Abstract
Reintroductions are used to reestablish populations to historical habitats from which they were extirpated. The long-term success of these efforts will depend on genetic diversity and the ability of reintroduced individuals to adapt to ecological change. We examined variation at circadian clock (OtsClock1b and OmyFbxw11) and reproductive timing (Ots515NWFSC)—associated genes in two threatened spring-run Chinook salmon (Oncorhynchus tshawytscha) populations that are undergoing restoration to historical habitats above dams. We also tested for an association between the genes and individual variation in arrival time to the spawning grounds. Our findings indicate that levels of genetic diversity in reintroduced individuals are similar to those found in previously studied spring, summer, fall and winter-run Chinook salmon populations. Captive-rearing programs established following dam construction and the more recent reintroduction efforts thus appear to have maintained diversity at these genes. We observed temporal (between run-years) and spatial (between populations) patterns of genetic differentiation, but little evidence that selection underlies these differences. However, there was a relationship between the circadian-associated gene, OmyFbxw11, and arrival time to the spawning grounds, and in one year of the study, “early” and “late” arrivers to the spawning grounds were more differentiated at the gene than at neutral markers. Taken together, these findings suggest that reintroduced salmon may be capable of an evolutionary response to ecological shifts that alter the adaptive landscape between fitness and arrival timing to the spawning grounds.
Similar content being viewed by others
References
Anderson JJ, Beer WN (2009) Oceanic, riverine, and genetic influences on spring chinook salmon migration timing. Ecol Appl 19:1989–2003
Anderson JH, Pess GR, Carmichael RW et al (2014) Planning Pacific salmon and steelhead reintroductions aimed at long-term viability and recovery. North Am J Fish Manag 34:72–93. doi:10.1080/02755947.2013.847875
Antao T, Lopes A, Lopes RJ et al (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinform 9:323. doi:10.1186/1471-2105-9-323
Armstrong DP, Seddon PJ (2008) Directions in reintroduction biology. Trends Ecol Evol 23:20–25. doi:10.1016/j.tree.2007.10.003
Banks MA, Blouin MS, Baldwin BA et al (1999) Isolation and inheritance of novel microsatellites in Chinook salmon. J Hered 90:281–288
Barrett LW, Fletcher S, Wilton SD (2012) Regulation of eukaryotic gene expression by the untranslated gene regions and other non-coding elements. Cell Mol Life Sci 69:3613–3634. doi:10.1007/s00018-012-0990-9
Biebach I, Keller LF (2009) A strong genetic footprint of the re-introduction history of Alpine ibex (Capra ibex ibex). Mol Ecol 18:5046–5058. doi:10.1111/j.1365-294X.2009.04420.x
Bracis C, Anderson JJ (2013) Inferring the relative oceanic distribution of salmon from patterns in age-specific arrival timing. Trans Am Fish Soc 142:556–567. doi:10.1080/00028487.2012.746240
Brannon E (1982) Orientation mechanisms of homing salmonids. In: Brannon E, Salo E (eds) Salmon and Trout migratory behavior symposium. University of Washington, Seattle, pp 219–227
Brunelli JP, Wertzler KJ, Sundin K, Thorgaard GH (2008) Y-specific sequences and polymorphisms in rainbow trout and Chinook salmon. Genome 51:739–748. doi:10.1139/G08-060
Croisetière S, Bernatchez L, Belhumeur P (2010) Temperature and length-dependent modulation of the MH class II beta gene expression in brook charr (Salvelinus fontinalis) by a cis-acting minisatellite. Mol Immunol 47:1817–1829. doi:10.1016/j.molimm.2009.12.012
Davie A, Minghetti M, Migaud H (2009) Seasonal variations in clock-gene expression in Atlantic salmon (Salmo salar). Chronobiol Int 26:379–395. doi:10.1080/07420520902820947
Do C, Waples RS, Peel D et al (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214. doi:10.1111/1755-0998.12157
Evans ML, Præbel K, Peruzzi S et al (2014) Phenotype-environment association of the oxygen transport system in trimorphic European whitefish populations. Evolution (N Y) 8:2197–2210. doi:10.1111/evo.12442
Excoffier L, Hofer T, Foll M (2009) Detecting loci under selection in a hierarchically structured population. Heredity (Edinb) 103:285–298. doi:10.1038/hdy.2009.74
Frankham R (1999) Quantitative genetics in conservation biology. Genet Res 74:237–244
