High degree of genetic differentiation in marine three-spined sticklebacks (Gasterosteus aculeatus)

Molecular Ecology

Volumn 22, Issue 18, 2013, Pages 4811-4828

  Defaveri, Jacquelin ^a   Shikano, Takahito ^a   Shimada, Yukinori ^a,b   Merilä, Juha ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b TOKYO UNIVERSITY OF MARINE SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

candidate gene; F ST; genomic heterogeneity; marine; population differentiation

Indexed keywords

GASTEROSTEUS ACULEATUS;

EID: 84883744195     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12430     Document Type: Article

References (123)

1. Aeschlimann PB, Häberli MA, Reusch TBH, Boehm T, Milinski M, (2003) Female sticklebacks Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection. Behavioral Ecology and Sociobiology, 54, 119-126.
2. André C, Larsson LC, Laikre L, et al,. (2011) Detecting population structure in a high gene-flow species, Atlantic herring (Clupea harengus): direct, simultaneous evaluation of neutral vs putatively selected loci. Heredity, 106, 270-280.
3. ST-outlier method. BMC Bioinformatics, 9, 323.
4. Avise JC, (1992) Molecular population structure and the biogeographic history of a regional fauna: a case history with lessons for conservation biology. Oikos, 63, 62-76.
5. Bamshad M, Wooding SP, (2003) Signatures of natural selection in the human genome. Nature Reviews Genetics, 4, 99-111.
6. Beaumont MA, Balding DJ, (2004) Identifying adaptive genetic divergence among populations from genome-scans. Molecular Ecology, 13, 969-980.
7. Beaumont MA, Nichols RA, (1996) Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society of London, Series B: Biological Sciences, 263, 1619-1626.
8. Behrens Yamada S, (1989) Are direct developers more locally adapted than planktonic developers? Marine Biology, 103, 403-412.
9. Bell MA, Foster SA, (1994) The Evolutionary Biology of the Threespine Stickleback. Oxford University Press, Oxford.
10. Billerbeck JM, Schultz ET, Conover DO, (2000) Adaptive variation in energy acquisition and allocation among latitudinal populations of the Atlantic silverside. Oecologia, 122, 210-219.
11. Bradbury IR, Hubert S, Higgins B, et al,. (2010) Parallel adaptive evolution of Atlantic cod on both sides of the Atlantic Ocean in response to temperature. Proceedings of the Royal Society of London, Series B: Biological Sciences, 277, 3725-3734.
12. Bradbury IR, Hubert S, Higgins B, et al,. (2013) Genomic islands of divergence and their consequences for the resolution of spatial structure in an exploited marine fish. Evolutionary Applications, 6, 450-461.
13. Bridle JR, Vines TH, (2007) Limits to evolution at range margins: when and why does adaptation fail? Trends in Ecology and Evolution, 22, 140-147.
14. Burton RS, (1986) Evolutionary consequences of restricted gene flow among natural populations of the copepod Tigriopus californicus. Bulletin of Marine Sciences, 39, 526-535.
15. Calvés I, Lavergne E, Meisterzheim AL, et al,. (2013) Genetic structure of European flounder Platichthys flesus: effects of both the southern limit of the species' range and chemical stress. Marine Ecological Progress Series, 472, 257-273.
16. Cano JM, Shikano T, Kuparinen A, Merilä J, (2008) Genetic differentiation, effective population size and gene flow in marine fishes: implications for stock management. Journal of Integrative Field Biology, 5, 1-10.
17. Colosimo PF, Hosemann KE, Balabhadra S, et al,. (2005) Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science, 307, 1928-1933.
18. Conover DO, Present TMC, (1990) Countergradient variation in growth rate: compensation for length of the growing season among Atlantic silversides from different latitudes. Oecologia, 83, 316-324.
19. Conover DO, Clarke LM, Munch SB, Wagner GN, (2006) Spatial and temporal scales of adaptive divergence in marine fishes and the implications for conservation. Journal of Fish Biology, 69, 21-47.
