On the origin of species: Insights from the ecological genomics of lake whitefish

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 365, Issue 1547, 2010, Pages 1783-1800

  Bernatchez, Louis ^a   Renaut, Sébastien ^a   Whiteley, Andrew R ^a,b   Derome, Nicolas ^a   Jeukens, Julie ^a   Landry, Lysandre ^a,c   Lu, Guoqing ^a,d   Nolte, Arne W ^a,e   Østbye, Kjartan ^a,f   Rogers, Sean M ^a,g   St Cyr, Jérôme ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c INSTITUT DES SCIENCES DE LA MER DE RIMOUSKI   (Canada)

^d UNIVERSITY OF NEBRASKA AT OMAHA   (United States)

^e MAX PLANCK INSTITUTE FOR EVOLUTIONARY BIOLOGY   (Germany)

^f UNIVERSITY OF OSLO   (Norway)

^g UNIVERSITY OF CALGARY   (Canada)

Author keywords

454 sequencing; Ecological genomics; Microarrays; Selection; Speciation; Stickleback

Indexed keywords

ADAPTIVE RADIATION; BIOTECHNOLOGY; DIVERGENCE; FISHERY MODELING; GENETIC ANALYSIS; GENOMICS; LAKE ECOSYSTEM; NATURAL SELECTION; REPRODUCTIVE ISOLATION; SALMONID; SYMPATRY;

COREGONUS; COREGONUS CLUPEAFORMIS;

EID: 77953575528     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2009.0274     Document Type: Conference Paper

References (111)

