Divergence hitchhiking and the spread of genomic isolation during ecological speciation-with-gene-flow

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 367, Issue 1587, 2012, Pages 451-460

  Via, Sara ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

Adaptation; Genome scan; Genomic divergence; Insects; Speciation genetics; Sympatric speciation

Indexed keywords

ALLOPATRY; DIVERGENCE; EVOLUTIONARY BIOLOGY; GENE FLOW; GENOME; GENOMICS; INSECT; SPECIATION (BIOLOGY); SYMPATRY;

EID: 84255187761     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0260     Document Type: Review

References (67)

1. Rice, W. R. & Hostert, E. E. 1993 Laboratory experiments on speciation: what have we learned in 40 years? Evolution 47, 1637-1653. (doi:10.2307/2410209)
2. Via, S. 2001 Sympatric speciation in animals: the ugly duckling grows up. Trends Ecol. Evol. 16, 381-390. (doi:10.1016/S0169-5347(01)02188-7)
3. Coyne, J. A. & Orr, H. A. 2004 Speciation. Sunderland, MA: Sinauer Associates.
4. Felsenstein, J. 1981 Skepticism toward Santa Rosalia, or why are there so few kinds of animals? Evolution 35, 124-138. (doi:10.2307/2407946)
5. Schluter, D. 2001 Ecology and the origin of species. Trends Ecol. Evol. 16, 372-380. (doi:10.1016/S0169- 5347(01)02198-X)
6. Gavrilets, S. 2004 Fitness landscapes and the origin of species. Princeton, NJ: Princeton University Press.
7. Gavrilets, S. & Vose, A. 2007 Case studies and mathematical models of ecological speciation. II. Palms on an oceanic island. Mol. Ecol. 16, 2910-2921. (doi:10.1111/j.1365-294X.2007.03304.x)
8. Noor, M. A. F. & Bennett, S. M. 2009 Islands of speciation or mirages in the desert? Examining the role of restricted recombination in maintaining species. Heredity 103, 439-444. (doi:10.1038/hdy.2009.151)
9. Pinho, C. & Hey, J. 2010 Divergence with gene flow: models and data. Annu. Rev. Ecol. Evol. Syst. 41, 215-230. (doi:10.1146/annurev-ecolsys-102209-144644)
10. Hoffman, A. A. & Rieseberg, L. H. 2008 Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation? Annu. Rev. Ecol. Evol. Syst. 39, 21-42. (doi:10.1146/annurev.ecolsys.39.110707.173532)
11. Feder, J. L., Roethele, J. B. & Filchak, K. 2003 Evidence for inversion polymorphism related to sympatric host race formation in the apple maggot fly, Rhagoletis pomonella. Genetics 163, 939-953.
12. Via, S. & West, J. 2008 The genetic mosaic suggests a new role for hitchhiking in ecological speciation. Mol. Ecol. 17, 4334-4345. (doi:10.1111/j.1365-294X.2008.03921.x)
13. Charlesworth, B. 2009 Effective population size and patterns of molecular evolution and variation. Nat. Rev. Genet. 10, 195-205. (doi:10.1038/nrg2526)
14. Stinchcombe, J. R. & Hoekstra, H. E. 2008 Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100, 158-170. (doi:10.1038/sj.hdy.6800937)
15. Feder, J. L. & Nosil, P. 2010 The efficacy of divergence hitchhiking in generating genomic islands during ecological speciation. Evolution 64, 1729-1747. (doi:10.1111/j.1558-5646.2009.00943.x)
16. Storz, J. 2005 Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol. Ecol. 14, 671-688. (doi:10.1111/j.1365-294X.2005.02437.x)
17. Lewontin, R. C. & Krakauer, J. 1973 Distribution of gene frequency as a test of the theory of selective neutrality of polymorphisms. Genetics 74, 175-195.
18. Wilding, C. S., Butlin, R. K. & Grahame, J. 2001 Differential gene exchange between parapatric morphs of Littorina saxatillis detected using AFLP markers. J. Evol. Biol. 14, 611-619. (doi:10.1046/j.1420-9101. 2001.00304.x)
