Genome-wide single-generation signatures of local selection in the panmictic European eel

Molecular Ecology

Volumn 23, Issue 10, 2014, Pages 2514-2528

  Pujolar, J M ^a   Jacobsen, M W ^a   Als, T D ^a,b   Frydenberg, J ^a   Munch, K ^a   Jonsson B ^c   Jian, J B ^d   Cheng, L ^d   Maes, G E ^e,f   Bernatchez, L ^g   Hansen, M M ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c Biopol Marine Biology and Biotechnology Center   (Iceland)

^d BGI SHENZHEN   (China)

^e UNIVERSITY OF LEUVEN   (Belgium)

^f JAMES COOK UNIVERSITY   (Australia)

^g UNIVERSITÉ LAVAL   (Canada)

Author keywords

anguilla; local adaptation; panmixia; spatially varying selection

Indexed keywords

MITOCHONDRIAL DNA;

ANGUILLA; ANGUILLA (FISH); ANIMAL; ARTICLE; DNA SEQUENCE; EUROPE; GENE FLOW; GENE FREQUENCY; GENETIC SELECTION; GENETICS; LOCAL ADAPTATION; MOLECULAR EVOLUTION; PANMIXIA; POPULATION GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM; SPATIALLY VARYING SELECTION;

ANGUILLA; LOCAL ADAPTATION; PANMIXIA; SPATIALLY VARYING SELECTION;

ANGUILLA; ANIMALS; DNA, MITOCHONDRIAL; EUROPE; EVOLUTION, MOLECULAR; GENE FLOW; GENE FREQUENCY; GENETICS, POPULATION; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA;

EID: 84900828213     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12753     Document Type: Article

References (76)

