A large-scale chromosomal inversion is not associated with life history development in rainbow trout from Southeast Alaska
Autoři:
Spencer Y. Weinstein aff001; Frank P. Thrower aff002; Krista M. Nichols aff003; Matthew C. Hale aff001
Působiště autorů:
Department of Biology, Texas Christian University, Fort Worth, United States of America
aff001; Ted Stevens Marine Research Institute, Alaska Fisheries Center, NOAA, Juneau, AK, United States of America
aff002; Conservation Biology Division, Northwest Fisheries Science Center, Seattle, WA, United States of America
aff003
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0223018
Souhrn
In studying the causative mechanisms behind migration and life history, the salmonids–salmon, trout, and charr–are an exemplary taxonomic group, as life history development is known to have a strong genetic component. A double inversion located on chromosome 5 in rainbow trout (Oncorhynchus mykiss) is associated with life history development in multiple populations, but the importance of this inversion has not been thoroughly tested in conjunction with other polymorphisms in the genome. To that end, we used a high-density SNP chip to genotype 192 F1 migratory and resident rainbow trout and focused our analyses to determine whether this inversion is important in life history development in a well-studied population of rainbow trout from Southeast Alaska. We identified 4,994 and 436 SNPs–predominantly outside of the inversion region–associated with life history development in the migrant and resident familial lines, respectively. Although F1 samples showed genomic patterns consistent with the double inversion on chromosome 5 (reduced observed and expected heterozygosity and an increase in linkage disequilibrium), we found no statistical association between the inversion and life history development. Progeny produced by crossing resident trout and progeny produced by crossing migrant trout both consisted of a mix of migrant and resident individuals, irrespective of the individuals’ inversion haplotype on chromosome 5. This suggests that although the inversion is present at a low frequency, it is not strongly associated with migration as it is in populations of Oncorhynchus mykiss from lower latitudes.
Klíčová slova:
Biology and life sciences – Organisms – Eukaryota – Animals – Vertebrates – Fish – Osteichthyes – Trout – Evolutionary biology – Genetics – Population genetics – Phenotypes – Heredity – Heterozygosity – Linkage disequilibrium – Population biology – Cell biology – Chromosome biology – Chromosomal aberrations – Chromosomal inversions – Earth sciences – Marine and aquatic sciences – Bodies of water – Geography – Cartography – Latitude – Ecology and environmental sciences – Aquatic environments – Freshwater environments – Lakes
Zdroje
1. Waples RS, Teel DJ, Myers JM, Marshall AR. 2004. Life-history divergence in Chinook salmon: Historic contingency and parallel evolution. Evolution 58:386–403. 15068355
2. Rosenblum EB and LJ Harmon LJ. 2011. "Same same but different": Replicated ecological speciation at White Sands. Evolution 65:946–960. doi: 10.1111/j.1558-5646.2010.01190.x 21073450
3. Colosimo PF, Peichel CL, Nereng K, Blackman BK, Shapiro MD, Schluter D, et al. 2004. The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS Biology 2(5):e109. doi: 10.1371/journal.pbio.0020109 15069472
4. 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(2):e1000862. doi: 10.1371/journal.pgen.1000862 20195501
5. Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, Johnson J, et al. 2012. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55–61. doi: 10.1038/nature10944 22481358
6. Nachman MW, Hoekstra HE, D'Agostino SL. 2003. The genetic basis of adaptive melanism in pocket mice. Proceedings of the National Academy of Sciences. 100(9):5268–73.
7. Schluter D, Clifford EA, Nemethy M, McKinnon JS. 2004. Parallel evolution and inheritance of quantitative traits. The American Naturalist. 163(6):809–22. doi: 10.1086/383621 15266380
8. Rockman MV. 2012. The QTN program and the alleles that matter for evolution: all that's gold does not glitter. Evolution: International Journal of Organic Evolution. 66(1):1–7.
9. Barth JMI, Berg PR, Jonsson PR, Bonanomi S, Corell H, Hemmer-Hansen J, et al. 2017. Genome architecture enables local adaptation of Atlantic cod despite high connectivity. Molecular Ecology 26:4452–4466. doi: 10.1111/mec.14207 28626905
10. Sinclair-Waters M, Bradbury IR, Morris CJ, Lien S, Kent MP, Bentzen P. 2018. Ancient chromosomal rearrangement associated with local adaptation of a postglacially colonized population of Atlantic Cod in the northwest Atlantic. Molecular Ecology. 27(2):339–51. doi: 10.1111/mec.14442 29193392
11. Lindtke D, Lucek K, Soria-Carrasco V, Villoutreix R, Farkas TE, Riesch R, et al. 2017. Long-term balancing selection on chromosomal variants associated with crypsis in a stick insect. Molecular Ecology 26:6189–6205. doi: 10.1111/mec.14280 28786544
12. Pearse DE, Barson NJ, Nome T, Gao G, Campbell MA, Abadia-Cardoso A, et al. 2018. Sex-dependent dominance maintains migration supergene in rainbow trout. BioRxiv: http://dx.doi.org/10.1101/504621
