The Locus Controls Age at Maturity in Wild and Domesticated Atlantic Salmon ( L.) Males

English version České info

For most species the factors that contribute to the genetic predisposition for age at maturity are currently unknown. In salmon aquaculture early maturation is negative for the growth, disease resistance and flesh quality. In addition, using populations of salmon selected to mature late may limit the genetic impact of aquaculture escapees, as these late maturing fish are more likely to die before they reach maturity. The aim of this study was to elucidate the genetic predisposition for salmon maturation. We determined the sequences of genomes from Atlantic salmon maturing early and late in six Norwegian rivers. This methodology enabled us to identify a short genomic region involved in determining the age at maturity in male Atlantic salmon. This region has also previously been linked to time of puberty in humans–supporting a general mechanism behind age at maturity in vertebrates. The results of this study may be used to breed salmon that are genetically predisposed to mature late which will improve welfare and production in aquaculture industry and aid in the management of escaped farmed salmon.

Vyšlo v časopise: The Locus Controls Age at Maturity in Wild and Domesticated Atlantic Salmon ( L.) Males. PLoS Genet 11(11): e32767. doi:10.1371/journal.pgen.1005628
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005628

Souhrn

Zdroje

1. Taranger GL, Carrillo M, Schulz RW, Fontaine P, Zanuy S, et al. (2010) Control of puberty in farmed fish. Gen Comp Endocrinol 165: 483–515. doi: 10.1016/j.ygcen.2009.05.004 19442666

2. Glover KA, Quintela M, Wennevik V, Besnier F, Sorvik AGE, et al. (2012) Three Decades of Farmed Escapees in the Wild: A Spatio-Temporal Analysis of Atlantic Salmon Population Genetic Structure throughout Norway. Plos One 7.

3. Glover KA, Pertoldi C, Besnier F, Wennevik V, Kent M, et al. (2013) Atlantic salmon populations invaded by farmed escapees: quantifying genetic introgression with a Bayesian approach and SNPs. BMC Genetics 14.

4. Olsen RE, Skilbrei OT (2010) Feeding preference of recaptured Atlantic salmon Salmo salar following simulated escape from fish pens during autumn. Aquaculture Environment Interactions 1: 167–174.

5. Wild V, Simianer H, Gjoen HM, Gjerde B (1994) Genetic-Parameters and Genotype X Environment Interaction for Early Sexual Maturity in Atlantic Salmon (Salmo-Salar). Aquaculture 128: 51–65.

6. Gjerde B, Simianer H, Refstie T (1994) Estimates of Genetic and Phenotypic Parameters for Body-Weight, Growth-Rate and Sexual Maturity in Atlantic Salmon. Livestock Production Science 38: 133–143.

7. Gjerde B, Gjedrem T (1984) Estimates of Phenotypic and Genetic-Parameters for Carcass Traits in Atlantic Salmon and Rainbow-Trout. Aquaculture 36: 97–110.

8. Gjerde B (1984) Response to Individual Selection for Age at Sexual Maturity in Atlantic Salmon. Aquaculture 38: 229–240.

9. Gjedrem T (2000) Genetic improvement of cold-water fish species. Aquaculture Research 31: 25–33.

10. Moghadam HK, Poissant J, Fotherby H, Haidle L, Ferguson MM, et al. (2007) Quantitative trait loci for body weight, condition factor and age at sexual maturation in Arctic charr (Salvelinus alpinus): comparative analysis with rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Mol Genet Genomics 277: 647–661. 17308931

11. Gutierrez AP, Yanez JM, Fukui S, Swift B, Davidson WS (2015) Genome-Wide Association Study (GWAS) for Growth Rate and Age at Sexual Maturation in Atlantic Salmon (Salmo salar). PLoS One 10: e0119730. doi: 10.1371/journal.pone.0119730 25757012

12. Gutierrez AP, Lubieniecki KP, Fukui S, Withler RE, Swift B, et al. (2014) Detection of quantitative trait loci (QTL) related to grilsing and late sexual maturation in Atlantic salmon (Salmo salar). Mar Biotechnol (NY) 16: 103–110.