20. Corander J, Cheng L, Majander K, Merilä J, (2013) High degree of cryptic population differentiation in the Baltic Sea herring Clupea harengus. Molecular Ecology, 22, 2931-2940.
21. Coscia I, Vogiatzi E, Kotoulas G, Tsigenopoulos CS, Mariani S, (2012) Exploring neutral and adaptive processes in expanding populations of gilthead sea bream, Sparus aurata L., in the North-East Atlantic. Heredity, 108, 537-546.
22. Cowen RK, Lwiza KMM, Sponaugle S, Paris CB, Olson DB, (2000) Connectivity of marine populations: open or closed? Science, 287, 857-859.
23. Crawford NG, (2010) SMOGD: software for the measurement of genetic diversity. Molecular Ecology Resources, 10, 556-557.
24. Cross TF, Payne RH, (1978) Geographic variation in Atlantic cod, Gadus morhua, off eastern North America: a biochemical systematics approach. Journal of the Fisheries Research Board of Canada, 35, 117-123.
25. De Mita S, Thuillet A-C, Gay L, et al,. (2013) Detecting selection along environmental gradients: analysis of eight methods and their effectiveness for outbreeding and selfing populations. Molecular Ecology, 22, 1383-1399.
26. Deagle BE, Jones FC, Absher DM, Kingsley DM, Reimchen TE, (2013) Phylogeography and adaptation genetics of stickleback from the Haida Gwaii archipelago revealed using genome-wide single nucleotide polymorphism genotyping. Molecular Ecology, 22, 1917-1932.
27. DeFaveri J, Shikano T, Shimada Y, Goto A, Merilä J, (2011) Global analysis of genes involved in freshwater adaptation in threespine sticklebacks (Gasterosteus aculeatus). Evolution, 65, 1800-1807.
28. DeFaveri J, Jonsson PR, Merilä J, (2013) Heterogeneous genomic differentiation in marine threespine sticklebacks: adaptation along an environmental gradient. Evolution. doi: 10.1111/evo.12097 (in press).
29. DeWoody JA, Avise JC, (2000) Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. Journal of Fish Biology, 56, 461-473.
30. Earl DA, vonHoldt BM, (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359-361.
31. Ellis JR, Burke JM, (2007) EST-SSRs as a resource for population genetic analyses. Heredity, 99, 125-132.
32. 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.
33. Excoffier L, Lischer HL, (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.
34. Excoffier L, Hofer T, Foll M, (2009) Detecting loci under selection in a hierarchically structured population. Heredity, 103, 285-298.
35. Feder JL, Egan SP, Nosil P, (2012) The genomics of speciation-with-gene- flow. Trends in Genetics, 28, 340-350.
36. Feulner PGD, Chain FJJ, Pancal M, et al,. (2013) Genome-wide patterns of standing genetic variation in a marine population of three-spined sticklebacks. Molecular Ecology, 22, 635-649.
37. Flaxman SM, Feder JL, Nosil P, (2013) Genetic hitchhiking and the dynamic buildup of genomic divergence during speciation with gene flow. Evolution. doi: 10.1111/evo. 12055 (in press).
38. 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.
39. Frydenberg O, Møller D, Nævdal G, Sick K, (1965) Haemoglobin polymorphism in Norwegian cod populations. Hereditas, 53, 257-271.
40. Funk WC, McKay JK, Hohenlohe PA, Allendorf FW, (2012) Harnessing genomics for delineating conservation units. Trends in Ecology and Evolution, 27, 489-496.
41. Gaggiotti OE, Bekkevold D, Jørgensen HBH, et al,. (2009) Disentangling the effects of evolutionary, demographic, and environmental factors influencing genetic structure of natural populations: Atlantic herring as a case study. Evolution, 63, 2939-2951.
42. Glover KA, Hansen MM, Lien S, Als TD, Høyheim B, Skaala Ø, (2010) A comparison of SNP and STR loci for delineating population structure and performing individual genetic assignment. BMC Genetics, 11, 2.
