Population genomic evidence for adaptive differentiation in Baltic Sea three-spined sticklebacks

BMC Biology

Volumn 13, Issue 1, 2015, Pages

  Guo, Baocheng ^a   DeFaveri, Jacquelin ^a   Sotelo, Graciela ^a,b   Nair, Abhilash ^a   Merilä, Juha ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b CENTRO DE INVESTIGAÇÃO EM BIODIVERSIDADE E RECURSOS GENÉTICOS   (Portugal)

Author keywords

Baltic Sea; Gasterosteus aculeatus; local adaptation; RAD sequencing; SNP, population differentiation

Indexed keywords

GASTEROSTEUS ACULEATUS; SPINACHIA SPINACHIA;

ADAPTATION; ANIMAL; DNA SEQUENCE; GENE ONTOLOGY; GENETIC ASSOCIATION; GENETIC DATABASE; GENETICS; GENOME; GEOGRAPHY; POPULATION GENETICS; RESTRICTION MAPPING; SEA; SINGLE NUCLEOTIDE POLYMORPHISM; SMEGMAMORPHA;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; DATABASES, GENETIC; GENE ONTOLOGY; GENETIC ASSOCIATION STUDIES; GENETICS, POPULATION; GENOME; GEOGRAPHY; OCEANS AND SEAS; POLYMORPHISM, SINGLE NUCLEOTIDE; RESTRICTION MAPPING; SEQUENCE ANALYSIS, DNA; SMEGMAMORPHA;

EID: 84928524608     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/s12915-015-0130-8     Document Type: Article

References (120)

