The genetic basis for ecological adaptation of the Atlantic herring revealed by genome sequencing

eLife

Volumn 5, Issue MAY2016, 2016, Pages

  Barrio, Alvaro Martinez ^a   Lamichhaney, Sangeet ^a   Fan, Guangyi ^b,c   Rafati, Nima ^a   Pettersson, Mats ^a   Zhang, He ^c,d   Dainat, Jacques ^a   Ekman, Diana ^e   Höppner, Marc ^a   Jern, Patric ^a   Martin, Marcel ^e   Nystedt, Björn ^a   Liu, Xin ^c   Chen, Wenbin ^c   Liang, Xinming ^c   Shi, Chengcheng ^c   Fu, Yuanyuan ^c,f   Ma, Kailong ^c   Zhan, Xiao ^c   Feng, Chungang ^a   Gustafson, Ulla ^g   Rubin, Carl Johan ^a   Almén, Markussällman ^a   Blass, Martina ^g   Casini, Michele ^g   Folkvord, Arild ^h,i,j   Laikre, Linda ^e   Ryman, Nils ^e   Lee, Simonming Yuen ^b   Xu, Xun ^c   Andersson, Leif ^a,g,k   more..

^a UPPSALA UNIVERSITY   (Sweden)

^b University of Macau   (Macao)

^c BGI SHENZHEN   (China)

^d QINGDAO UNIVERSITY   (China)

^e STOCKHOLM UNIVERSITY   (Sweden)

^f SOUTHEAST UNIVERSITY   (China)

^g SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^h UNIVERSITY OF BERGEN   (Norway)

ⁱ Uni Research and Hjort Centre for Marine Ecosystem Dynamics   (Norway)

^j INSTITUTE OF MARINE RESEARCH   (Norway)

^k TEXAS A AND M UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ATLANTIC HERRING; ATLANTIC OCEAN; AUTUMN; BALTIC SEA; EVOLUTIONARY ADAPTATION; GENETIC VARIABILITY; GENOME; GEOGRAPHIC ORIGIN; HAPLOTYPE; SPAWNING; SPRING; ADAPTATION; ANIMAL; CLASSIFICATION; FISH; GENETIC VARIATION; GENETICS; GENOMICS; PHYSIOLOGY; POPULATION GENETICS;

SALT WATER; SEA WATER;

ADAPTATION, BIOLOGICAL; ANIMALS; ATLANTIC OCEAN; FISHES; GENETIC VARIATION; GENETICS, POPULATION; GENOMICS; SALINE WATERS; SEAWATER;

EID: 84971642339     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.12081     Document Type: Article

References (99)