13. Johnston SE, Orell P, Pritchard VL, Kent MP, Lien S, et al. (2014) Genome-wide SNP analysis reveals a genetic basis for sea-age variation in a wild population of Atlantic salmon (Salmo salar). Mol Ecol 23: 3452–3468. doi: 10.1111/mec.12832 24931807

14. Lien S, Gidskehaug L, Moen T, Hayes BJ, Berg PR, et al. (2011) A dense SNP-based linkage map for Atlantic salmon (Salmo salar) reveals extended chromosome homeologies and striking differences in sex-specific recombination patterns. BMC Genomics 12: 615. doi: 10.1186/1471-2164-12-615 22182215

15. Davidson WS, Koop BF, Jones SJ, Iturra P, Vidal R, et al. (2010) Sequencing the genome of the Atlantic salmon (Salmo salar). Genome Biol 11: 403. doi: 10.1186/gb-2010-11-9-403 20887641

16. Rubin CJ, Zody MC, Eriksson J, Meadows JR, Sherwood E, et al. (2010) Whole-genome resequencing reveals loci under selection during chicken domestication. Nature 464: 587–591. doi: 10.1038/nature08832 20220755

17. Ferretti L, Ramos-Onsins SE, Perez-Enciso M (2013) Population genomics from pool sequencing. Mol Ecol 22: 5561–5576. doi: 10.1111/mec.12522 24102736

18. Rubin CJ, Megens HJ, Barrio AM, Maqbool K, Sayyab S, et al. (2012) Strong signatures of selection in the domestic pig genome. Proceedings of the National Academy of Sciences of the United States of America 109: 19529–19536. doi: 10.1073/pnas.1217149109 23151514

19. Rubin CJ, Zody MC, Eriksson J, Meadows JRS, Sherwood E, et al. (2010) Whole-genome resequencing reveals loci under selection during chicken domestication. Nature 464: 587–U145. doi: 10.1038/nature08832 20220755

20. Gidskehaug L, Kent M, Hayes BJ, Lien S (2011) Genotype calling and mapping of multisite variants using an Atlantic salmon iSelect SNP array. Bioinformatics 27: 303–310. doi: 10.1093/bioinformatics/btq673 21149341

21. Pedersen S, Berg PR, Culling M, Danzmann RG, Glebe B, et al. (2013) Quantitative trait loci for precocious parr maturation, early smoltification, and adult maturation in double-backcrossed trans-Atlantic salmon (Salmo salar). Aquaculture 410: 164–171.

22. Johnston SE, Orell P, Pritchard VL, Kent MP, Lien S, et al. (2014) Genome-wide SNP analysis reveals a genetic basis for sea-age variation in a wild population of Atlantic salmon (Salmo salar). Mol Ecol.

23. Gurney WS, Bacon PJ, Speirs DC, McGinnity P, Verspoor E (2012) Sea-age variation in maiden Atlantic salmon spawners: phenotypic plasticity or genetic polymorphism? Bull Math Biol 74: 615–640. doi: 10.1007/s11538-011-9679-8 21818674

24. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559–575. 17701901

25. Miller AS, Sheehan TF, Renkawitz MD, Meister AL, Miller TJ (2012) Revisiting the marine migration of US Atlantic salmon using historical Carlin tag data. Ices Journal of Marine Science 69: 1609–1615.

26. Bacon PJ, Palmer SCF, MacLean JC, Smith GW, Whyte BDM, et al. (2009) Empirical analyses of the length, weight, and condition of adult Atlantic salmon on return to the Scottish coast between 1963 and 2006. Ices Journal of Marine Science 66: 844–859.