1. Amsterdam, A., Nissen, R. M., Sun, Z., Swindell, E. C., Farrington, S. & Hopkins, N. 2004 Identification of 315 genes essential for early zebrafish development. Proc. Natl Acad. Sci. USA 101, 12 792-12 797. (doi:10. 1073/pnas.0403929101)
2. Amundsen, P.-A., Bøhn, T. & Vågå, G. H. 2004 Gill raker morphology and feeding ecology of two sympatric morphs of European whitefish (Coregonus lavaretus). Ann. Zool. Fenn. 41, 291-300.
3. Barbazuk, W. D., Emrich, S. J., Chen, H. D., Li, L. & Schanble, P. S. 2007 SNP discovery via 454 transcriptome sequencing. Plant J. 51, 910-918. (doi:10.1111/j. 1365-313X.2007.03193.x)
4. Barrett, R. D. H., Rogers, S. M. & Schluter, D. 2008 Threespine stickleback natural selection on a major armor gene in threespine stickleback. Science 322, 255-257. (doi: 10. 1126/science.1159978)
5. Barton, N. H. 2001 The role of hybridization in evolution. Mol. Ecol. 10, 551-568. (doi:10.1046/j.1365-294x. 2001.01216.x)
6. 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.1365294X.2004.02125.x)
7. Beaumont, M. A. & Nichols, R. A. 1996 Evaluating loci for use in the genetic analysis of population structure. Proc. R. Soc. Lond. B 263, 1619-1626. (doi:10.1098/ rspb. 1996.0237)
8. Bernatchez, L. 2004 Ecological theory of adaptive radiation: an empirical assessment from coregonine fishes (Salmoniformes). In Evolution illuminated: salmon and their relatives (eds A. P. Hendry & S. C. Stearns), pp. 175-207. Oxford, UK: Oxford University Press.
9. Bernatchez, L. & Dodson, J. J. 1990 Allopatric origin of sympatric populations of lake whitefish (Coregonus clupeaformis) as revealed by mitochondrial DNA restriction analysis. Evolution 44, 1263-1271. (doi:10.2307/ 2409287)
10. Bernatchez, L. & Dodson, J. J. 1991 Phylogeographic structure in mitochondrial DNA of the Lake Whitefish (Coregonus clupeaformis) in North America and its relationships to Pleistocene glaciations. Evolution 45, 1016-1035. (doi: 10.2307/2409706)
11. Bernatchez, L. & Tseng, M. 2008 Editorial. Evol. Appl. 1, 1-2. (doi:10.1111/j.1752-4571.2008.00016.x)
12. Bernatchez, L., Chouinard, A. & Lu, G. 1999 Integrating molecular genetics and ecology in studies of adaptive radiation: whitefish, Coregonus, as a case study. Biol. J. Linn. Soc. 68, 173-194. (doi:10.1111/j.10958312.1999. tb01165.x)
13. Bochdanovits, Z., van der Klis, H. & de Jong, G. 2003 Covariation of larval gene expression and adult body size in natural populations of Drosophila melanogaster. Mol. Biol. Evol. 20, 1760-1766. (doi:10.1093/molbev/ msg179)
14. Britten, R. J. & Davidson, E. H. 1971 Repetitive and nonrepetitive DNA sequences and a speculation on origins of evolutionary novelty. Q. Rev. Biol. 46, 111-138. (doi: 10.1086/406830)
15. Campbell, D. & Bernatchez, L. 2004 Genomic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Mol. Biol. Evol. 21, 945-956. (doi:10.1093/ molbev/msh101)
16. Chouinard, A. & Bernatchez, L. 1998 A study of trophic niche partitioning between larval populations of reproductively isolated whitefish (Coregonus sp.) ecotypes. J. Fish Biol. 53, 1231-1242.
17. Coyne, J. A. & Orr, H. A. 2004 Speciation. Sunderland, MA: Sinauer Associates.
18. Cushing, D. H. 1990 Plankton production and year class strength in fish populations-an update of the match mismatch hypothesis. Adv. Mar. Biol. 26, 249-293. (doi: 10. 1016/S0065-2881 (08)60202-3)
19. Darwin, C. 1859 On the origin of species by means of natural selection. London, UK: John Murray.