1. Amemiya CT, Alföldi J, Lee AP, Fan S, Philippe H, Maccallum I, Braasch I, Manousaki T, Schneider I, Rohner N, Organ C, Chalopin D, Smith JJ, Robinson M, Dorrington RA, Gerdol M, Aken B, Biscotti MA, Barucca M, Baurain D, et al. 2013. The african coelacanth genome provides insights into tetrapod evolution. Nature 496: 311-316. doi: 10.1038/nature12027
2. Andersson L, Ryman N, Rosenberg R, Ståhl G. 1981. Genetic variability in atlantic herring (Clupea harengus harengus): Description of protein loci and population data. Hereditas 95:69-78. doi: 10.1111/j.1601-5223.1981.tb01330.x
3. Andersson L. 2013. Molecular consequences of animal breeding. Current Opinion in Genetics & Development 23:295-301. doi: 10.1016/j.gde.2013.02.014
4. Andrén T, Björck S, Andrén E, Conley D, Zillén L, Anjar J. 2011. The Development of the Baltic Sea Basin During the Last 130 ka. Harff J, Bjorck S, Hoth P (Eds). The Baltic Sea Basin. Berlin, Heidelberg: Springer Berlin Heidelberg. p 75-97. doi: 10.1007/978-3-642-17220-54
5. Aneer G. 1985. Some speculations about the Baltic herring (Clupea harengus membras) in connection with the eutrophication of the Baltic Sea. Canadian Journal of Fisheries and Aquatic Sciences 42:s83-s90. doi: 10.1139/f85-264
6. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. 2000. Gene ontology: Tool for the unification of biology. the gene ontology consortium. Nature Genetics 25:25-29. doi: 10.1038/75556
7. Bates D, Maechler M, Bolker BM, Walker S. 2014. lme4: Linear mixed-effects models using eigen and S4. R package version. Available at http://arxiv.org/abs/1406.5823.
8. Bondesson M, Hao R, Lin CY, Williams C, Gustafsson JÅ. 2015. Estrogen receptor signaling during vertebrate development. Biochimica Et Biophysica Acta 1849:142-151. doi: 10.1016/j.bbagrm.2014.06.005
9. Bornestaf C, Antonopoulou E, Mayer I, Borg B. 1997. Effects of aromatase inhibitors on reproduction in male three-spined sticklebacks, gasterosteus aculeatus, exposed to long and short photoperiods. Fish Physiology and Biochemistry 16:419-423. doi: 10.1023/A:1007776517447
10. Browning SR, Browning BL. 2007. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. American Journal of Human Genetics 81: 1084-1097. doi: 10.1086/521987
11. Burridge CP, Craw D, Fletcher D, Waters JM. 2008. Geological dates and molecular rates: Fish DNA sheds light on time dependency. Molecular Biology and Evolution 25:624-633. doi: 10.1093/molbev/msm271
12. Cai W, Rambaud J, Teboul M, Masse I, Benoit G, Gustafsson JA, Delaunay F, Laudet V, Pongratz I. 2008. Expression levels of estrogen receptor beta are modulated by components of the molecular clock. Molecular and Cellular Biology 28:784-793. doi: 10.1128/MCB.00233-07
13. Cantarel BL, Korf I, Robb SM, Parra G, Ross E, Moore B, Holt C, Sánchez Alvarado A, Yandell M. 2008. MAKER: An easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Research 18: 188-196. doi: 10.1101/gr.6743907
14. Carneiro M, Rubin CJ, Di Palma F, Albert FW, Alföldi J, Barrio AM, Pielberg G, Rafati N, Sayyab S, Turner-Maier J, Younis S, Afonso S, Aken B, Alves JM, Barrell D, Bolet G, Boucher S, Burbano HA, Campos R, Chang JL, et al. 2014. Rabbit genome analysis reveals a polygenic basis for phenotypic change during domestication. Science 345:1074-1079. doi: 10.1126/science.1253714
15. 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. Genetical Research 70:155-174. doi: 10.1017/S0016672397002954