19. Galindo, J., Grahame, J. W. & Butlin, R. K. 2010 An EST-based genome scan using 454 sequencing in the marine snail Littorina saxatilis. J. Evol. Biol. 23, 2004-2016. (doi:10.1111/j.1420-9101.2010.02071.x)
20. Stapley, J. A. et al. 2010 Adaptation genomics: the next generation. Trends Ecol. Evol. 25, 705-772. (doi:10. 1016/j.tree.2010.09.002)
21. Wood, H. M., Grahame, J. W., Humphray, S., Rogers, J. & Butlin, R. K. 2008 Sequence differentiation in regions identified by a genome scan for local adaptation. Mol. Ecol. 17, 3123-3135. (doi:10.1111/j.1365-294X.2008. 03755.x)
22. Beaumont, M. A. & Balding, D. J. 2004 Identifying adaptive genetic divergence among populations from genome scans. Mol. Ecol. 13, 969-980. (doi:10.1111/j. 1365-294X.2004.02125.x)
23. Vitalis, R., Dawson, K., Boursot, P. & Belkhir, K. 2003 DetSel 1.0: a computer program to detect markers responding to selection. J. Hered. 94, 429-431.(doi:10.1093/jhered/esg083)
24. Vasemagi, A. & Primmer, C. R. 2005 Challenges for indentifying functionally important genetic variation: the promise of combining complementary research strategies. Mol. Ecol. 14, 3623-3642. (doi:10.1111/j. 1365-294X.2005.02690.x)
25. Excoffier, L., Hofer, T. & Foll, M. 2009 Detecting loci under selection in a hierarchically structured population. Heredity 103, 285-298. (doi:10.1038/hdy.2009.74)
26. Strasburg, J. L., Sherman, N. A., Wright, K. M., Moyle, L. C., Willis, J. H. & Rieseberg, L. H. 2012 What can patterns of differentiation across plant genomes tell us about adaptation and speciation? Phil. Trans. R. Soc. B 367, 364-373. (doi:10.1098/rstb.2011.0199)
27. Charlesworth, B., Nordborg, M. & Charlesworth, D. 1997 The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genet. Res. 70, 155-174. (doi:10.1017/S0016672397002954)
28. Bierne, N., Welch, J., Loire, E., Bonhomme, F. & David, P. 2011 The coupling hypothesis: why genome scans may fail to map local adaptation genes. Mol. Ecol. 20, 2044-2072. (doi:10.1111/j.1365-294X.2011.05080.x)
29. Manel, S., Conord, C. & Despres, L. 2009 Genome scan to assess the respective role of host-plant and environmental constraints on the adaptation of a widespread insect. BMC Evol. Biol. 9, 288. (doi:10.1186/1471- 2148-9-288)
30. Mariac, C. et al. 2011 Genetic basis of pearl millet adaptation along an environmental gradient investigated by a combination of genome scan and association mapping. Mol. Ecol. 20, 80-91. (doi:10.1111/j.1365-294X.2010.04893.x)
31. Turner, T. L., von Wettberg, E. J. & Nuzhdin, S. V. 2008 Genomic analysis of differentiation between soil types reveals candidate genes for local adaptation in Arabidopsis lyrata. PLoS ONE 3, e3183. (doi:10.1371/journal.pone. 0003183)
32. DeFaveri, J., Shikano, T., Shimada, Y., Goto, A. & Merila, J. 2011 Global analysis of genes involved in freshwater adaptation in threespine sticklebacks (Gasterosteus aculeatus). Evolution 65, 1800-1807. (doi:10.1111/j. 1558-5646.2011.01247.x)
33. Rogers, S. M. & Bernatchez, L. 2007 The genetic architecture of ecological speciation and the association with signatures of selection in natural lake whitefish (Coregonus sp. Salmonidae) species pairs. Mol. Biol. Evol. 24, 1423-1438. (doi:10.1093/molbev/msm066)
34. Via, S. 2009 Natural selection in action during speciation. Proc. Natl Acad. Sci. USA 106, 9339-9946. (doi:10.1073/pnas.0901397106)