1. Albert V, Jõnsson B, Bernatchez L, (2006) Natural hybrids in Atlantic eels (Anguilla anguilla, A. rostrata): evidence for successful reproduction and fluctuating abundance in space and time. Molecular Ecology, 15, 1903-1916.
2. Als TD, Hansen MM, Maes GE, et al,. (2011) All roads lead to home: panmixia of European eel in the Sargasso Sea. Molecular Ecology, 20, 1333-1346.
3. Andrello M, Bevacqua D, Maes GE, De Leo GA, (2011) An integrated genetic-demographic model to unravel the origin and genetic structure in European eel (Anguilla anguilla). Evolutionary Applications, 4, 517-533.
4. ST-outlier method. BMC Bioinformatics, 9, 323.
5. Avise JC, Nelson WS, Arnold J, Koehn RJ, Williams GC, Thorsteinsson V, (1990) The evolutionary status of Iceland eels. Evolution, 44, 1254-1262.
6. Baird NA, Etter PD, Atwood TS, et al,. (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE, 3, e3376.
7. Baltazar-Soares M, Biastoch A, Harrod C, et al,. (2014) Recruitment collapse and population structure of the European eel shaped by local ocean current dynamics. Current Biology, 24, 1-5.
8. Beaumont MA, Nichols RA, (1996) Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society B-Biological Sciences, 263, 1619-1626.
9. Berridge MJ, Lipp P, Bootman MD, (2000) The versatility and universality of calcium signalling. Nature Reviews Molecular Cell Biology, 1, 11-21.
10. Bourret V, Dionne M, Kent MP, Lien S, Bernatchez L, (2013) Landscape genomics in Atlantic salmon (Salmo salar): searching for gene-environment interactions driving local adaptation. Evolution, 67, 3469-3487.
11. 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.
12. Catchen JM, Hohenlohe PA, Bassham S, Amores A, Cresko WA, (2013) Stacks: an analysis tool set for population genomics. Molecular Ecology, 22, 3124-3140.
13. Coop G, Witonsky D, Di Rienzo A, Pritchard JK, (2010) Using environmental correlations to identify loci underlying local adaptation. Genetics, 185, 411-1423.
14. ST = 0 and North Atlantic Oscillation effects on demographic fluctuations of a panmictic species. Molecular Ecology, 22, 1763-1776.
15. Coyne JA, Orr HA, (2004) Speciation. Sinauer Associates, Sunderland, Massachusetts.
16. Dannewitz J, Maes GE, Johansson L, Wickström H, Volckaert FAM, Jarvi T, (2005) Panmixia in the European eel: a matter of time. Proceedings of the Royal Society B-Biological Sciences, 272, 1129-1137.
17. Daverat F, Limburg K, Thibaut I, et al,. (2006) Phenotypic plasticity of habitat use by three temperate eel species Anguilla anguilla, A. japonica and A. rostrata. Marine Ecology Progress Series, 308, 231-241.
18. Davey JW, Hohenlohe PA, Etter PD, et al,. (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nature Reviews Genetics, 12, 499-510.
19. Ellison CE, Hall C, Kowbel D, et al,. (2011) Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proceedings of the National Academy of Science of the USA, 108, 2831-2836.
20. Etter PD, Preston JL, Bassham S, Cresko WA, Johnson EA, (2011) Local de novo assembly of RAD paired-end contigs using short sequencing reads. PLoS ONE, 6, e18561.
21. 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.
22. Feder JL, Nosil P, (2010) The efficacy of divergence hitchhiking in generating genomic islands during ecological speciation. Evolution, 64, 1729-1747.
23. Feder JL, Egan SP, Nosil P, (2012) The genomics of speciation-with-gene- flow. Trends in Genetics, 28, 342-350.
24. 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.
25. Fraser DJ, Weir LK, Bernatchez L, Hansen MM, Taylor EB, (2011) Extend and scale of local adaptation in salmonid fishes: review and meta-analysis. Heredity, 106, 404-420.
26. Friedland KD, Miller MJ, Knights B, (2007) Oceanic changes in the Sargasso Sea and declines in recruitment of the European eel. ICES Journal of Marine Science, 64, 519-530.
27. Gagnaire PA, Normandeau E, Côté C, Hansen MM, Bernatchez L, (2012a) The genetic consequences of spatially varying selection in the panmictic American eel (Anguilla rostrata). Genetics, 190, 725-736.
28. Gagnaire PA, Normandeau E, Bernatchez L, (2012b) Comparative genomics reveals adaptive protein evolution and a possible cytonuclear incompatibility between European and American eels. Molecular Biology and Evolution, 29, 2909-2919.
29. Gagnaire PA, Pavey SA, Normandeau E, Bernatchez L, (2013) The genetic architecture of reproductive isolation during speciation-with-gene-flow in lake whitefish species pairs assessed by RAD sequencing. Evolution, 67, 2483-2497.
30. Götz S, Garcia-Gomez JM, Terol J, et al,. (2008) High throughput functional annotation and data mining with the Blast2Go suite. Nucleic Acids Research, 36, 3420-3435.
31. Hancock AM, Witonsky DB, Ehler E, et al,. (2010) Colloquium paper: human adaptations to diet, subsistence, and ecoregion are due to subtle shifts in allele frequency. Proceedings of the National Academy of Sciences of the USA, 107, 8924-8930.
32. Hastings JW, Rusak B, Boulos Z, (1991) Circadian rhythms: the physiology of biological timing. In: Neural and Integrative Animal Physiology (ed, Prosser CL,), pp. 435-546. Wiley-Liss, New York.
33. Hedrick PW, (2006) Genetic polymorphism in heterogeneous environments: the age of genomics. Annual Review of Ecology Evolution and Systematics, 37, 67-93.
34. Hemmer-Hansen J, Nielsen EE, Therkildsen NJ, et al,. (2013) A genomic island linked to ecotype divergence in Atlantic cod. Molecular Ecology, 22, 2653-2667.
35. Henkel CV, Burgerhout E, Danielle L, et al,. (2012) Primitive duplicate hox clusters in the European eel's genome. PLoS ONE, 7, e32231.
36. Hoffer T, Foll M, Excoffier L, (2012) Evolutionary forces shaping genomic islands of population differentiation in humans. BMC Genomics, 13, 107.
37. Hoffmann AA, Willi Y, (2008) Detecting genetic responses to environmental change. Nature Reviews Genetics, 9, 421-432.
38. Hohenlohe PA, Basshan 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.
39. 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.
40. Jones FC, Grabherr MG, Chan YF, et al,. (2012b) The genomic basis of adaptive evolution in threespine sticklebacks. Nature, 484, 55-61.