16. Chen K, Wallis JW, McLellan MD, Larson DE, Kalicki JM, Pohl CS, McGrath SD, Wendl MC, Zhang Q, Locke DP, Shi X, Fulton RS, Ley TJ, Wilson RK, Ding L, Mardis ER. 2009. BreakDancer: An algorithm for high-resolution mapping of genomic structural variation. Nature Methods 6:677-681. doi: 10.1038/nmeth.1363
17. Cimino MC, Bahr GF. 1974. The nuclear DNA content and chromatin ultrastructure of the coelacanth Latimeria chalumnae. Experimental Cell Research 88:263-272. doi: 10.1016/0014-4827(74)90240-7
18. Cingolani P, Platts A, Wang le L, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM. 2012. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: Snps in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6:80-92. doi: 10.4161/fly.19695
19. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R, 1000 Genomes Project Analysis Group. 2011. The variant call format and vcftools. Bioinformatics 27:2156-2158. doi: 10.1093/bioinformatics/btr330
20. Dickey-Collas M, Nash RDM, Brunel T, van Damme CJG, Marshall CT, Payne MR, Corten A, Geffen AJ, Peck MA, Hatfield EMC, Hintzen NT, Enberg K, Kell LT, Simmonds EJ. 2010. Lessons learned from stock collapse and recovery of North Sea herring: A review. ICES Journal of Marine Science 67:1875-1886. doi: 10.1093/icesjms/fsq033
21. Dolezel J, Bartos J, Voglmayr H, Greilhuber J. 2003. Letter to the editor. Cytometry Part A,51A. 127-128.
22. Edwards M, Richardson AJ. 2004. Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881-884. doi: 10.1038/nature02808
23. Ewing G, Hermisson J. 2010. Msms: A coalescent simulation program including recombination, demographic structure and selection at a single locus. Bioinformatics 26:2064-2065. doi: 10.1093/bioinformatics/btq322
24. FAO. 2014. Yearbook Fishery and Aquaculture Statistics. Rome: Fao.
25. Felsenstein J. 1989. Phylip -phylogeny inference package (version 3.2). Cladistics 5:164-166.
26. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M. 2014. Pfam: The protein families database. Nucleic Acids Research 42:D222-D230. doi: 10.1093/nar/gkt1223
27. Freeman JL, Adeniyi A, Banerjee R, Dallaire S, Maguire SF, Chi J, Ng BL, Zepeda C, Scott CE, Humphray S, Rogers J, Zhou Y, Zon LI, Carter NP, Yang F, Lee C. 2007. Definition of the zebrafish genome using flow cytometry and cytogenetic mapping. BMC Genomics 8. doi: 10.1186/1471-2164-8-195
28. Glasauer SM, Neuhauss SC. 2014. Whole-genome duplication in teleost fishes and its evolutionary consequences. Molecular Genetics and Genomics: MGG 289:1045-1060. doi: 10.1007/s00438-014-0889-2
29. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29:644-652. doi: 10.1038/nbt.1883
30. Günther T, Coop G. 2013. Robust identification of local adaptation from allele frequencies. Genetics 195:205-220. doi: 10.1534/genetics.113.152462
31. Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith RK, Hannick LI, Maiti R, Ronning CM, Rusch DB, Town CD, Salzberg SL, White O. 2003. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Research 31:5654-5666. doi: 10.1093/nar/gkg770
32. Hall B, Derego T, Geib S. 2014. Gag: The genome annotation generator [online]. available. http://genomeannotation.github.io/Gag.
33. Hanon EA, Lincoln GA, Fustin JM, Dardente H, Masson-Pévet M, Morgan PJ, Hazlerigg DG. 2008. Ancestral TSH mechanism signals summer in a photoperiodic mammal. Current Biology: CB 18:1147-1152. doi: 10.1016/j.cub.2008.06.076
34. Hay DE, McCarter PB, Daniel KS, Schweigert JF. 2009. Spatial diversity of Pacific herring (Clupea pallasi) spawning areas. ICES Journal of Marine Science 66:1662-1666. doi: 10.1093/icesjms/fsp139