1. Blanquart F, Gandon S, Nuismer SL. The effects of migration and drift on local adaptation to a heterogeneous environment. J Evol Biol. 2012;25:1351-63.
2. Blanquart F, Kaltz O, Nuismer SL, Gandon S. A practical guide to measuring local adaptation. Ecol Lett. 2013;16:1195-205.
3. Savolainen O, Lascoux M, Merilä J. Ecological genomics of local adaptation. Nat Rev Genet. 2013;14:807-20.
4. Hereford J. A quantitative survey of local adaptation and fitness trade-offs. Am Nat. 2009;173:579-88.
5. Kawecki TJ, Ebert D. Conceptual issues in local adaptation. Ecol Lett. 2004;7:1225-41.
6. Savolainen O, Pyhajarvi T, Knurr T. Gene flow and local adaptation in trees. Annu Rev Ecol Evol S. 2007;38:595-619.
7. Kremer A, Le Corre V. Decoupling of differentiation between traits and their underlying genes in response to divergent selection. Heredity. 2012;108:375-85.
8. ST comparisons: evolutionary and ecological insights from genomic heterogeneity. Nat Rev Genet. 2013;14:179-90.
9. Leinonen T, O'Hara RB, Cano JM, Merilä J. Comparative studies of quantitative trait and neutral marker divergence: a meta-analysis. J Evol Biol. 2008;21:1-17.
10. McKay JK, Latta RG. Adaptive population divergence: markers. QTL and traits Trends Ecol Evol. 2002;17:285-91.
11. Fan SH, Elmer KR, Meyer A. Genomics of adaptation and speciation in cichlid fishes: recent advances and analyses in African and neotropical lineages. Philos T R Soc B. 2012;367:385-94.
12. Hancock AM, Brachi B, Faure N, Horton MW, Jarymowycz LB, Sperone FG, et al. Adaptation to climate across the Arabidopsis thaliana genome. Science. 2011;334:83-6.
13. Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, Johnson J, et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature. 2012;484:55-61.
14. Pool JE, Hellmann I, Jensen JD, Nielsen R. Population genetic inference from genomic sequence variation. Genome Res. 2010;20:291-300.
15. De Mita S, Thuillet AC, Gay L, Ahmadi N, Manel S, Ronfort J, et al. Detecting selection along environmental gradients: analysis of eight methods and their effectiveness for outbreeding and selfing populations. Mol Ecol. 2013;22:1383-99.
16. ST outlier tests. Mol Ecol. 2014;23:2178-92.
17. Storz JF. Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol. 2005;14:671-88.
18. Cano JM, Shikano T, Kuparinen A, Merilä J. Genetic differentiation, effective population size and gene flow in marine fishes: implications for stock management. J Integr Field Biol. 2008;5:1-10.
19. DeWoody JA, Avise JC. Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J Fish Biol. 2000;56:461-73.
20. Grosberg R, Cunningham CW. Genetic structure in the sea: from populations to communities. In: Bertness MD, Gaines SD, Hay ME, editors. Marine Community Ecology. Sunderland, Massachusetts: Sinauer Associates; 2001. p. 61-84.
21. Gyllensten U. The genetic-structure of fish - differences in the intraspecific distribution of biochemical genetic-variation between marine, anadromous, and fresh-water species. J Fish Biol. 1985;26:691-9.
22. Ward RD, Woodwark M, Skibinski DOF. A comparison of genetic diversity levels in marine, fresh-water, and anadromous fishes. J Fish Biol. 1994;44:213-32.
23. Conover DO. Local adaptation in marine fishes: evidence and implications for stock enhancement. B Mar Sci. 1998;62:477-93.
24. Conover DO, Clarke LM, Munch SB, Wagner GN. Spatial and temporal scales of adaptive divergence in marine fishes and the implications for conservation. J Fish Biol. 2006;69:21-47.
25. DeFaveri J, Merilä J. Local adaptation to salinity in the three-spined stickleback? J Evol Biol. 2014;27:290-302.
26. Hice LA, Duffy TA, Munch SB, Conover DO. Spatial scale and divergent patterns of variation in adapted traits in the ocean. Ecol Lett. 2012;15:568-75.
27. Marcil J, Swain DP, Hutchings JA. Countergradient variation in body shape between two populations of Atlantic cod (Gadus morhua). P Roy Soc B-Biol Sci. 2006;273:217-23.
28. Bradbury IR, Hubert S, Higgins B, Borza T, Bowman S, Paterson IG, et al. Parallel adaptive evolution of Atlantic cod on both sides of the Atlantic Ocean in response to temperature. P Roy Soc B-Biol Sci. 2010;277:3725-34.
29. Corander J, Majander KK, Cheng L, Merilä J. High degree of cryptic population differentiation in the Baltic Sea herring Clupea harengus. Mol Ecol. 2013;22:2931-40.
30. Hale MC, Thrower FP, Berntson EA, Miller MR, Nichols KM. Evaluating. adaptive divergence between migratory and nonmigratory ecotypes of a salmonid fish, Oncorhynchus mykiss. G3-Genes Genom Genet. 2013;3:1273-85.
31. Lamichhaney S, Barrio AM, Rafati N, Sundstrom G, Rubin CJ, Gilbert ER, et al. Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring. P Natl Acad Sci USA. 2012;109:19345-50.