43. Goetz FW, MacKenzie S, (2008) Functional genomics with microarrays in fish biology and fisheries. Fish and Fisheries, 9, 378-395.
44. Goudet J, (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www2.unil.ch/popgen/ softwares/fstat.htm (last accessed on 09 July 2013).
45. Grosberg R, Cunningham CW, (2001) Genetic structure in the sea: from populations to communities. In: Marine Community Ecology (eds, Bertness MD, Gaines SD, Hay ME,), pp. 61-84. Sinauer Associates, Sunderland, Massachusetts.
46. Gyllensten U, (1985) The genetic structure of fish-differences in the intraspecific distribution of biochemical genetic variation between marine anadromous, and fresh-water species. Journal of Fish Biology, 26, 691-699.
47. Haglund TR, Buth DG, Lawson R, (1992) Allozyme variation and phylogenetic relationships of Asian, North American, and European populations of the threespine stickleback, Gasterosteus aculeatus. Copeia, 1992, 432-443.
48. Hauser L, Carvalho GR, (2008) Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish and Fisheries, 9, 333-362.
49. Hedgecock D, (1986) Is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine invertebrates?. Bulletin of Marine Science, 39, 550-564.
50. Hedrick PW, (2005) A standardized genetic differentiation measure. Evolution, 59, 1633-1638.
51. Hellberg ME, (2009) Gene flow and isolation among populations of marine animals. Annual Review of Ecology, Evolution, and Systematics, 40, 291-310.
52. Hemmer-Hansen J, Nielsen EE, Frydenberg J, Loeschcke V, (2007) Adaptive divergence in a high gene flow environment: Hsc70 variation in the European flounder (Platichthys flesus L.). Heredity, 99, 592-600.
53. Herrera VL, Xie HX, Lopez LV, Schork NJ, Ruiz-Opazo N, (1998) The alpha1 Na, K-ATPase gene is a susceptibility hypertension gene in the Dahl salt-sensitive HSD rat. Journal of Clinical Investigations, 102, 1102-1111.
54. Hice LA, Duffy TA, Munch SB, Conover DO, (2012) Spatial scale and divergent patterns of variation in adapted traits in the ocean. Ecology Letters, 15, 568-575.
55. Hilbish TJ, Koehn RK, (1985) The physiological basis of natural selection at the LAP locus. Evolution, 39, 1302-1317.
56. Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA, (2010) Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genetics, 6, e1000862.
57. Hohenlohe PA, Bassham S, Currey M, Cresko WA, (2012) Extensive linkage disequilibrium and parallel adaptive divergence across threespine stickleback genomes. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences, 367, 395-408.
58. Hutchings JA, Swain DP, Rowe S, Eddington JD, Puvanendran V, Brown JA, (2007) Genetic variation in life-history reaction norms in a marine fish. Proceedings of the Royal Society of London, Series B: Biological Sciences, 274, 1693-1699.
59. Iwata M, (1973) Genetic polymorphism of tetrazolium oxidase in walleye pollock. Japanese Journal of Genetics, 48, 147-149.
60. Johannesson K, André C, (2006) Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea. Molecular Ecology, 15, 2013-2029.
61. Jones DH, John AWG, (1978) A three-spined stickleback, Gasterosteus aculeatus L. from the north Atlantic. Journal of Fish Biology, 13, 231-236.
62. Jones F, Brown C, Pemberton J, Braithwaite V, (2006) Reproductive isolation in a threespine stickleback hybrid zone. Journal of Evolutionary Biology, 19, 1531-1544.
63. Jones FC, Chan YF, Schmutz J, et al,. (2012a) A genome-wide SNP genotyping array reveals patterns of global and repeated species-pair divergence in sticklebacks. Current Biology, 22, 83-90.
64. Jones FC, Grabherr MG, Chan YF, et al,. (2012b) The genomic basis of adaptive evolution in threespine sticklebacks. Nature, 484, 55-61.