35. Hayward A, Cornwallis CK, Jern P. 2015. Pan-vertebrate comparative genomics unmasks retrovirus macroevolution. Proceedings of the National Academy of Sciences of the United States of America 112:464-469. doi: 10.1073/pnas.1414980112
36. Hinegardner R, Rosen DE. 1972. Cellular DNA content and the evolution of teleostean fishes. American Naturalist 106:621-644. doi: 10.1086/282801
37. Holt C, Yandell M. 2011. Maker2: An annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinformatics 12. doi: 10.1186/1471-2105-12-491
38. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collins JE, Humphray S, McLaren K, Matthews L, McLaren S, Sealy I, Caccamo M, Churcher C, Scott C, Barrett JC, Koch R, Rauch GJ, White S, Chow W, et al. 2013. The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498-503. doi: 10.1038/nature12111
39. Hunter S, Jones P, Mitchell A, Apweiler R, Attwood TK, Bateman A, Bernard T, Binns D, Bork P, Burge S, de Castro E, Coggill P, Corbett M, Das U, Daugherty L, Duquenne L, Finn RD, Fraser M, Gough J, Haft D, et al. 2012. InterPro in 2011: New developments in the family and domain prediction database. Nucleic Acids Research 40:D306-D312. doi: 10.1093/nar/gkr948
40. ICES. 2014. Report of the Baltic Fisheries Assessment Working Group (WGBFAS). 3-10 April 2014 ICES HQ, Copenhagen, Denmark ICES CM 2014/ACOM:10 919.
41. Ida H, Oka N, Hayashigaki K. 1991. Karyotypes and cellular DNA contents of three species of the subfamily Clupeinae. Japanese Journal of Ichthyology 38:289-294.
42. Iles TD, Sinclair M. 1982. Atlantic herring: Stock discreteness and abundance. Science 215:627-633. doi: 10.1126/science.215.4533.627
43. Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, Johnson J, Swofford R, Pirun M, Zody MC, White S, Birney E, Searle S, Schmutz J, Grimwood J, Dickson MC, Myers RM, Miller CT, Summers BR, Knecht AK, Brady SD, et al. 2012. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55-61. doi: 10.1038/nature10944
44. Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong SY, Lopez R, Hunter S. 2014. InterProScan 5: Genome-scale protein function classification. Bioinformatics 30:1236-1240. doi: 10.1093/bioinformatics/btu031
45. Karasov T, Messer PW, Petrov DA. 2010. Evidence that adaptation in Drosophila is not limited by mutation at single sites. PLoS Genetics 6:e1000924. doi: 10.1371/journal.pgen.1000924
46. Kawaguchi M, Yasumasu S, Shimizu A, Kudo N, Sano K, Iuchi I, Nishida M. 2013. Adaptive evolution of fish hatching enzyme: One amino acid substitution results in differential salt dependency of the enzyme. Journal of Experimental Biology 216:1609-1615. doi: 10.1242/jeb.069716
47. Kijas JW, Lenstra JA, Hayes B, Boitard S, Porto Neto LR, San Cristobal M, Servin B, McCulloch R, Whan V, Gietzen K, Paiva S, Barendse W, Ciani E, Raadsma H, McEwan J, Dalrymple B, International Sheep Genomics Consortium Members. 2012. Genome-wide analysis of the world’s sheep breeds reveals high levels of historic mixture and strong recent selection. PLoS Biology 10:e1001258. doi: 10.1371/journal.pbio.1001258
48. Kim HD, Choe HK, Chung S, Kim M, Seong JY, Son GH, Kim K. 2011. Class-C SOX transcription factors control gnrh gene expression via the intronic transcriptional enhancer. Molecular Endocrinology 25:1184-1196. doi: 10.1210/me.2010-0332
49. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013. TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology 14:R36. doi: 10.1186/gb-2013-14-4-r36
50. King MC, Wilson AC. 1975. Evolution at two levels in humans and chimpanzees. Science 188:107-116. doi: 10.1126/science.1090005