13. Lowry DB and Willis JH. 2010. A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. PLoS Biology 8.
14. Feder JL and Nosil P. 2009. Chromosomal inversions and species differences: When are genes affecting adaptive divergence and reproductive isolation expected to reside within inversions? Evolution 63:3061–3075. doi: 10.1111/j.1558-5646.2009.00786.x 19656182
15. Wellenreuther M and Bernatchez L. 2018. Eco-Evolutionary genomics of chromosomal inversions. Trends in Ecology & Evolution 33:427–440.
16. Knief U, Forstmeier W, Pei YF, Ihle M, Wang DP, Martin K, et al. 2017. A sex-chromosome inversion causes strong overdominance for sperm traits that affect siring success. Nature Ecology & Evolution 1:1177–1184.
17. Sundin K, Brown KH, Drew RE, Nichols KM, Wheeler PA, Thorgaard GH. 2005. Genetic analysis of a development rate QTL in backcrosses of clonal rainbow trout, Oncorhynchus mykiss. Aquaculture 247:75–83.
18. O'Malley KG, Sakamoto T, Danzmann RG, Ferguson MM. 2003. Quantitative trait loci for spawning date and body weight in rainbow trout: Testing for conserved effects across ancestrally duplicated chromosomes. Journal of Heredity 94:273–284. doi: 10.1093/jhered/esg067 12920098
19. Danzmann RG, Cairney M, Davidson WS, Ferguson MM, Gharbi K, Guyomard R, et al. 2005. A comparative analysis of the rainbow trout genome with 2 other species of fish (Arctic charr and Atlantic salmon) within the tetraploid derivative Salmonidae family (subfamily: Salmoninae). Genome. 48(6):1037–51. doi: 10.1139/g05-067 16391673
20. Leder EH, Danzmann RG, Ferguson MM. 2006. The candidate gene, Clock, localizes to a strong spawning time quantitative trait locus region in rainbow trout. Journal of Heredity 97:74–80. doi: 10.1093/jhered/esj004 16407529
21. Nichols KM, Broman KW, Sundin K, Young JM, Wheeler PA, Thorgaard GH. 2007. Quantitative trait loci x maternal cytoplasmic environment interaction for development rate in Oncorhynchus mykiss. Genetics 175(1):335–47. doi: 10.1534/genetics.106.064311 17057232
22. Miller MR, Brunelli JP, Wheeler PA, Liu S, Rexroad CE, Palti Y, et al. 2012. A conserved haplotype controls parallel adaptation in geographically distant salmonid populations. Mol Ecol 21(2):237–49. doi: 10.1111/j.1365-294X.2011.05305.x 21988725
23. Pearse DE, Miller MR, Abadia-Cardoso A, Garza JC. 2014. Rapid parallel evolution of standing variation in a single, complex, genomic region is associated with life history in steelhead/rainbow trout. Proc Biol Sci 281(1783):20140012. doi: 10.1098/rspb.2014.0012 24671976
24. Leitwein M, Garza JC, Pearse DE. 2017. Ancestry and adaptive evolution of anadromous, resident, and adfluvial rainbow trout (Oncorhynchus mykiss) in the San Francisco Bay area: application of adaptive genomic variation to conservation in a highly impacted landscape. Evolutionary Applications 10:56–67. doi: 10.1111/eva.12416 28035235
25. Arostegui MC, Quinn TP, Seeb LW, Seeb JE, McKinney GJ. 2019. Retention of a chromosomal inversion from an anadromous ancestor provides the genetic basis for alternative freshwater ecotypes in rainbow trout. Molecular Ecology.
26. Nichols KM, Edo AF, Wheeler PA, Thorgaard GH. 2008. The genetic basis of smoltification-related traits in Oncorhynchus mykiss. Genetics 179(3):1559–75. doi: 10.1534/genetics.107.084251 18562654
27. Hecht BC, Thrower FP, Hale MC, Miller MR, Nichols KM. 2012. Genetic architecture of migration-related traits in rainbow and steelhead trout, Oncorhynchus mykiss. G3: Genes| Genomes| Genetics 2(9):1113–27. doi: 10.1534/g3.112.003137 22973549
28. Hecht BC, Campbell NR, Holecek DE, Narum SR. 2013. Genome‐wide association reveals genetic basis for the propensity to migrate in wild populations of rainbow and steelhead trout. Mol Ecol 22(11):3061–76. doi: 10.1111/mec.12082 23106605
29. Hale MC, Thrower FP, Berntson EA, Miller MR, Nichols KM. 2013. Evaluating adaptive divergence between migratory and nonmigratory ecotypes of a salmonid fish, Oncorhynchus mykiss. G3: Genes| Genomes| Genetics 3(8):1273–85. doi: 10.1534/g3.113.006817 23797103
30. Hecht BC, Hard JJ, Thrower FP, Nichols KM. 2015. Quantitative genetics of migration-related traits in rainbow and steelhead trout. G3: Genes| Genomes| Genetics 5(5):873–89. doi: 10.1534/g3.114.016469 25784164
31. Thrower FP and Joyce JE. 2004. Effects of 70 years of freshwater residency on survival, growth, early maturation, and smolting in a stock of anadromous rainbow trout from southeast Alaska. American Fisheries Society Symposium. 485.