20. Derome, N. & Bernatchez, L. 2006 The transcriptomics of ecological convergence between two limnetic coregonine fishes (Salmonidae). Mol. Biol. Evol. 23, 2370-2378. (doi:10.1093/molbev/msl110)
21. Derome, N., Duchesne, P. & Bernatchez, L. 2006 Parallelism in gene transcription among sympatric lake whitefish ecotypes (Coregonus clupeaformis Mitchill). Mol. Ecol. 15, 1239-1250. (doi:10.1111/j.1365-294X. 2005.02968.x)
22. Derome, N., Bougas, B., Rogers, S. M., Whiteley, A. & Bernatchez, L. 2008 Pervasive sex-linked effects on transcription regulation as revealed by eQTLmapping in lake whitefish species pairs (Coregonus sp, Salmonidae). Genetics 179, 1903-1917. (doi: 10.1534/genetics. 107.086306)
23. Douglas, M. R., Brunner, P. C. & Bernatchez, L. 1999 Do assemblages of Coregonus (Teleostei: Salmoniformes) in the Central Alpine region of Europe represent species flocks? Mol. Ecol. 8, 589-603. (doi: 10.1046/j.1365294x.1999. 00581.x)
24. Ehrich, M., Bocker, S. & van den Boom, D. 2005 Multiplexed discovery of sequence polymorphisms using base-specific cleavage and MALDI-TOF MS. Nucleic Acids Res. 33, e38. (doi:10.1093/nar/gni038)
25. Ellison, C. K. & Burton, R. S. 2008 Genotype-dependent variation of mitochondrial transcriptional profiles in interpopulation hybrids. Proc. Natl Acad. Sci. USA 105, 15 831-15 836. (doi:10.1073/pnas.0804253105)
26. Fay, J. C. & Wittkopp, P. J. 2008 Evaluating the role of natural selection in the evolution of gene regulation. Heredity 100, 191-199. (doi:10.1038/sj.hdy.6801000)
27. Fenderson, O. C. 1964 Evidence of subpopulations of lake whitefish, Coregonus clupeaformis, involving a dwarfed form. Trans. Am. Fish. Soc. 93, 77-94. (doi:10.1577/ 1548-8659(1964)93[77:EOSOLW]2.0.CO;2)
28. 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. (doi:10.1534/genetics.108.092221)
29. Gershoni, M., Templeton, A. R. & Mishmar, D. 2009 Mitochondrial bioenergetics as a major motive force of speciation. Bioessays 31, 642-650. (doi:10.1002/bies. 200800139)
30. Gibson, G. & Weir, B. 2005 The quantitative genetics of transcription. Trends Genet. 21, 616-623. (doi:10.1016/ j.tig.2005.08.010)
31. Gilad, Y., Rifkin, S. A. & Pritchard, J. K. 2008 Revealing the architecture of gene regulation: the promise of eQTL studies. Trends Genet. 24, 408-415. (doi:10.1016/j.tig. 2008.06.001)
32. Gow, J. L., Peichel, C. L. & Taylor, E. B. 2007 Ecological selection against hybrids in natural populations of sympatric threespine sticklebacks. J. Evol. Biol. 20, 2173-2180. (doi:10.1111/j.1420-9101.2007.01427.x)
33. Harrod, C. & Kahilainen, K. 2006 Multiple tissue stable isotope analysis show resource segregation between whitefish morphs is maintained across different temporal scales. J. Fish Biol. Suppl. C 69, 249-250.
34. Harvey, P. H. & Pagel, M. D. 1991 The comparative method in evolutionary biology. Oxford, UK: Oxford University Press.
35. Hoekstra, H. E., Hirschmann, R. J., Bundey, R. A., Insel, P. A. & Crossland, J. P. 2006 A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313, 101-104. (doi:10.1126/science. 1126121)
36. Hudson, A. G., Vonlanthen, P., Mueller, R. & Seehausen, O. 2007 Review: the geography of speciation and adaptive radiation in coregonines. Biology and management of coregonid fishes. Adv. Limnol. 60, 111-146.
37. Jeukens, J., Bittner, D., Knudsen, R. & Bernatchez, L. 2009 Candidate genes and adaptive radiation: insights from transcriptional adaptation to the limnetic niche among coregonine fishes (Coregonus sp., Salmonidae). Mol. Biol. Evol. 26, 155-166. (doi:10.1093/molbev/msn235)