Gharrett AJ, Joyce J, Smoker WW (2013) Fine-scale temporal adaptation within a salmonid population: mechanism and consequences. Mol Ecol 22:4457–4469. doi:10.1111/mec.12400
Greig C, Jacobson DP, Banks MA (2003) New tetranucleotide microsatellites for fine-scale discrimination among endangered chinook salmon. Mol Ecol Notes 3:376–379. doi:10.1046/j.1471-8286.2003.00455.x
Hendry A, Bohlin T, Jonsson B, Berg O (2003) To sea or not to sea? Anadromy versus non-anadromy in salmonids. In: Hendry A, Stearns S (eds) Evolution illuminated: Salmon and their relatives. Oxford University Press, New York, pp 95–125
Ivanova N, Dewaard JR, Hebert PDN (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol Ecol Notes 6:998–1002. doi:10.1111/j.1471-8286.2006.01428.x
Jamieson IG, Allendorf FW (2012) How does the 50/500 rule apply to MVPs? Trends Ecol Evol 27:578–584. doi:10.1016/j.tree.2012.07.001
Johnson MA, Friesen TA (2010) Spring Chinook salmon hatcheries in the Willamette basin: existing data, discernable patterns and information gaps. US Army Corps Eng Task Order NWPPM-09-FH-05 88
Johnson MA, Friesen TA (2014) Genetic diversity and population structure of spring Chinook salmon from the Upper Willamette River, Oregon. North Am J Fish Manag 34:853–862. doi:10.1080/02755947.2014.920739
Kenaston K, Schroeder K, Monzyk F, Cannon B (2009) Interim activities for monitoring impacts associated with Hatchery programs in the Willamette basin, USACE funding 2008
King DP, Zhao Y, Sangoram AM et al (1997) Positional cloning of the mouse circadian clock gene. Cell 89:641–653. doi:10.1016/S0092-8674(00)80245-7
Kovach RP, Gharrett AJ, Tallmon DA (2012) Genetic change for earlier migration timing in a pink salmon population. Proc Biol Sci 279:3870–3878. doi:10.1098/rspb.2012.1158
Lemay MA, Russello MA (2014) Latitudinal cline in allele length provides evidence for selection in a circadian rhythm gene. Biol J Linn Soc 111:869–877
Lowrey PL, Takahashi JS (2004) Mammalian circadian biology: elucidating genome-wide levels of temporal organization. Annu Rev Genom Hum Genet 5:407–441. doi:10.1146/annurev.genom.5.061903.175925
Mattson C (1962) An investigation of adult spring Chinook salmon of the Willamette River system, 1946–51. Oregon Fish Commission, Portland
Miller KA, Towns DR, Allendorf FW et al (2010) Genetic structure and individual performance following a recent founding event in a small lizard. Conserv Genet 12:461–473. doi:10.1007/s10592-010-0154-0
Minckley WL (1995) Translocation as a tool for conserving impleriled fishes: experiences in western United States. Biol Conserv 72:297–309
Morbey YE (2002) Protandry models and their application to salmon. Behav Ecol Sociobiol 13:337–343
Morbey YE, Jensen EL, Russello MA (2014) Time scale matters: genetic analysis does not support adaptation-by-time as the mechanism for adaptive seasonal declines in kokanee reproductive life span. Ecol Evol 4:3714–3722. doi:10.1002/ece3.1214
Moritz C (1994) Defining “evolutionarily significant units” for conservation. Trends Ecol Evol 9:373–375. doi:10.1016/0169-5347(94)90057-4
Naish KA, Park LK (2002) Linkage relationships for 35 new microsatellite loci in Chinook salmon. Anim Genet 33:316–318
O’Malley KG, Banks MA (2008a) Duplicated Clock genes with unique polyglutamine domains provide evidence for nonhomologous recombination in Chinook salmon (Oncorhynchus tshawytscha). Genetica 132:87–94. doi:10.1007/s10709-007-9151-8
O’Malley KG, Banks MA (2008b) A latitudinal cline in the Chinook salmon (Oncorhynchus tshawytscha) Clock gene: evidence for selection on PolyQ length variants. Proc Biol Sci 275:2813–2821. doi:10.1098/rspb.2008.0524
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. J Hered 94:273–284. doi:10.1093/jhered/esg067
O’Malley KG, Camara MD, Banks MA (2007) Candidate loci reveal genetic differentiation between temporally divergent migratory runs of Chinook salmon (Oncorhynchus tshawytscha). Mol Ecol 16:4930–4941. doi:10.1111/j.1365-294X.2007.03565.x
O’Malley KG, Ford MJ, Hard JJ (2010) Clock polymorphism in Pacific salmon: evidence for variable selection along a latitudinal gradient. Proc Biol Sci 277:3703–3714. doi:10.1098/rspb.2010.0762
O’Malley KG, Jacobson DP, Kurth R et al (2013) Adaptive genetic markers discriminate migratory runs of Chinook salmon (Oncorhynchus tshawytscha) amid continued gene flow. Evol Appl 6:1184–1194. doi:10.1111/eva.12095
ODFW, NMFS (2011) Upper Willamette River conservation and recovery plan for Chinook salmon and steelhead