27. Hansen LP, Quinn TR (1998) The marine phase of the Atlantic salmon (Salmo salar) life cycle, with comparisons to Pacific salmon. Canadian Journal of Fisheries and Aquatic Sciences 55: 104–118.

28. Taranger GL, Haux C, Hansen T, Stefansson SO, Bjornsson BT, et al. (1999) Mechanisms underlying photoperiodic effects on age at sexual maturity in Atlantic salmon, Salmo salar. Aquaculture 177: 47–60.

29. Taranger GL, Vikingstad E, Klenke U, Mayer I, Stefansson SO, et al. (2003) Effects of photoperiod, temperature and GnRHa treatment on the reproductive physiology of Atlantic salmon (Salmo salar L.) broodstock. Fish Physiology and Biochemistry 28: 403–406.

30. Glover KA, Ottera H, Olsen RE, Slinde E, Taranger GL, et al. (2009) A comparison of farmed, wild and hybrid Atlantic salmon (Salmo salar L.) reared under farming conditions. Aquaculture 286: 203–210.

31. Solberg MF, Zhang ZW, Nilsen F, Glover KA (2013) Growth reaction norms of domesticated, wild and hybrid Atlantic salmon families in response to differing social and physical environments. BMC Evolutionary Biology 13.

32. Solberg MF, Skaala O, Nilsen F, Glover KA (2013) Does Domestication Cause Changes in Growth Reaction Norms? A Study of Farmed, Wild and Hybrid Atlantic Salmon Families Exposed to Environmental Stress. Plos One 8.

33. de Juan D, Pazos F, Valencia A (2013) Emerging methods in protein co-evolution. Nat Rev Genet 14: 249–261. doi: 10.1038/nrg3414 23458856

34. Helias-Rodzewicz Z, Perot G, Chibon F, Ferreira C, Lagarde P, et al. (2010) YAP1 and VGLL3, encoding two cofactors of TEAD transcription factors, are amplified and overexpressed in a subset of soft tissue sarcomas. Genes Chromosomes Cancer 49: 1161–1171. doi: 10.1002/gcc.20825 20842732

35. Cousminer DL, Berry DJ, Timpson NJ, Ang W, Thiering E, et al. (2013) Genome-wide association and longitudinal analyses reveal genetic loci linking pubertal height growth, pubertal timing and childhood adiposity. Hum Mol Genet 22: 2735–2747. doi: 10.1093/hmg/ddt104 23449627

36. Halperin DS, Pan C, Lusis AJ, Tontonoz P (2013) Vestigial-like 3 is an inhibitor of adipocyte differentiation. J Lipid Res 54: 473–481. doi: 10.1194/jlr.M032755 23152581

37. Trombley S, Mustafa A, Schmitz M (2014) Regulation of the seasonal leptin and leptin receptor expression profile during early sexual maturation and feed restriction in male Atlantic salmon, Salmo salar L., parr. General and Comparative Endocrinology 204: 60–70. doi: 10.1016/j.ygcen.2014.04.033 24818969

38. Larsen DA, Beckman BR, Strom CR, Parkins PJ, Cooper KA, et al. (2006) Growth modulation alters the incidence of early male maturation and physiological development of hatchery-reared spring Chinook salmon: A comparison with wild fish. Transactions of the American Fisheries Society 135: 1017–1032.

39. Silverstein JT, Shearer KD, Dickhoff WW, Plisetskaya EM (1999) Regulation of nutrient intake and energy balance in salmon. Aquaculture 177: 161–169.

40. Silverstein JT, Shearer KD, Dickhoff WW, Plisetskaya EM (1998) Effects of growth and fatness on sexual development of chinook salmon (Oncorhynchus tshawytscha) parr. Canadian Journal of Fisheries and Aquatic Sciences 55: 2376–2382.