65. Joost S, Bonin A, Bruford MW, et al,. (2007) A spatial analysis method (SAM) to detect candidate loci for selection: towards a landscape genomics approach to adaptation. Molecular Ecology, 16, 3955-3969.
66. Joost S, Kalbermatten M, Bonin A, (2008) Spatial analysis method (SAM): a software tool combining molecular and environmental data to identify candidate loci for selection. Molecular Ecology Resources, 8, 957-960.
67. ST and its relatives do not measure differentiation. Molecular Ecology, 17, 4015-4026.
68. Jurvelius J, Leinikki J, Mamylovc V, Pushkin S, (1996) Stock assessment of pelagic three-spined stickleback (Gasterosteus aculeatus): a simultaneous up- and down-looking echo-sounding study. Fisheries Research, 27, 227-241.
69. Kalinowski ST, (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes, 5, 187-189.
70. Kostamo K, Korpelainen H, Olsson S, (2012) Comparative study on the population genetics of the red algae Furcellaria lumbricalis occupying divergent salinity conditions. Marine Biology, 159, 561-571.
71. Lamichhaney S, Marinez Barrio A, Rafato N, et al,. (2012) Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring. Proceedings of the National Academy of Sciences of the United States of America, 20, 19345-19350.
72. Langella O, (2002) Populations 1.2.28. Logiciel de géné tique des populations. Available from: http://www.bioinformatics.org/~tryphon/ populations/#ancre.telechargement (last accessed on 4 January 2012).
73. Larmuseau MHD, Raeymaekers JAM, Ruddick KG, Van Houdt JKJ, Volckaert FAM, (2009) To see in different seas: spatial variation in the rhodopsin gene in the sand goby (Pomatoschistus minutus). Molecular Ecology, 18, 4227-4239.
74. Larmuseau MHD, VanCampenhout K, Raeymaekers JAM, Van Houdt JKJ, Volckaert FAM, (2010) Differential modes of selection on the rhodopsin gene in coastal Baltic and North Sea populations of the sand goby, Pomatoschistus minutus. Molecular Ecology, 19, 2256-2268.
75. Larsen PF, Nielsen EE, Williams TD, et al,. (2007) Adaptive differences in gene expression in European flounder (Platichthys flesus). Molecular Ecology, 16, 4674-4683.
76. Larsen PF, Nielsen EE, Williams TD, Loeschcke V, (2008) Intraspecific variation in expression of candidate genes for osmoregulation, heme biosynthesis and stress resistance suggests local adaptation in European flounder (Platichthys flesus). Heredity, 101, 247-259.
77. Larsen PF, Nielsen EE, Meier K, Olsvik PA, Hansen MM, Loeschcke V, (2012) Differences in salinity tolerance and gene expression between two populations of Atlantic cod (Gadus morhua) in response to salinity stress. Biochemical Genetics, 50, 454-466.
78. Leinonen T, O'Hara RB, Cano JM, Merilä J, (2008) Comparative studies of quantitative trait and neutral marker divergence: a meta-analysis. Journal of Evolutionary Biology, 21, 1-17.
79. ST comparisons: evolutionary and ecological insights from genomic heterogeneity. Nature Reviews Genetics, 14, 179-190.
80. Limborg MT, Heylar SJ, De Bruyn M, et al,. (2012) Environmental selection on transcriptome-derived SNPs in a high gene flow marine fish, the Atlantic herring (Clupea harengus). Molecular Ecology, 21, 3686-3703.
81. Luttikhuizen PC, Drent J, van Delden W, Piersma T, (2003) Spatially structured genetic variation in a broadcast spawning bivalve: quantitative versus molecular traits. Journal of Evolutionary Biology, 16, 260-272.
82. Mäkinen HS, Merilä J, (2008) Mitochondrial DNA phylogeography of the three-spined stickleback (Gasterosteus aculeatus) in Europe-evidence for multiple glacial refugia. Molecular Phylogenetics and Evolution, 46, 167-182.