51. Kuleshov V, Xie D, Chen R, Pushkarev D, Ma Z, Blauwkamp T, Kertesz M, Snyder M. 2014. Whole-genome haplotyping using long reads and statistical methods. Nature Biotechnology 32:261-266. doi: 10.1038/nbt.2833
52. Lamichhaney S, Martinez Barrio A, Rafati N, Sundström G, Rubin CJ, Gilbert ER, Berglund J, Wetterbom A, Laikre L, Webster MT, Grabherr M, Ryman N, Andersson L. 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 109:19345-19350. doi: 10.1073/pnas.1216128109
53. Lamichhaney S, Berglund J, Almén MS, Maqbool K, Grabherr M, Martinez-Barrio A, Promerová M, Rubin CJ, Wang C, Zamani N, Grant BR, Grant PR, Webster MT, Andersson L. 2015. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518:371-375. doi: 10.1038/nature14181
54. Lander ES, Waterman MS. 1988. Genomic mapping by fingerprinting random clones: A mathematical analysis. Genomics 2:231-239. doi: 10.1016/0888-7543(88)90007-9
55. Larsson LC, Laikre L, Palm S, André C, Carvalho GR, Ryman N. 2007. Concordance of allozyme and microsatellite differentiation in a marine fish, but evidence of selection at a microsatellite locus. Molecular Ecology 16:1135-1147. doi: 10.1111/j.1365-294X.2006.03217.x
56. Larsson LC, Laikre L, André C, Dahlgren TG, Ryman N. 2010. Temporally stable genetic structure of heavily exploited Atlantic herring (Clupea harengus) in swedish waters. Heredity 104:40-51. doi: 10.1038/hdy.2009.98
57. Li L, Stoeckert CJ, Roos DS. 2003. OrthoMCL: Identification of ortholog groups for eukaryotic genomes. Genome Research 13:2178-2189. doi: 10.1101/gr.1224503
58. Li H, Durbin R. 2009. Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25: 1754-1760. doi: 10.1093/bioinformatics/btp324
59. Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, Li S, Yang H, Wang J, Wang J. 2010. De novo assembly of human genomes with massively parallel short read sequencing. Genome Research 20: 265-272. doi: 10.1101/gr.097261.109
60. Limborg MT, Helyar SJ, De Bruyn M, Taylor MI, Nielsen EE, Ogden R, Carvalho GR, Bekkevold D, FPT Consortium. Environmental selection on transcriptome-derived snps in a high gene flow marine fish, the Atlantic herring (Clupea harengus). Molecular Ecology 21:3686-3703. doi: 10.1111/j.1365-294X.2012.05639.x
61. Linnaeus C. 1761. Fauna Suecica. Stockholm.
62. Lowe TM, Eddy SR. 1997. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research 25:955-964. doi: 10.1093/nar/25.5.0955
63. Magrane M, Consortium U. 2011. Uniprot knowledgebase: A hub of integrated protein data. Database 2011. doi: 10.1093/database/bar009
64. Manzon LA. 2002. The role of prolactin in fish osmoregulation: A review. General and Comparative Endocrinology 125:291-310. doi: 10.1006/gcen.2001.7746
65. Marco-Sola S, Sammeth M, Guigó R, Ribeca P. 2012. The GEM mapper: Fast, accurate and versatile alignment by filtration. Nature Methods 9:1185-1188. doi: 10.1038/nmeth.2221
66. Smith JM, Haigh J. 1974. The hitch-hiking effect of a favourable gene. Genetical Research 23:23-35. doi: 10.1017/s0016672300014634
67. McCoy RC, Taylor RW, Blauwkamp TA, Kelley JL, Kertesz M, Pushkarev D, Petrov DA, Fiston-Lavier AS. 2014. Illumina truseq synthetic long-reads empower de novo assembly and resolve complex, highly-repetitive transposable elements. PLoS One 9:e106689. doi: 10.1371/journal.pone.0106689
68. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA. 2010. The genome analysis toolkit: A mapreduce framework for analyzing next-generation DNA sequencing data. Genome Research 20:1297-1303. doi: 10.1101/gr.107524.110