32. Thrower FP, Hard JJ, Joyce JE. 2004. Genetic architecture of growth and early life‐history transitions in anadromous and derived freshwater populations of steelhead. J Fish Biol 65(s1):286–307.
33. Hale MC, McKinney GJ, Thrower FP, Nichols KM. 2016. RNA-seq reveals differential gene expression in the brains of juvenile resident and migratory smolt rainbow trout (Oncorhynchus mykiss). Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 20:136–50.
34. Brunelli JP, Wertzler KJ, Sundin K, Thorgaard GH. 2008. Y-specific sequences and polymorphisms in rainbow trout and Chinook salmon. Genome 51:739–48. doi: 10.1139/G08-060 18772952
35. Palti Y, Gao G, Liu S, Kent MP, Lien S, Miller MR, et al. 2015. The development and characterization of a 57K single nucleotide polymorphism array for rainbow trout. Molecular Ecology Resources 15:662–672. doi: 10.1111/1755-0998.12337 25294387
36. Langmead B and Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods 9:357–U354. doi: 10.1038/nmeth.1923 22388286
37. Chang CC, Chow CC, Tellier L, Vattikuti S, Purcell SM, Lee JJ. 2015. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience 4.
38. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES. (2007) TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–35. doi: 10.1093/bioinformatics/btm308 17586829
39. Foll M and 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. doi: 10.1534/genetics.108.092221 18780740
40. McKinney GJ, Hale MC, Goetz G, Gribskov M, Thrower FP, Nichols KM. 2015. Ontogenetic changes in embryonic and brain gene expression in progeny produced from migratory and resident Oncorhynchus mykiss. Molecular Ecology 24:1792–1809. doi: 10.1111/mec.13143 25735875
41. Lien S, Koop BF, Sandve SR, Miller JR, Kent MP, Nome T, et al. 2016. The Atlantic salmon genome provides insights into rediploidization. Nature 533(7602):200. doi: 10.1038/nature17164 27088604
42. McCormick SD. 2012. Smolt physiology and endocrinology. Fish Physiology 32:199–251.
43. Stefansson S, Bjornsson B, Ebbensson L, McCormick S. (2008) Smoltification. In: Kappor BJ, Finn RN (eds). Fish Larval Physiology. Wiley-Blackwell: London, UK.
44. Hecht BC, Valle ME, Thrower FP, Nichols KM. 2014. Divergence in expression of candidate genes for the smoltification process between juvenile resident rainbow and anadromous steelhead trout. Marine Biotechnology 16(6):638–56. doi: 10.1007/s10126-014-9579-7 24952010
45. Roesti M, Moser D, Berner D. 2013. Recombination in the threespine stickleback genome–patterns and consequences. Molecular Ecology 22:3014–3027. doi: 10.1111/mec.12322 23601112
46. Hale MC, Colletti JA, Gahr SA, Scardina J, Thrower FP, Harmon M, et al. 2014. Mapping and expression of candidate genes for development rate in rainbow trout (Oncorhynchus mykiss). J Hered 105(4):506–20. doi: 10.1093/jhered/esu018 24744432
47. McCusker MR, Parkinson E, Taylor EB. 2000. Mitochondrial DNA variation in rainbow trout (Oncorhynchus mykiss) across its native range: testing biogeographical hypotheses and their relevance to conservation. Molecular Ecology. 9(12):2089–108. 11123621
48. Docker MF and Heath DD. 2003. Genetic comparison between sympatric anadromous steelhead and freshwater resident rainbow trout in British Columbia, Canada. Conserv Genet 4(2):227–31.
49. Nichols KM, Kozfkay CC, Narum SR. 2016. Genomic signatures among Oncorhynchus nerka ecotypes to inform conservation and management of endangered sockeye salmon. Evolutionary Applications 9(10):1285–300. doi: 10.1111/eva.12412 27877206
50. Morro B, Balseiro P, Albalat A, Pedrosa C, Mackenzie S, Nakamura S, et al. 2019. Effects of different photoperiod regimes on the smoltification and seawater adaptation of seawater-farmed rainbow trout (Oncorhynchus mykiss): Insights from Na+, K+- ATPase activity and transcription of osmoregulation and growth genes. Aquaculture 507: 282–292.
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