41. Kawecki TJ, Ebert D, (2004) Conceptual issues in local adaptation. Ecology Letters, 7, 1225-1241.
42. Keller SR, Levsen N, Olson MS, Tiffin P, (2012) Local adaptation in the flowering-time gene network of balsam poplar, Populus balsamifera. Molecular Biology and Evolution, 29, 3143-3152.
43. Kettle A, Haines K, (2006) How does the European eel (Anguilla anguilla) retain its population structure during its larval migration across the Atlantic Ocean? Canadian Journal of Fisheries and Aquatic Sciences, 63, 90-106.
44. Koehn RK, Williams GC, (1978) Genetic differentiation without isolation in American eel, Anguilla rostrata. 2. Temporal stability of geographic patterns. Evolution, 32, 624-637.
45. Koehn RK, Milkman R, Mitton JB, (1976) Population genetics of marine pelecypods. IV. selection, migration, and genetic differentiation in the blue mussel Mytilus edulis. Evolution, 30, 2-30.
46. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology, 10, R25.
47. Lecomte-Finiger R, (1994) The early life of the European eel. Nature, 370, 424.
48. Lemaire C, Allegrucci G, Naciri M, Bahri-Sfar L, Kara H, Bonhomme F, (2000) Do discrepancies between microsatellite and allozyme variation reveal differential selection between sea and lagoon in the sea bass (Dicentrarchus labrax). Molecular Ecology, 9, 457-467.
49. Levene H, (1953) Genetic equilibrium when more than one ecological niche is available. American Naturalist, 87, 331-333.
50. Ma XF, Hall D, Onge KR, Jansson S, Ingvarsson PK, (2010) Genetic differentiation, clinal variation and phenotypic associations with growth cessation across the Populus tremula photoperiodic pathway. Genetics, 186, 1033-1044.
51. Maes GE, Volckaert FAM, (2002) Clinal genetic variation and isolation by distance in the European eel Anguilla anguilla. Biological Journal of the Linnean Society, 77, 509-522.
52. Maes GE, Pujolar JM, Hellemans B, Volckaert FAM, (2006) Evidence for isolation by time in the European eel (Anguilla anguilla). Molecular Ecology, 15, 2095-2107.
53. Mantel N, (1967) The detection of disease clustering and generalised regression approach. Cancer Research, 27, 209-220.
54. McCleave JD, (1993) Physical and behavioral controls on the oceanic distribution and migration of leptocephali. Journal of Fish Biology, 43, 243-273.
55. Munk P, Hansen MM, Maes GE, et al,. (2010) Oceanic fronts in the Sargasso Sea control the early life and drift of Atlantic eels. Proceedings of the Royal Society B-Biological Sciences, 277, 3593-3599.
56. Nacci DE, Champlin D, Jayaraman S, (2010) Adaptation of the estuarine fish Fundulus heteroclitus (Atlantic killifish) to polychlorinated biphenyls (PCBs). Estuaries and Coasts, 33, 853-864.
57. Nadeau NJ, Whible A, Jones RT, et al,. (2012) Genomic islands of divergence in hybridizing Heliconius butterflies identified by large scale targeted sequencing. Philosophical Transactions of the Royal Society B-Biological Sciences, 367, 343-353.
58. Nielsen R, (2005) Molecular signatures of natural selection. Annual Review of Genetics, 39, 197-218.
59. Nosil P, Egan SP, Funk DJ, (2008) Heterogenous genomic differentiation between walking-stick ecotypes: "isolation by adaptation" and multiple roles for divergent selection. Evolution, 62, 316-336.
60. Pritchard JK, Stephens M, Donelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
61. Pujolar JM, Maes GE, Volckaert FAM, (2007) Genetic and morphometric heterogeneity among recruits of the European eel Anguilla anguilla. Bulletin of Marine Science, 81, 297-308.
62. Pujolar JM, Jacobsen MW, Frydenberg J, et al,. (2013) A resource of genome-wide single-nucleotide polymorphisms by RAD tag sequencing in the critically endangered European eel. Molecular Ecology Resources, 13, 706-714.
63. Pujolar JM, Jacobsen MW, Als TD, et al,. (2014) Assessing patterns of hybridization between North Atlantic eels using diagnostic single nucleotide polymorphisms. Heredity. in press.
64. Radwan J, Babik W, (2012) The genomics of adaptation. Proceedings of the Royal Society B-Biological Sciences, 279, 5024-5028.
65. Raymond M, Rousset F, (1995) GENEPOP (version 1.2): a population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248-249.
66. Rice WR, (1989) Analyzing tables and statistical tests. Evolution, 43, 223-225.
67. Scaglione S, Acquadro A, Portis E, Tirone M, Knapp SJ, Lanteri S, (2012) RAD tag sequencing as a source of SNP markers in Cynara cardunculus. BMC Genomics, 13, 3.
68. Stapley J, Reger J, Feulner PGD, et al,. (2010) Adaptation genomics: the next generation. Trends in Ecology and Evolution, 25, 705-712.
69. Van Bers NEM, Van Oers K, Kerstens HHD, (2010) Genome-wide SNP detection in the great tit Parus major using high throughput sequencing. Molecular Ecology, 19, 89-99.
70. Van den Thillart G, Rankin JC, Dufour S, (2009) Spawning Migration of the European Eel: Reproduction Index, a Useful Tool for Conservation Management. Springer, Dordecht, The Netherlands.
71. Véliz D, Bourget E, Bernatchez L, (2004) Regional variation in the spatial scale of selection at MPI* and GPI* in the acorn barnacle Semibalanus balanoides (Crustacea). Journal of Evolutionary Biology, 17, 953-966.
72. Wagner CE, Keller I, Wittwer S, et al,. (2012) Genome-wide RAD sequence data provide unprecedented resolution in species boundaries and relationships in the Lake Victoria cichlid adaptive radiation. Molecular Ecology, 22, 787-798.
73. Whitehead A, Galvez F, Zhang S, Williams LM, Oleksiak MF, (2011) Functional genomics of phenotypic plasticity and local adaptation in killifish. Journal of Heredity, 102, 499-511.
74. Wirth T, Bernatchez L, (2001) Genetic evidence against panmixia in the European eel. Nature, 409, 1037-1040.
75. Yeaman S, Otto SP, (2011) Establishment and maintenance of adaptive genetic divergence under migration, selection and drift. Evolution, 65, 2123-2129.
76. Yeaman S, Whitlock MC, (2011) The genetic architecture of adaptation under migration-selection balance. Evolution, 65, 1897-1911.