38. Joron, M. et al. 2006 A conserved supergene locus controls colour pattern diversity in Heliconius butterflies. PLoS Biol. 4, e303. (doi:10.1371/journal. pbio.0040303)
39. Kahilainen, K. & Lehtonen, H. 2002 Brown trout Salmo trutta, L. and Artie charr Salvelinus alpinus, L. as predators on three sympatric whitefish Coregonus lavaretus, L. forms in a subartic Lake Muddusjarvi. Ecol. Freshw. Fish 11, 158-167. (doi:10.1034/j.1600-0633.2002.t012-00001.x)
40. Kahilainen, K. K., Mahnen, T., Tuomaala, A., Alajaervi, E., Tolonen, A. & Lehtonen, H. 2007 Empirical evaluation of phenotype-environment correlation and trait utility with allopatric and sympatric whitefish, Coregonus lavaretus (L.), populations in subarctic lakes. Biol. J. Linn. Soc. 92, 561-572. (doi:10.1111/j.10958312.2007.00856.x)
41. Kane, N. C., King, M. G., Barker, M. S., Raduski, A., Karrenberg, S., Yatabe, Y., Knapp, S. J. & Rieseberg, L. H. 2009 Compartive genomic and population genetic analyses indicate highly porous genomes and high levels of gene flow between divergent Helianthus species. Evolution 63, 2061-2075. (doi: 10.1111/j.1558-5646. 2009.00703.x)
42. King, M. C. & Wilson, A. C. 1975 Evolution at two levels in humans and chimpanzees. Science 188,107-116. (doi:10. 1126/science.1090005)
43. Kottelat, M. & Freyhof, J. 2007 Handbook of European freshwater fishes. Cornol, Switzerland: Publications Kottelat.
44. Landry, C. R. 2009 Systems biology spins off a new model for the study of canalization. Trends Ecol. Evol. 24, 64-66.
45. Landry, L., Vincent, W. F. & Bernatchez, L. 2007a Parallel evolution of lake white fish dwarf ecotypes in association with limnological features of their adaptive lanscape. J. Evol. Biol. 20, 971-984. (doi: 10.1111/j. 1420-9101. 2007.01304.x)
46. Landry, C. R., Hard, D. L. & Ranz, J. 2007& Genome clashes in hybrids: insights from gene expression. Heredity 99, 483-493. (doi:10.1038/sj.hdy.6801045)
47. Linnen, C. R., Kingsley, E. P., Jensen, J. D. & Hoekstra, H. E. 2009 On the origin and spread of an adaptive allele in deer mice. Science 325, 1095-1098. (doi:10. 1126/science.1175826)
48. Lipson, D. et al. 2009 Quantification of the yeast transcriptome by single-molecule sequencing. Nat. Biotechnol. 27, 652-659. (doi:10.1038/nbt.1551)
49. Lu, G. & Bernatchez, L. 1998 Experimental evidence for reduced hybrid viability between dwarf and normal ecotypes of lake whitefish (Coregonus clupeaformis Mitchill). Proc. R. Soc. Lond. B 265, 1025-1030. (doi:10.1098/ rspb.1998.0394)
50. Lu, G. & Bernatchez, L. 1999 Correlated trophic specialization and genetic divergence in sympatric lake whitefish ecotypes (Coregonus clupeaformis): support for the ecological speciation hypothesis. Evolution 53, 1491-1505. (doi: 10.2307/2640895)
51. Lu, G., Basley, D. J. & Bernatchez, L. 2001 Contrasting patterns of mitochondrial DNA and microsatellite introgressive hybridization between lineages of lake whitefish (Coregonus clupeaformis): relevance for speciation. Mol. Ecol. 10, 965-985. (doi:10.1046/j.1365-294X.2001. 01252.x)
52. Mackay, T. F. C., Stone, E. A. & Ayroles, J. F. 2009 The genetics of quantitative traits: challenges and prospects. Nat. Rev. Genet. 10, 565-577. (doi:10.1038/nrg2612)
53. Margulies, M. et al. 2005 Genome sequencing in microfabricated high-density picoliter reactors. Nature 437, 376-380. (doi:10.1038/nature03959)
54. Matzkin, L. M., Watts, T D., Bitler, B. G., Machado, C. A. & Markow, T. A. 2006 Functional genomics of cactus host shifts in Drosophila mojavensis. Mol. Ecol. 15, 4635-4643.