83. Mäkinen HS, Cano JM, Merilä J, (2006) Genetic relationships among marine and freshwater populations of the European three-spined stickleback (Gasterosteus aculeatus) revealed by microsatellites. Molecular Ecology, 15, 1519-1534.
84. Marcil J, Swain DP, Hutchings JA, (2006) Genetic and environmental components of phenotypic variation in body shape among populations of Atlantic cod (Gadus morhua L.). Biological Journal of the Linnean Society, 88, 351-365.
85. Merilä J, Crnokrak P, (2001) Comparison of genetic differentiation at marker loci and quantitative traits. Journal of Evolutionary Biology, 14, 892-903.
86. Michel AP, Sim S, Powell T, Nosil P, Feder JL, (2010) Widespread genomic divergence during sympatric speciation. Proceedings of the National Academy of Sciences of the United States of America, 107, 9724-9729.
87. Molina-Luzõn MJ, Lõpez NJR, Navajas-Pérez R, Robles F, Ruiz-Rejõn C, DeLaHerrán R, (2012) Validation and comparison of microsatellite markers derived from Senegalese sole (Solea senegalensis, Kaup) genomic and expressed sequence tags libraries. Molecular Ecology Resources, 12, 956-966.
88. Mork J, Ryman N, Ståhl G, Utter F, Sundness G, (1985) Genetic variation in Atlantic cod (Gadus morhua) throughout its range. Canadian Journal of Fisheries and Aquatic Sciences, 42, 1580-1587.
89. Nielsen EE, Hemmer-Hansen J, Larsen PF, Bekkevold D, (2009a) Population genomics of marine fishes: identifying adaptive variation in space and time. Molecular Ecology, 18, 3128-3150.
90. Nielsen EE, Hemmer-Hansen J, Poulsen NA, et al,. (2009b) Genomic signatures of local directional selection in a high gene flow marine organism; the Atlantic cod (Gadus morhua). BMC Evolutionary Biology, 9, 276.
91. Nielsen EE, Cariani A, Mac Aoidh E, et al,. (2012) Gene-associated markers provide tools for tackling illegal fishing and false eco-certification. Nature Communications, 3, 851.
92. Nosil P, Funk DJ, Ortiz-Barrientos D, (2009) Divergent selection and heterogeneous genomic divergence. Molecular Ecology, 18, 375-402.
93. Oetjen K, Ferber S, Dankert I, Reusch TBH, (2010) New evidence for habitat-specific selection in Wadden Sea Zostera marina populations revealed by genome-scanning using SNP and microsatellite markers. Marine Biology, 157, 81-89.
94. Ortí G, Bell MA, Reimchen TE, Meyer A, (1994) Global survey of mitochondrial DNA sequences in the threespine stickleback: evidence for recent migrations. Evolution, 48, 608-622.
95. Ovajeer E, Pihu E, Saat T, (2000) Fishes of Estonia. Estonian Marine Institute, Tallin.
96. Pespeni MH, Garfield DA, Manier MK, Palumbi SR, (2012) Genome-wide polymorphisms show unexpected targets of natural selection. Proceedings of the Royal Society of London, Series B: Biological Sciences, 279, 1412-1420.
97. Ponce-Palafox J, Martinez-Palacios CA, Ross LG, (1997) The effects of salinity and temperature on the growth and survival rates of juvenile white shrimp, Penaeus vannamei, Boone, 1931. Aquaculture, 157, 107-115.
98. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
99. Quinn TP, Light JT, (1988) Occurrence of threespine sticklebacks (Gasterosteus aculeatus) in the open North Pacific Ocean: migration or drift? Canadian Journal of Zoology, 67, 2850-2852.
100. Raeymaekers JAM, Maes GE, Audenaert E, Volckaert FAM, (2005) Detecting Holocene divergence in the anadromous-freshwater three-spined stickleback (Gasterosteus aculeatus) system. Molecular Ecology, 14, 1001-1014.