69. McQuinn I. 1997. Metapopulations and the Atlantic herring. Reviews in Fish Biology and Fisheries 7:297-329. doi: 10.1023/A:1018491828875
70. Melamed P, Savulescu D, Lim S, Wijeweera A, Luo Z, Luo M, Pnueli L. 2012. Gonadotrophin-releasing hormone signalling downstream of calmodulin. Journal of Neuroendocrinology 24:1463-1475. doi: 10.1111/j.1365-2826.2012.02359.x
71. Meuwissen T, Hayes B, Goddard M. 2013. Accelerating improvement of livestock with genomic selection. Annual Review of Animal Biosciences 1:221-237. doi: 10.1146/annurev-animal-031412-103705
72. Nakane Y, Ikegami K, Iigo M, Ono H, Takeda K, Takahashi D, Uesaka M, Kimijima M, Hashimoto R, Arai N, Suga T, Kosuge K, Abe T, Maeda R, Senga T, Amiya N, Azuma T, Amano M, Abe H, Yamamoto N, et al. 2013. The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nature Communications 4. doi: 10.1038/ncomms3108
73. Nakao N, Ono H, Yamamura T, Anraku T, Takagi T, Higashi K, Yasuo S, Katou Y, Kageyama S, Uno Y, Kasukawa T, Iigo M, Sharp PJ, Iwasawa A, Suzuki Y, Sugano S, Niimi T, Mizutani M, Namikawa T, Ebihara S, et al. 2008. Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature 452:317-322. doi: 10.1038/nature06738
74. Near TJ, Eytan RI, Dornburg A, Kuhn KL, Moore JA, Davis MP, Wainwright PC, Friedman M, Smith WL. 2012. Resolution of ray-finned fish phylogeny and timing of diversification. Proceedings of the National Academy of Sciences of the United States of America 109:13698-13703. doi: 10.1073/pnas.1206625109
75. Ohno S, Muramoto J, Klein J, Atkin NB. 1969. Diploid-tetraploid relationship in clupeoid and salmonoid fish. Darlington CD, Lewis KR (Eds). Chromosomes Today. Edinburgh: Oliver & Boyd.
76. Ono H, Hoshino Y, Yasuo S, Watanabe M, Nakane Y, Murai A, Ebihara S, Korf HW, Yoshimura T. 2008. Involvement of thyrotropin in photoperiodic signal transduction in mice. Proceedings of the National Academy of Sciences of the United States of America 105:18238-18242. doi: 10.1073/pnas.0808952105
77. Parra G, Bradnam K, Korf I. 2007. Cegma: A pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23:1061-1067. doi: 10.1093/bioinformatics/btm071
78. Parra G, Bradnam K, Ning Z, Keane T, Korf I. 2009. Assessing the gene space in draft genomes. Nucleic Acids Research 37:289-297. doi: 10.1093/nar/gkn916
79. Pedersen BS, Schwartz DA, Yang IV, Kechris KJ. 2012. Comb-p: Software for combining, analyzing, grouping and correcting spatially correlated p-values. Bioinformatics 28:2986-2988. doi: 10.1093/bioinformatics/bts545
80. Price MN, Dehal PS, Arkin AP. 2010. Fasttree 2-approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490. doi: 10.1371/journal.pone.0009490
81. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC. 2007. Plink: A tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics 81:559-575. doi: 10.1086/519795
82. Rausch T, Zichner T, Schlattl A, Stutz AM, Benes V, Korbel JO. 2012. Delly: Structural variant discovery by integrated paired-end and split-read analysis. Bioinformatics 28:i333-i339. doi: 10.1093/bioinformatics/bts378
83. Rubin CJ, Zody MC, Eriksson J, Meadows JR, Sherwood E, Webster MT, Jiang L, Ingman M, Sharpe T, Ka S, Hallböök F, Besnier F, Carlborg O, Bed’hom B, Tixier-Boichard M, Jensen P, Siegel P, Lindblad-Toh K, Andersson L. 2010. Whole-genome resequencing reveals loci under selection during chicken domestication. Nature 464:587-591. doi: 10.1038/nature08832