41. McDowell EN, Kisielewski AE, Pike JW, Franco HL, Yao HHC, et al. (2012) A Transcriptome-Wide Screen for mRNAs Enriched in Fetal Leydig Cells: CRHR1 Agonism Stimulates Rat and Mouse Fetal Testis Steroidogenesis. Plos One 7.

42. Reinton N, Collas P, Haugen TB, Skalhegg BS, Hansson V, et al. (2000) Localization of a novel human A-kinase-anchoring protein, hAKAP220, during spermatogenesis. Dev Biol 223: 194–204. 10864471

43. Bodon G, Chassefeyre R, Pernet-Gallay K, Martinelli N, Effantin G, et al. (2011) Charged multivesicular body protein 2B (CHMP2B) of the endosomal sorting complex required for transport-III (ESCRT-III) polymerizes into helical structures deforming the plasma membrane. J Biol Chem 286: 40276–40286. doi: 10.1074/jbc.M111.283671 21926173

44. Ferrari R, Kapogiannis D, Huey ED, Grafman J, Hardy J, et al. (2010) Novel missense mutation in charged multivesicular body protein 2B in a patient with frontotemporal dementia. Alzheimer Dis Assoc Disord 24: 397–401. doi: 10.1097/WAD.0b013e3181df20c7 20592581

45. Ghazi-Noori S, Froud KE, Mizielinska S, Powell C, Smidak M, et al. (2012) Progressive neuronal inclusion formation and axonal degeneration in CHMP2B mutant transgenic mice. Brain 135: 819–832. doi: 10.1093/brain/aws006 22366797

46. Parkinson N, Ince PG, Smith MO, Highley R, Skibinski G, et al. (2006) ALS phenotypes with mutations in CHMP2B (charged multivesicular body protein 2B). Neurology 67: 1074–1077. 16807408

47. Zohar Y, Munoz-Cueto JA, Elizur A, Kah O (2010) Neuroendocrinology of reproduction in teleost fish. Gen Comp Endocrinol 165: 438–455. doi: 10.1016/j.ygcen.2009.04.017 19393655

48. Eisbrenner WS, Botwright N, Cook M, Davidson EA, Dominik S, et al. (2014) Evidence for multiple sex-determining loci in Tasmanian Atlantic salmon (Salmo salar). Heredity 113: 86–92. doi: 10.1038/hdy.2013.55 23759729

49. Yano A, Guyomard R, Nicol B, Jouanno E, Quillet E, et al. (2012) An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Curr Biol 22: 1423–1428. doi: 10.1016/j.cub.2012.05.045 22727696

50. Pendas AM, Moran P, Martinez JL, Garcia-Vazquez E (1995) Applications of 5s-Rdna in Atlantic Salmon, Brown Trout, and in Atlantic Salmon X Brown Trout Hybrid Identification. Molecular Ecology 4: 275–276. 7735532

51. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet journal 17: pp. 10–12.

52. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359. doi: 10.1038/nmeth.1923 22388286

53. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

54. Kofler R, Pandey RV, Schlotterer C (2011) PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinformatics 27: 3435–3436. doi: 10.1093/bioinformatics/btr589 22025480

55. Benjamini Y, Hochberg Y (1995) Controlling the False Discovery Rate—a Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B-Methodological 57: 289–300.

56. Stanke M, Morgenstern B (2005) AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res 33: W465–467. 15980513

57. Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith RK Jr., et al. (2003) Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res 31: 5654–5666. 14500829

58. Wang S, Furmanek T, Kryvi H, Krossoy C, Totland GK, et al. (2014) Transcriptome sequencing of Atlantic salmon (Salmo salar L.) notochord prior to development of the vertebrae provides clues to regulation of positional fate, chordoblast lineage and mineralisation. BMC Genomics 15: 141. doi: 10.1186/1471-2164-15-141 24548379

59. Berthelot C, Brunet F, Chalopin D, Juanchich A, Bernard M, et al. (2014) The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat Commun 5: 3657. doi: 10.1038/ncomms4657 24755649