35. Renaut, S., Maillet, N., Normandeau, E., Sauvage, C., Derome, N., Rogers, S. M. & Bernatchez, L. 2012 Genome-wide patterns of divergence during speciation: the lake whitefish case study. Phil. Trans. R. Soc. B 367, 354-363. (doi:10.1098/rstb.2011.0197)
36. Mather, K. 1983 Response to selection. In The genetics and biology of Drosophila, vol. 3c (eds M. Ashburner, H. L. Carson & J. N Thompson), pp. 155-221. London, UK: Academic Press.
37. Burke, J. M., Tang, S., Knapp, S. J. & Rieseberg, L. H. 2002 Genetic analysis of sunflower domestication. Genetics 161, 1257-1267.
38. Wright, D., Rubin, C.-J., Martinez Barrio, A., Schütz, K., Kerje, S., Brändström, H., Kindmark, A., Jensen, P. & Andersson, L. 2010 The genetic architecture of domestication in the chicken: effects of pleiotropy and linkage. Mol. Ecol. 19, 5140-5156. (doi:10.1111/j.1365-294X.2010.04882.x)
39. Albert, F. W. et al. 2009 Genetic architecture of tameness in a rat model of animal domestication. Genetics 182, 541-554. (doi:10.1534/genetics.109.102186)
40. Baack, E. J., Sapir, Y., Chapman, M. A., Burke, J. H. & Rieseberg, L. H. 2007 Selection on domestication traits and quantitative trait loci in crop-wild sunflower hybrids. Mol. Ecol. 17, 666-677. (doi:10.1111/j.1365-294X. 2007.03596.x)
41. Hawthorne, D. J. & Via, S. 2001 Genetic linkage facilitates ecological specialization and reproductive isolation in pea aphids. Nature 412, 904-907. (doi:10.1038/35091062)
42. Turner, T. L., Levine, M. I., Eckert, M. L. & Begun, D. 2008 Genomic analysis of adaptive differentiation in Drosophila melanogaster. Genetics 179, 455-473. (doi:10.1534/genetics.107.083659)
43. Merrill, R.M., VanSchooten, B., Scott, J.A. & Jiggins, C.D. 2011 Pervasive genetic associations between traits causing reproductive isolation in Heliconius butterflies. Proc. R. Soc. B. 278, 511-518. (doi:10.1098/rspb.2010.1493)
44. Kim, S. C. & Rieseberg, L. H. 1999 Genetic architecture of species differences in annual sunflowers: implications for adaptive trait introgression. Genetics 153, 965-977.
45. Begun, D. J. & Aquadro, C. F. 1992 Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356, 519-520.(doi:10.1038/356519a0)
46. Via, S., Bouck, A. C. & Skillman, S. 2000 Reproductive isolation between sympatric races of pea aphids. II. Selection against migrants and hybrids in the parental environment. Evolution 54, 1626-1637.
47. Via, S., Conte, G. L., Mason-Foley, C., Mills, K. & Lew, J. Submitted. Coupling a QTL map with a genome scan reveals evidence for divergence hitchhiking during incipient speciation.
48. Feder, J. L., Gejji, R., Yeaman, S. & Nosil, P. 2012 Establishment of new mutations under divergence and genomic hitchhiking. Phil. Trans. R. Soc. B 367, 461-474. (doi:10.1098/rstb.2011.0256)
49. Kobayashi, Y. & Telschow, A. 2010 The concept of effective recombination rate and its application in speciation theory. Evolution 65, 617-628. (doi:10.1111/j.1558-5646.2010.01156.x)
50. Ting, C.-T., Tsaur, S.-C. & Wu, C.-I. 2000 The phylogeny of closely related species as revealed by the genealogy of a speciation gene, Odysseus. Proc. Natl Acad. Sci. USA 97, 5313-5316. (doi:10.1073/pnas.090541597)
51. Michel, A. P., Sim, S., Powell, T. H. Q., Taylor, M. S., Nosil, P. & Feder, J. L. 2010 Widespread genomic divergence during sympatric speciation. Proc. Natl Acad. Sci. USA 107, 9724-9729. (doi:10.1073/pnas. 1000939107)