Quinn TP (1982) A model for salmon navigation on the high seas. In: Brannon E, Salo E (eds) Salmon and trout migratory behaviour symposium. University of Washington, Seattle, pp 229–237
Quinn TP, Adams DJ (1996) Environmental changes affecting the migratory timing of American shad and sockeye salmon. Ecology 77:1151–1162
Quinn TP, Dittman AH (1990) Pacific salmon migrations and homing: mechanisms and adaptive significance. Trends Ecol Evol 5:174–177. doi:10.1016/0169-5347(90)90205-R
Quinn TP, Unwin MJ, Kinnison MT (2000) Evolution of temporal isolation in the wild: genetic divergence in timing of migration and breeding by introduced Chinook salmon populations. Evolution (N Y) 54:1372–1385
Raymond HL (1988) Effects of hydroelectric development and fisheries enhancement on spring and summer Chinook salmon and steelhead in the Columbia River basin. North Am J Fish Manag 8:37–41. doi:10.1577/1548-8675(1988)008<0001
Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution (N Y) 49:1280–1283. doi:10.2307/2410454
Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237
Ricker WE (1972) Hereditary and environmental factors affecting certain salmonid populations. In: Simon RC, Larkin PA (eds) Stock concept Pacific salmon. The University of British Columbia, Vancouver, pp 19–160
Ryman N, Palm S, André C et al (2006) Power for detecting genetic divergence: differences between statistical methods and marker loci. Mol Ecol 15:2031–2045. doi:10.1111/j.1365-294X.2006.02839.x
Saino N, Bazzi G, Gatti E et al (2015) Polymorphism at the Clock gene predicts phenology of long-distance migration in birds. Mol Ecol 24:1758–1773. doi:10.1111/mec.13159
Salem M, Rexroad CE, Wang J et al (2010) Characterization of the rainbow trout transcriptome using Sanger and 454-pyrosequencing approaches. BMC Genom 11:564. doi:10.1186/1471-2164-11-564
Sard NM, O’Malley KO, Jacobson DP, Hogansen MJ, Johnson MA, Banks MA (2015) Factors influencing spawner success in a spring Chinook salmon reintroduction program. Can J Fish Aquat Sci (in press)
Siwach P, Pophaly SD, Ganesh S (2006) Genomic and evolutionary insights into genes encoding proteins with single amino acid repeats. Mol Biol Evol 23:1357–1369. doi:10.1093/molbev/msk022
Smoker WW, Gharrett AJ, Stekoll MS (1998) Genetic variation of return date in a population of pink salmon: a consequence of fluctuating environment and dispersive selection? Alaska Fish Res Bull 5:46–54
Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary N e using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262. doi:10.1111/j.1752-4571.2009.00104.x
Waples RS, Teel DJ (1990) Conservation genetics of Pacific salmon I. Temporal changes in allele frequency. Conserv Biol 4:144–156
Waples RS, Zabel RW, Scheuerell MD, Sanderson BL (2007) Evolutionary responses by native species to major anthropogenic changes to their ecosystems: Pacific salmon in the Columbia River hydropower system. Mol Ecol 17:84–96. doi:10.1111/j.1365-294X.2007.03510.x
Waples RS, Antao T, Luikart G (2014) Effects of overlapping generations on linkage disequilibrium estimates of effective population size. Genetics 197:769–780. doi:10.1534/genetics.114.164822
Weeks AR, Moro D, Thavornkanlapachai R et al (2015) Conserving and enhancing genetic diversity in translocation programs. In: Armstrong D, Hayward M, Moro D, Seddon P (eds) Advances in Reintroduction biology of Australian and New Zealand fauna. CSIRO Publishing, Melbourne, pp 127–140
Whitmore D, Foulkes NS, Sassone-Corsi P (2000) Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature 404:87–91
Zhang EE, Liu AC, Hirota T et al (2009) A genome-wide RNAi screen for modifiers of the circadian clock in human cells. Cell 139:199–210. doi:10.1016/j.cell.2009.08.031
Zhdanova IV, Reebs SG (2006) Circadian rhythms in fish. Fish Physiol 24:197–238
Acknowledgments
Thanks to the U.S. Army Corps of Engineers and ODFW for sampling adult Chinook salmon at Foster and Cougar dams during the spawning migrations of 2012 and 2013. This study was co-funded by the ASSURE program of the Department of Defense in partnership with the National Science Foundation REU Site program under Grant No. NSF OCE-1263349.
Data accessibility
Data will be uploaded to DRYAD upon acceptance.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Evans, M.L., Shry, S.J., Jacobson, D.P. et al. Functional gene diversity and migration timing in reintroduced Chinook salmon. Conserv Genet 16, 1455–1464 (2015). https://doi.org/10.1007/s10592-015-0753-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-015-0753-x