55. Mitchell-Olds, T., Willis, J. H. & Goldstein, D. B. 2007 Which evolutionary processes influence natural genetic variation for phenotypic traits? Nat. Rev. Genet. 8, 845-856. (doi:10.1038/nrg2207)
56. Morjan, C. L. & Rieseberg, L. H. 2004 How species evolve collectively: implications of gene flow and selection for the spread of advantageous alleles. Mol. Ecol. 13, 1341-1356. (doi:10.1111/j.1365-294X.2004. 02164.x)
57. Nolte, A. W., Renaut, S. & Bernatchez, L. 2009 Divergence in gene regulation at young life history stages of whitefish (Coregonus sp.) and the emergence of genomic isolation. BMC Evol. Biol. 9, 59. (doi:10.1186/1471-2148-9- 59)
58. Noor, M. A. F. & Feder, J. L. 2006 Speciation genetics: evolving approaches. Nat. Rev. Genet. 7, 851-861. (doi: 10. 1038/nrg1968)
59. Nosil, P., Funk, D. J. & Ortiz-Barrientos, D. 2009a Divergent selection and heterogeneous genomic divergence. Mol. Ecol. 18, 375-402. (doi: 10.1111/J.1365-294X. 2008.03946.x)
60. Nosil, P., Harmon, L. J. & Seehausen, O. 2009e Ecological explanations for (incomplete) speciation. Trends Ecol. Evol. 24, 145-156. (doi:10.1016/j.tree.2008.10.011)
61. Oleksiak, M. F., Churchill, G. A. & Crawford, D. L. 2002 Variation in gene expression within and among natural populations. Nat Genet. 32, 261-266. (doi:10.1038/ ng983)
62. Orr, H. A. 1998 Testing natural selection versus genetic drift in phenotypic evolution using quantitative trait locus data. Genetics 149, 2099-2104.
63. Orr, H. A. 2005 The genetic theory of adaptation: a brief history. Nat. Rev. Genet 6, 119-127. (doi:10.1038/ nrg1523)
64. Orr, H. A. & Turelli, M. 2001 The evolution of postzygotic isolation: accumulating Dobzhansky-Muller incompatibilities. Evolution 55, 1085-1094.
65. Østbye, K., Bernatchez, L., Naesje, T. F. Himberg, M. & Hindar, K. 2005a Evolutionary history of European whitefish (Coregonus lavaretus L.) as inferred from mtDNA phylogeography and gill-raker numbers. Mol Ecol. 14, 4371-4388.
66. Ostbye, K., Naesje, T. F., Bernatchez, L., Sandlund, O. T. & Hindar, K. 20056 Morphological divergence and origin of sympatric populations of European whitefish (Coregonus lavaretus L.) in Lake Femund, Norway. J. Evol. Biol. 18, 683-702. (doi:10.1111/j.1420-9101.2004.00844.x)
67. Ostbye, K., Amundsen, P.-A., Bernatchez, L., Klemetsen, A., Knudsen, R., Kristoffersen, R., Naesje, T. F. & Hindar, K. 2006 Parallel evolution of eco-morphological traits in European whitefish Coregonus lavaretus (L.) during postglacial times. Mol. Ecol. 15, 3983-4001. (doi:10.1111/j.1365-294X.2006. 03062.x)
68. Pigeon, D., Chouinard, A. & Bernatchez, L. 1997 Multiple modes of speciation involved in the parallel evolution of sympatric morphotypes of lake whitefish Coregonus clupeaformis, Salmonidae. Evolution 51,196-205. (doi:10.2307/ 2410973)
69. Ranz, J. M. & Machado, C. A. 2005 Uncovering evolutionary patterns of gene expression using microarrays. Trends Ecol. Evol. 21, 29-37. (doi:10.1016/j.tree.2005.09.002)
70. Ranz, J. M., Namgyal, K., Gibson, G. & Hard, D. 2004 Anomalies in the expression profile of interspecific hybrids of Drosophila melanogaster and Drosophila simulons. Genome Res. 14, 373-379. (doi:10.1101/gr.2019804)
71. Renaut, S., Nolte, A. W. & Bernatchez, L. 2009 Gene expression divergence and hybrid misexpression between lake whitefish species pairs (Coregonus spp. Salmonidae). Mol. Biol. Evol. 26, 925-936. (doi:10.1093/molbev/ msp017)
72. Renaut, S., Nolte, A. W. & Bernatchez, L. 2010 Mining transcriptome sequences towards identifying adaptive single nucleotide polymorphisms in lake whitefish species pairs (Coregonus sp.). Mol. Ecol. 19(Suppl. 1), 115-131.