101. Raymond M, Rousset F, (1995) Genepop (Version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248-249.
102. Reed DH, Frankham R, (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution, 55, 1095-1103.
103. Reitzel AM, Herrera S, Layden MJ, Marindale MQ, Shank TM, (2013) Going where traditional markers have not gone before: utility of and promise for RAD sequencing in marine invertebrate phylogeography and population genomics. Molecular Ecology, 22, 2953-2970.
104. Rice WR, (1989) Analyzing tables of statistical tests. Evolution, 43, 223-225.
105. Russello MA, Kirk SL, Frazer KK, Askey PJ, (2011) Detection of outlier loci and their utility for fisheries management. Evolutionary Applications, 5, 39-52.
106. Sanford E, Kelly MW, (2011) Local adaptation in marine invertebrates. Annual Review of Marine Science, 3, 509-535.
107. Savolainen O, Pyhäjärvi T, Knürr T, (2007) Gene flow and local adaptation in trees. Annual Review of Ecology, Evolution, and Systematics, 38, 595-619.
108. Schluter D, Conte G, (2009) Genetics and ecological speciation. Proceedings of the National Academy of Sciences of the United States of America, 106, 9955-9962.
109. Schmidt PS, Rand DM, (1999) Intertidal microhabitat and selection at Mpi: interlocus contrasts in the northern acorn barnacle Semibalanus balanoides. Evolution, 53, 135-146.
110. Shikano T, Ramadevi J, Merilä J, (2010) Identification of local- and habitat-dependent selection: scanning functionally important genes in nine-spined sticklebacks (Pungitius pungitius). Molecular Biology and Evolution, 27, 2775-2789.
111. Shimada Y, Shikano T, Merilä J, (2011) A high incidence of selection on physiologically important genes in the three-spined stickleback, Gasterosteus aculeatus. Molecular Biology and Evolution, 28, 181-193.
112. Smith PJ, Fujio Y, (1982) Genetic variation in marine teleosts: high variability in habitat specialists and low variability in habitat generalists. Marine Biology, 69, 7-20.
113. Teacher AGF, André C, Jonsson PR, Merilä J, (2013) Oceanographic connectivity and environmental correlates of genetic structuring in Atlantic herring the Baltic Sea. Evolutionary Applications, 6, 549-567.
114. Travis JM, Munkemuller T, Burton OJ, (2010) Mutation surfing and the evolution of dispersal during range expansions. Journal of Evolutionary Biology, 23, 2656-2667.
115. Vasemägi A, Gross R, Paaver T, Koljonen M-L, Säisä M, Nilsson J, (2005a) Analysis of gene associated tandem repeat markers in Atlantic salmon (Salmo salar L.) populations: implications for restoration and conservation in the Baltic Sea. Conservation Genetics, 6, 385-397.
116. Vasemägi A, Nilsson J, Primmer A, (2005b) Expressed sequence tag-linked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in Atlantic salmon (Salmo salar L.). Molecular Biology and Evolution, 22, 1067-1076.
117. Via S, (2012) Divergence hitchhiking and the spread of genomic isolation during ecological speciation-with-gene-flow. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences, 367, 451-460.
118. Vilas R, Bouza C, Vera M, Millán A, Martínez P, (2010) Variation in anonymous and EST-microsatellites suggests adaptive population divergence in turbot. Marine Ecology Progress Series, 420, 231-239.
119. Ward RD, Woodwark M, Skibinski DOF, (1994) A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. Journal of Fish Biology, 44, 213-232.
120. Waters JM, Fraser CI, Hewitt GM, (2013) Founder takes all: density-dependent processes structure biodiversity. Trends in Ecology and Evolution, 28, 78-85.
121. Weersing K, Toonen RJ, (2009) Population genetics, larval dispersal, and connectivity in marine systems. Marine Ecology Progress Series, 393, 1-12.
122. Weir BS, Cockerham C, (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358-1370.
123. Wood HM, Grahame JW, Humphray S, Rogers J, Butlin RK, (2008) Sequence differentiation in regions identified by a genome-scan for local adaptation. Molecular Ecology, 17, 3123-3135.