32. Pujolar JM, Jacobsen MW, Als TD, Frydenberg J, Munch K, Jonsson B, et al. Genome-wide single-generation signatures of local selection in the panmictic European eel. Mol Ecol. 2014;23:2514-28.
33. DeFaveri J, Shikano T, Shimada Y, Merilä J. High degree of genetic differentiation in marine three-spined sticklebacks (Gasterosteus aculeatus). Mol Ecol. 2013;22:4811-28.
34. Hemmer-Hansen J, Nielsen EE, Frydenberg J, Loeschcke V. Adaptive divergence in a high gene flow environment: Hsc70 variation in the European flounder (Platichthys flesus L.). Heredity. 2007;99:592-600.
35. Limborg MT, Helyar SJ, de Bruyn M, Taylor MI, Nielsen EE, Ogden R, et al. Environmental selection on transcriptome-derived SNPs in a high gene flow marine fish, the Atlantic herring (Clupea harengus). Mol Ecol. 2012;21:3686-703.
36. Nielsen EE, Hemmer-Hansen J, Poulsen NA, Loeschcke V, Moen T, Johansen T, et al. Genomic signatures of local directional selection in a high gene flow marine organism; the Atlantic cod (Gadus morhua). BMC Evol Biol. 2009;9:276.
37. Shikano T, Ramadevi J, Merilä J. Identification of local- and habitat-dependent selection: scanning functionally important genes in nine-spined sticklebacks (Pungitius pungitius). Mol Biol Evol. 2010;27:2775-89.
38. Teacher AGF, Andre C, Jonsson PR, Merilä J. Oceanographic connectivity and environmental correlates of genetic structuring in Atlantic herring in the Baltic Sea. Evol Appl. 2013;6:549-67.
39. Jackson AM, Semmens BX. Sadovy de Mitcheson Y, Nemeth RS, Heppell SA, Bush PG, et al. Population structure and phylogeography in Nassau grouper (Epinephelus striatus), a mass-aggregating marine fish. PloS One. 2014;9:e97508.
40. Karlsen BO, Klingan K, Emblem A, Jorgensen TE, Jueterbock A, Furmanek T, et al. Genomic divergence between the migratory and stationary ecotypes of Atlantic cod. Mol Ecol. 2013;22:5098-111.
41. Kruck NC, Innes DI, Ovenden JR. New SNPs for population genetic analysis reveal possible cryptic speciation of eastern Australian sea mullet (Mugil cephalus). Mol Ecol Resour. 2013;13:715-25.
42. Liggins L, Treml EA, Riginos C. Taking the plunge: an introduction to undertaking seascape genetic studies and using biophysical models. Geogr Compass. 2013;7:173-96.
43. Selkoe KA, Henzler CM, Gaines SD. Seascape genetics and the spatial ecology of marine populations. Fish Fish. 2008;9:363-77.
44. Albert AY, Sawaya S, Vines TH, Knecht AK, Miller CT, Summers BR, et al. The genetics of adaptive shape shift in stickleback: pleiotropy and effect size. Evolution. 2008;62:76-85.
45. Barrett RD, Paccard A, Healy TM, Bergek S, Schulte PM, Schluter D, et al. Rapid evolution of cold tolerance in stickleback. P Roy Soc B-Biol Sci. 2011;278:233-8.
46. Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G, Dickson M, Grimwood J, et al. Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science. 2005;307:1928-33.
47. DeFaveri J, Jonsson PR, Merilä J. Heterogeneous genomic differentiation in marine threespine sticklebacks: adaptation along an environmental gradient. Evolution. 2013;67:2530-46.
48. DeFaveri J, Merilä J. Evidence for adaptive phenotypic differentiation in Baltic Sea sticklebacks. J Evol Biol. 2013;26:1700-15.
49. DeFaveri J, Shikano T, Shimada Y, Goto A, Merilä J. Global analysis of genes involved in freshwater adaptation in threespine sticklebacks (Gasterosteus aculeatus). Evolution. 2011;65:1800-7.
50. Marchinko KB, Schluter D. Parallel evolution by correlated response: lateral plate reduction in threespine stickleback. Evolution. 2007;61:1084-90.
51. McCairns RJS, Bernatchez L. Landscape genetic analyses reveal cryptic population structure and putative selection gradients in a large-scale estuarine environment. Mol Ecol. 2008;17:3901-16.
52. McCairns RJS, Bernatchez L. Adaptive divergence between freshwater and marine sticklebacks: insights into the role of phenotypic plasticity from an integrated analysis of candidate gene expression. Evolution. 2010;64:1029-47.
53. McCairns RJS, Bourget S, Bernatchez L. Putative causes and consequences of MHC variation within and between locally adapted stickleback demes. Mol Ecol. 2011;20:486-502.
54. ST in three-spined stickleback (Gasterosteus aculeatus) populations along a coastal-inland gradient. Mol Ecol. 2007;16:891-905.
55. Hendry AP, Peichel CL, Matthews B, Boughman JW, Nosil P. Stickleback research: the now and the next. Evol Ecol Res. 2013;15:111-41.
56. Catchen J, Bassham S, Wilson T, Currey M, O'Brien C, Yeates Q, et al. The population structure and recent colonization history of Oregon threespine stickleback determined using restriction-site associated DNA-sequencing. Mol Ecol. 2013;22:2864-83.
57. Ferchaud AL, Pedersen SH, Bekkevold D, Jian J, Niu Y, Hansen MM, et al. A low-density SNP array for analyzing differential selection in freshwater and marine populations of threespine stickleback (Gasterosteus aculeatus). BMC Genomics. 2014;15:867.