73. Reshetnikov, J. S. 1988 Coregonid fishes in recent conditions. Finn. Fish. Res. 9, 11-16.
74. Rice, W. R. & Hosten, E. E. 1993 Laboratory experiments on speciation: what have we learned in 40 years? Evolution 47, 1637-1653. (doi:10.2307/2410209)
75. Rieseberg, L. H. 1998 Genetic mapping as a tool for studying speciation. Molecular systematics of plants 2 (eds D. E. Soltis, P. S. Soltis & J. J. Doyle), pp. 459-787. New York, NY: Chapman & Hall.
76. Rieseberg, L. H., Whitton, J. & Gardner, K. 1999 Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152, 713-727.
77. Rise, M. L. et al. 2004 Development and application of a salmonid EST database and cDNA microarray: data mining and interspecific hybridization characteristics. Genome Res. 14,478-490. (doi:10.1101/gr.1687304)
78. Rise, M. L., von Schalburg, K. R., Cooper, G. A. & Koop, B. F. 2007 Salmonid DNA microarrays and other tools for functional genomics research. In Aquaculture Genome Technologies (ed. Z. Liu), pp. 369-411. Oxford, UK: Blackwell Publishing.
79. Roff, D. A. 2007 Contributions of genomics to life-history theory. Nat. Rev. Genet. 8, 116-125. (doi:10.1038/ nrg2040)
80. Rogers, S. M. & Bernatchez, L. 2005 Integrating QTL mapping and genomic scans towards the characterization of candidate loci under parallel directional selection in the lake whitefish (Coregonus clupeaformis). Mol. Ecol. 14, 351-361. (doi:10.1111/j.1365-294X.2004.02396.x)
81. Rogers, S. M. & Bernatchez, L. 2006 The genetic basis of intrinsic and extrinsic postzygotic reproductive isolation jointly promoting speciation in the lake whitefish sepcies complex (Coregonus Clupeaformis). J. Evol. Biol. 19, 1979-1994. (doi: 10.1111/j.1420-9101.2006.01150.x)
82. 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)
83. Rogers, S. M., Campbell, D., Baird, S., Danzmann, R. G. & Bernatchez, L. 2001 Combining the analyses of introgressive hybridization and linkage mapping to investigate the genetic architecture of population divergence in the lake whitefish (Coregonus clupeaformis, Mitchill). Genetica 111, 25-41. (doi:10.1023/A:1013773600304)
84. Rogers, M. R., Gagnon, V. & Bernatchez, L. 2002 Genetically based phenotype-environment association for swimming behavior in lake whitefish ecotypes (Coregonus clupeaformis Mitchill). Evolution 56, 2322-2329.
85. Rogers, S. M., Isabel, N. & Bernatchez, L. 2007 Linkage maps of the dwarf and normal lake whitefish (Coregonus Clupeaformis) species complex and their hybrids reveal the genetic architecture of population divergence. Genetics 175, 1-24.
86. Rokas, A. & Abbot, P. 2009 Harnessing genomics for evolutionary insights. Trends Ecol. Evol. 24, 192-200. (doi:10.1016/j.tree.2008.11.004)
87. Rundell, R. J. & Price, T. D. 2009 Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation. Trends Ecol. Evol. 24, 394-399. (doi:10.1016/j.tree.2009.02.007)
88. Schemske, D. W. & Bierzychudek, P. 2007 Spatial differentiation for flower color in the desert annual Linanthus parryae: was Wright right? Evolution 61, 2528-2543. (doi:10.1111/j.1558-5646.2007.00219.x)
89. Schluter, D. 2000 The ecology of adaptive radiation. Oxford, UK: Oxford University Press.
90. Schluter, D. 2009 Evidence for ecological speciation and its alternative. Science 323, 737-741. (doi:10.1126/science. 1160006)
91. Spitze, K. 1993 Population structure in Daphnia obtusa: quantitative genetic and allozymic variation. Genetics 135, 367-374.