84. Ryman N, Lagercrantz U, Andersson L, Chakraborty R, Rosenberg R. 1984. Lack of correspondence between genetic and morphologic variability patterns in Atlantic herring (Clupea harengus). Heredity 53:687-704. doi: 10.1038/hdy.1984.127
85. Schennink A, Trott JF, Manjarin R, Lemay DG, Freking BA, Hovey RC. 2015. Comparative genomics reveals tissue-specific regulation of prolactin receptor gene expression. Journal of Molecular Endocrinology 54:1-15. doi: 10.1530/JME-14-0212
86. Sheehan S, Harris K, Song YS. 2013. Estimating variable effective population sizes from multiple genomes: A sequentially Markov conditional sampling distribution approach. Genetics 194:647-662. doi: 10.1534/genetics.112.149096
87. Smit A, Hubley R. 2010. Repeatmodeler open-1.0 [online]. Available at. http://www.repeatmasker.org/RepeatModeler.html.
88. Smit AFA, Hubley R, Green P. 2015. Repeatmasker [online]. Available at. http://repeatmasker.org.
89. Sperber GO, Airola T, Jern P, Blomberg J. 2007. Automated recognition of retroviral sequences in genomic data-retrotector. Nucleic Acids Research 35:4964-4976. doi: 10.1093/nar/gkm515
90. Stanke M, Diekhans M, Baertsch R, Haussler D. 2008. Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24:637-644. doi: 10.1093/bioinformatics/btn013
91. Star B, Nederbragt AJ, Jentoft S, Grimholt U, Malmstrøm M, Gregers TF, Rounge TB, Paulsen J, Solbakken MH, Sharma A, Wetten OF, Lanzén A, Winer R, Knight J, Vogel JH, Aken B, Andersen O, Lagesen K, Tooming-Klunderud A, Edvardsen RB, et al. 2011. The genome sequence of Atlantic cod reveals a unique immune system. Nature 477:207-210. doi: 10.1038/nature10342
92. Tate R, Hall B, Derego T, Geib S. 2014. Annie: The annotation information extractor [online]. Available at. http://genomeannotation.github.io/Annie.
93. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 28:511-515. doi: 10.1038/nbt.1621
94. Vinogradov AE. 1998. Genome size and gc-percent in vertebrates as determined by flow cytometry: The triangular relationship. Cytometry 31:100-109. doi: 10.1002/(SICI)1097-0320(19980201)31:2<100::AID-CYTO5>3.0.CO;2-Q
95. Visser ME, Gienapp P, Husby A, Morrisey M, de la Hera I, Pulido F, Both C. 2015. Effects of spring temperatures on the strength of selection on timing of reproduction in a long-distance migratory bird. PLoS Biology 13: e1002120. doi: 10.1371/journal.pbio.1002120
96. Voskoboynik A, Neff NF, Sahoo D, Newman AM, Pushkarev D, Koh W, Passarelli B, Fan HC, Mantalas GL, Palmeri KJ, Ishizuka KJ, Gissi C, Griggio F, Ben-Shlomo R, Corey DM, Penland L, White RA, Weissman IL, Quake SR. 2013. The genome sequence of the colonial chordate, Botryllus schlosseri. eLife 2:e00569. doi: 10.7554/eLife.00569
97. Wang G, Yang E, Smith KJ, Zeng Y, Ji G, Connon R, Fangue NA, Cai JJ. 2014. Gene expression responses of threespine stickleback to salinity: Implications for salt-sensitive hypertension. Frontiers in Genetics 5:312. doi: 10.3389/fgene.2014.00312
98. Wood AR, Esko T, Yang J, Vedantam S, Pers TH, Gustafsson S, Chu AY, Estrada K, Luan J, Kutalik Z, Amin N, Buchkovich ML, Croteau-Chonka DC, Day FR, Duan Y, Fall T, Fehrmann R, Ferreira T, Jackson AU, Karjalainen J, et al. 2014. Defining the role of common variation in the genomic and biological architecture of adult human height. Nature Genetics 46:1173-1186. doi: 10.1038/ng.3097
99. Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Jackson JB, Lotze HK, Micheli F, Palumbi SR, Sala E, Selkoe KA, Stachowicz JJ, Watson R. 2006. Impacts of biodiversity loss on ocean ecosystem services. Science 314:787-790. doi: 10.1126/science.1132294