52. Turner, T. L., Hahn, M. W. & Nuzhdin, S. V. 2005 Genomic islands of speciation in Anopheles gambiae. PLoS Biol. 3, e285. (doi:10.1371/journal.pbio.0030285)
53. Hohenlohe, P. A., Bassham, S., Etter, P. D., Stiffler, N., Johnson, E. A. & Cresko, W. A. 2010 Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 6, e1000862. (doi:10.1371/journal.pgen.1000862)
54. Albert, S. Y. K., Sawaya, S., Vines, T. H. et al. 2007 The genetics of adaptive shape shift in stickleback: pleiotropy and effect size. Evolution 62, 76-85.
55. Makinen, H. S., Shikano, T., Manuel Cano, J. & Merila, J. 2008 Hitchhiking mapping reveals a candidate genomic region for natural selection in three-spined stickleback chromosome VIII. Genetics 178, 453-465. (doi:10.1534/genetics.107.078782)
56. Lawniczak, M. K. N. et al. 2010 Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science 330, 512-514. (doi:10.1126/science.1195755)
57. Egan, S. P., Nosil, P. & Funk, D. J. 2008 Selection and genomic differentiation during ecological speciation: isolating the contributions of host association via a comparative genome scan of Neochlamisus bebbianae leaf beetles. Evolution 62, 1162-1181. (doi:10.1111/j.1558-5646.2008.00352.x)
58. Willig, E.-M., Bentzen, P., van Oosterhout, C., Hoffmann, M., Cable, C., Breden, F., Weigel, D. & Dreyer, C. 2010 Genome-wide single nucleotide polymorphism reveals population history and adaptive divergence in wild guppies. Mol. Ecol. 19, 968-984.(doi:10.1111/j.1365-294X.2010.04528.x)
59. MacKay, T. F. C., Stone, E. A. & Ayroles, J. 2009 The genetics of quantitative traits: challenges and prospects. Nat. Rev. Genet. 10, 565-577. (doi:10.1038/nrg2612)
60. Butlin, R. 2008 Population genomics and speciation. Genetica 138, 409-418. (doi:10.1007/s10709-008-9321-3)
61. Strasburg, J. L., Scotti-Saintagne, C., Scotti, I., Lai, Z. & Rieseberg, L. H. 2009 Genomic patterns of adaptive divergence between chromosomally differentiated sunflower species. Mol. Biol. Evol. 26, 1341-1355. (doi:10. 1093/molbev/msp043)
62. Scascitelli, M., Whitney, K. D., Randell, R. A., King, M., Buerkle, C. A. & Rieseberg, L. H. 2010 Genome scan of hybridizing sunflowers from Texas (Helianthus annuus and H. debilis) reveals asymmetric patterns of introgression and small islands of genomic differentiation. Mol. Ecol. 19, 521-541. (doi:10.1111/j.1365-294X.2009.04504.x)
63. Carneiro, M., Blanco-Aguiar, J. A., Villafuerte, R., Ferrand, N. & Nachman, M. W. 2010 Speciation in the european rabbit (Oryctolagus cuniculus): islands of differentiation on the X chromosome and autosomes. Evolution 64, 3443-3460. (doi:10.1111/j.1558-5646.2010.01092.x)
64. Hohenlohe, P. A., Bassham, S., Currey, M. & Cresko, W. A. 2012 Extensive linkage disequilibrium and parallel adaptive divergence across threespine stickleback genomes. Phil. Trans. R. Soc. B 367, 395-408. (doi:10. 1098/rstb.2011.0245)
65. Le Rouzic, A., Østbye, K., Klepaker, T. O., Hansen, T. M., Bernatchez, L., Schluter, D. & Vollestad, A. 2011 Strong and consistent natural selection associated with armour reduction in sticklebacks. Mol. Ecol. 20, 2483-2493. (doi:10.1111/j.1365-294X.2011.05071.x)
66. Avise, J. C. 2000 Phylogeography: the history and formation of species. Cambridge, MA: Harvard University Press.
67. Pritchard, J. K., Stephens, M. & Donnelly, P. 2000 Inference of population structure using multilocus genotype data. Genetics 155, 945-949.