUNTER, Z.K. YANG, T. M. YIN, M. M. SEWELL et al., 2004 Characterization of microsatellites revealed by genomic sequencing of Populus trichocarpa. Can. J. Forest Res. 34: 85-93.
63. TUSKAN, G. A., S. DIFAZIO, S. JANSSON, J. BOHLMANN, I. GRIGORIEV et al., 2006 The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596-1604.
64. VAN DER SCHOOT, J., M. POSPISKOVA, B. VOSMAN and M. J. M. SMULDERS, 2000 Development and characterization of microsatellite markers in black poplar (Populus nigra L.). Thoer. Appl. Genet. 101: 317-322.
65. VAN LOO, M., J. A. JOSEPH, B. HEINZE, M. F. FAY and C. LEXER, 2008 Clonality and spatial genetic structure in Populus 3 canescens and its sympatric backcross parent P. alba in a Central European hybrid zone. New Phytol. 177: 506-516.
66. VIA, S., and J.WEST, 2008 The genetic mosaic suggests a new role for hitchhiking in ecological speciation. Mol. Ecol. 17: 4334-4345.
67. VINES, T. H., S. C. KOHLER, A. THIEL, I. GHIRA, T. R. SANDS et al., 2003 The maintenance of reproductive isolation in a mosaic hybrid zone between the fire-bellied toads Bombina bombina and B. variegata. Evolution 57: 1876-1888.
68. WEIR, B. S., and C. C. COCKERHAM, 1984 Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
69. WHITLOCK, M. C., 1992 Temporal fluctuations in demographic parameters and the genetic variance among populations. Evolution 46: 608-615.
70. WHITNEY, K. D., R. A. RANDELL and L. H. RIESEBERG, 2006 Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus. Am. Nat. 167: 794-807.
71. WOLF, D. E., N. TAKEBAYASHI and L. H. RIESEBERG, 2001 Predicting the risk of extinction through hybridization. Conserv. Biol. 15: 1039-1053.
72. WU, C. I., 2001 The genic view of the process of speciation. J. Evol. Biol. 14: 851-865.
73. YATABE, Y., N. C. KANE, C. SCOTTI-SAINTAGNE and L. H. RIESEBERG, 2007 Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 175: 1883-1893.
74. ZHU, X., A. LUKE, R. COOPER, T. QUERTERMOUS, C. HANIS et al., 2005 Admixture mapping for hypertension loci with genomescan markers. Nat. Genet. 37: 177-181.