58. Feulner PGD, Chain FJJ, Panchal M, Eizaguirre C, Kalbe M, Lenz TL, et al. Genome-wide patterns of standing genetic variation in a marine population of three-spined sticklebacks. Mol Ecol. 2013;22:635-49.
59. Hohenlohe PA, Bassham S, Currey M, Cresko WA. Extensive linkage disequilibrium and parallel adaptive divergence across threespine stickleback genomes. Philos T R Soc B. 2012;367:395-408.
60. Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA, et al. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 2010;6:e1000862.
61. Jones FC, Chan YF, Schmutz J, Grimwood J, Brady SD, Southwick AM, et al. A genome-wide SNP genotyping array reveals patterns of global and repeated species-pair divergence in sticklebacks. Curr Biol. 2012;22:83-90.
62. Roesti M, Gavrilets S, Hendry AP, Salzburger W, Berner D. The genomic signature of parallel adaptation from shared genetic variation. Mol Ecol. 2014;23:3944-56.
63. Roesti M, Hendry AP, Salzburger W, Berner D. Genome divergence during evolutionary diversification as revealed in replicate lake-stream stickleback population pairs. Mol Ecol. 2012;21:2852-62.
64. Roesti M, Moser D, Berner D. Recombination in the threespine stickleback genome - patterns and consequences. Mol Ecol. 2013;22:3014-27.
65. Terekhanova NV, Logacheva MD, Penin AA, Neretina TV, Barmintseva AE, Bazykin GA, et al. Fast evolution from precast bricks: genomics of young freshwater populations of threespine stickleback Gasterosteus aculeatus. PLoS Genet. 2014;10:e1004696.
66. DeFaveri J, Shikano T, Ab Ghani NI, Merilä J. Contrasting population structures in two sympatric fishes in the Baltic Sea basin. Mar Biol. 2012;159:1659-72.
67. Hämmerli A, Reusch TB. Local adaptation and transplant dominance in genets of the marine clonal plant Zostera marina. Mar Ecol Prog Ser. 2002;242:111-8.
68. Wrange AL, Andre C, Lundh T, Lind U, Blomberg A, Jonsson PJ, et al. Importance of plasticity and local adaptation for coping with changing salinity in coastal areas: a test case with barnacles in the Baltic Sea. BMC Evol Biol. 2014;14:156.
69. Johannesson K, Smolarz K, Grahn M, Andre C. The future of Baltic Sea populations: local extinction or evolutionary rescue? Ambio. 2011;40:179-90.
70. Johannesson K, Andre C. Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea. Mol Ecol. 2006;15:2013-29.
71. Wennerstrom L, Laikre L, Ryman N, Utter FM, Ab Ghani NI, Andre C, et al. Genetic biodiversity in the Baltic Sea: species-specific patterns challenge management. Biodivers Conserv. 2013;22:3045-65.
72. Davey JW, Blaxter ML. RADSeq: next-generation population genetics. Brief Funct Genomics. 2010;9:416-23.
73. Coop G, Witonsky D, Di Rienzo A, Pritchard JK. Using environmental correlations to identify loci underlying local adaptation. Genetics. 2010;185:1411-23.
74. Jeffreys H. Theory of Probability. 3rd ed. London: Oxford University Press; 1961.
75. Nielsen EE, Hemmer-Hansen J, Larsen PF, Bekkevold D. Population genomics of marine fishes: identifying adaptive variation in space and time. Mol Ecol. 2009;18:3128-50.
76. Nosil P, Funk DJ, Ortiz-Barrientos D. Divergent selection and heterogeneous genomic divergence. Mol Ecol. 2009;18:375-402.
77. Yeaman S, Whitlock MC. The genetic architecture of adaptation under migration-selection balance. Evolution. 2011;65:1897-911.
78. Flaxman SM, Feder JL, Nosil P. Genetic hitchhiking and the dynamic buildup of genomic divergence during speciation with gene flow. Evolution. 2013;67:2577-91.
79. Jacobsen MW, Pujolar JM, Bernatchez L, Munch K, Jian J, Niu Y, et al. Genomic footprints of speciation in Atlantic eels (Anguilla anguilla and A. rostrata). Mol Ecol. 2014;23:4785-98.
80. Michel AP, Sim S, Powell THQ, Taylor MS, Nosil P, Feder JL, et al. Widespread genomic divergence during sympatric speciation. P Natl Acad Sci USA. 2010;107:9724-9.
81. Via S. Divergence hitchhiking and the spread of genomic isolation during ecological speciation-with-gene-flow. Philos T R Soc B. 2012;367:451-60.
82. Feder JL, Egan SP, Nosil P. The genomics of speciation-with-gene-flow. Trends Genet. 2012;28:342-50.
83. Seehausen O, Butlin RK, Keller I, Wagner CE, Boughman JW, Hohenlohe PA, et al. Genomics and the origin of species. Nat Rev Genet. 2014;15:176-92.
84. Hauser L, Carvalho GR. Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish. 2008;9:333-62.
85. Beaumont MA. Selection and sticklebacks. Mol Ecol. 2008;17:3425-7.
86. Makinen HS, Cano JM, Merilä J. Identifying footprints of directional and balancing selection in marine and freshwater three-spined stickleback (Gasterosteus aculeatus) populations. Mol Ecol. 2008;17:3565-82.
87. Hedrick PW. A standardized genetic differentiation measure. Evolution. 2005;59:1633-8.