92. St-Cyr, J., Derome, N. & Bernatchez, L. 2008 The transcriptomics of life-history trade-offs in whitefish species pairs (Coregonus sp.). Mol. Ecol. 17, 1850-1870. (doi: 10.1111/j.1365-294X.2008.03696.x)
93. 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)
94. Storz, J. F., Sabatino, S. J., Hoffmann, F. G., Gering, E. J., Moriyama, H., Ferrand, N., Monteiro, B. & Nachman, M. W. 2007 The molecular basis of high-altitude adaptation in deer mice. PLoS Genet. 3, 448-459.
95. Torres, T., Metta, M., Ottenwalder, B. & Schlotterer, C. 2007 Gene expression profiling by massively parallel sequencing. Genome Res. 18, 172-177. (doi:10.1101/gr. 6984908)
96. Trudel, M., Tremblay, A., Schetagne, R. & Rasmussen, J. 2001 Why are dwarf fish so small? An energetic analysis of polymorphism in lake whitefish (Coregonus clupeaformis). Can. J. Fish. Aquat. Sci. 58, 394-405. (doi:10. 1139/cjfas-58-2-394)
97. 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)
98. van der Sluijs, L, van Dooren, T. J. M., Seehausen, O. & van Alphen, J. J. M. 2008 A test of fitness consequences of hybridization in sibling species of Lake Victoria cichlid fish. J. Evol. Biol. 21, 480-491. (doi:10.111 l/j.14209101.2007.01495.x)
99. Vasemagi, A. & Primmer, C. R. 2005 Challenges for identifying 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)
100. Vera, J. C., Wheat, C. W., Fescemyer, H. W., Frilander, M. J., Crawford, D. L., Hnski, I. & Marden, J. H. 2008 Rapid transcriptome characterization for a nonmodel organism using 454 pyrosequencing. Mol. Ecol. 17, 1636-1647. (doi:10.1111/j.1365-294X.2008.03666.x)
101. Via, S. 2009 Natural selection in action during speciation. Proc. Natl Acad. Sci. USA 106, 9939-9946. (doi: 10. 1073/pnas.0901397106)
102. 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)
103. Vogl, C. & Xu, S. Z. 2000 Multipoint mapping of viability and segregation distorting loci using molecular markers. Genetics 155, 1439-1447.
104. Vonlanthen, P., Roy, D., Hudson, A. G., Largiader, C. R., Bittner, D. & Seehausen, O. 2009 Divergence along a steep ecological gradient in lake whitefish (Coregonus sp.). J. Evol. Biol. 22, 498-514. (doi:10.1111/j.14209101. 2008.01670.x)
105. von Schalburg, K. R., Rise, M. L., Cooper, G. A., Brown, G. D., Gibbs, A. R., Nelson, C. C., Davidson, W. S. & Koop, B. F. 2005 Fish and chips: various methodologies demonstrate utility of a 16, 006-gene salmonid microarray. BMC Genomics 6, 126. (doi:10.1186/1471-2164-6126)
106. Wentzell, A. M., Rowe, H. C., Hansen, B. G., Ticconi, C., Halkier, B. A. & Kliebenstein, D. J. 2007 Linking metabolic QTLs with network and cis-eQTLs controlling biosynthetic pathways. PLoS Genet. 3, 1687-1701.
107. Whiteley, A. R. et al. 2008 The phenomics and expression quantitative trait locus mapping of brain transcriptomes regulating adaptive divergence in lake whitefish species pairs (Coregonus sp.). Genetics 180, 147-164. (doi:10. 1534/genetics.108.089938)
108. Whiteley, A. R., Persaud, K. N., Derome, N., Montgomerie, R. & Bernatchez, L. 2009 Reduced sperm performance in backcross hybrids between species pairs of whitefish (Coregonus clupeaformis). Can. J. Zool. 87, 566-572. (doi:10.1139/Z09-042)
109. Wittkopp, P. J. 2007 Variable gene expression in eukaryotes: a network perspective. J. Exp. Biol. 210, 1567-1575. (doi:10.1242/jeb.002592)
110. Wray, G. A. 2007 The evolutionary significance of cisregulatory mutations. Nat. Rev. Genet. 8, 206-216. (doi:10.1038/nrg2063)
111. Wu, C. I. & Ting, C. T. 2004 Genes and speciation. Nat. Rev. Genet 5, 114-122. (doi:10.1038/nrg1269)