88. Nichols RA, Freeman KL. Using molecular markers with high mutation rates to obtain estimates of relative population size and to distinguish the effects of gene flow and mutation: a demonstration using data from endemic Mauritian skinks. Mol Ecol. 2004;13:775-87.
89. Newman RM, Hall L, Connole M, Chen GL, Sato S, Yuste E, et al. Balancing selection and the evolution of functional polymorphism in Old World monkey TRIM5aα. P Natl Acad Sci USA. 2006;103:19134-9.
90. Kamiya T, O'Dwyer K, Westerdahl H, Senior A, Nakagawa S. A quantitative review of MHC-based mating preference: the role of diversity and dissimilarity. Mol Ecol. 2014;23:5151-63.
91. Sommer S. The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool. 2005;2:16.
92. Altizer S, Harvell D, Friedle E. Rapid evolutionary dynamics and disease threats to biodiversity. Trends Ecol Evol. 2003;18:589-96.
93. Budria A, Candolin U. Human-induced eutrophication maintains high parasite prevalence in breeding threespine stickleback populations. Parasitology. 2014. doi:10.1017/S0031182014001814.
94. Zander CD. Parasite diversity of sticklebacks from the Baltic Sea. Parasitol Res. 2007;100:287-97.
95. Wang G, Yang E, Smith KJ, Zeng Y, Ji G, Connon R, et al. Gene expression responses of threespine stickleback to salinity: implications for salt-sensitive hypertension. Front Genet. 2014;5:312.
96. Deagle BE, Jones FC, Chan YGF, Absher DM, Kingsley DM, Reimchen TE, et al. Population genomics of parallel phenotypic evolution in stickleback across stream-lake ecological transitions. P Roy Soc B-Biol Sci. 2012;279:1277-86.
97. Ojaveer H, Jaanus A, Mackenzie BR, Martin G, Olenin S, Radziejewska T, et al. Status of biodiversity in the Baltic Sea. PLoS One. 2010;5:e12467.
98. Schluter D, Conte GL. Genetics and ecological speciation. P Natl Acad Sci USA. 2009;106:9955-62.
99. Star B, Nederbragt AJ, Jentoft S, Grimholt U, Malmstrom M, Gregers TF, et al. The genome sequence of Atlantic cod reveals a unique immune system. Nature. 2011;477:207-10.
100. Futschik A, Schlötterer C. The next generation of molecular markers from massively parallel sequencing of pooled DNA samples. Genetics. 2010;186:207-18.
101. Arnold B, Corbett-Detig RB, Hartl D, Bomblies K. RADseq underestimates diversity and introduces genealogical biases due to nonrandom haplotype sampling. Mol Ecol. 2013;22:3179-90.
102. Lynch M, Bost D, Wilson S, Maruki T, Harrison S. Population-genetic inference from pooled-sequencing data. Genome Biol Evol. 2014;6:1210-8.
103. Anderson EC, Skaug HJ, Barshis DJ. Next-generation sequencing for molecular ecology: a caveat regarding pooled samples. Mol Ecol. 2014;23:502-12.
104. Kofler R, Orozco-terWengel P, De Maio N, Pandey RV, Nolte V, Futschik A, et al. PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS One. 2011;6:e15925.
105. Fabian DK, Kapun M, Nolte V, Kofler R, Schmidt PS, Schlötterer C, et al. Genome-wide patterns of latitudinal differentiation among populations of Drosophila melanogaster from North America. Mol Ecol. 2012;21:4748-69.
106. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One. 2011;6, e19379.
107. FASTX-Toolkit. http://hannonlab.cshl.edu/fastx_toolkit/index.html .
108. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:1754-60.
109. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. 1000 Genome Project Data Processing Subgroup. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078-9.
110. Kofler R, Pandey RV, Schlötterer C. PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinformatics. 2011;27:3435-6.
111. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, et al. Circos: an information aesthetic for comparative genomics. Genome Res. 2009;19:1639-45.
112. Akey JM, Ruhe AL, Akey DT, Wong AK, Connelly CF, Madeoy J, et al. Tracking footprints of artificial selection in the dog genome. P Natl Acad Sci USA. 2010;107:1160-5.
113. Foll M, Gaggiotti O. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics. 2008;180:977-93.
114. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841-2.
115. Kasprzyk A. BioMart:. driving a paradigm change in biological data management. Database. 2011;2011:bar049.
116. Bluthgen N, Brand K, Cajavec B, Swat M, Herzel H, Beule D, et al. Biological profiling of gene groups utilizing Gene Ontology. Genome Inform. 2005;16:106-15.
117. LabDSV. http://ecology.msu.montana.edu/labdsv/R/ .
118. Latter BD. Selection in finite populations with multiple alleles. 3. Genetic divergence with centripetal selection and mutation. Genetics. 1972;70:475-90.
119. Populations 1.2.32. http://bioinformatics.org/~tryphon/populations/ .
120. Ye J, Fang L, Zheng HK, Zhang Y, Chen J, Zhang ZJ, et al. WEGO: a web tool for plotting GO annotations. Nucleic Acids Res. 2006;34:W293-7.