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Thermal tolerance of a thermally selected strain of rainbow trout Oncorhynchus mykiss and the pedigrees of its F1 and F2 generations indicated by their critical thermal maxima

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Abstract

A thermally selected strain of rainbow trout has been established by selective breeding since 1966 in Miyazaki, Japan. In the present study, we compared the critical thermal maxima (CTMs), the temperatures at which organisms reach a predefined sublethal endpoint and lose their equilibrium, between a thermally selected and two normal (Donaldson) strains of rainbow trout. The CTM of one normal strain from Nikko (Nikko strain) acclimated to 20 °C (29.7 °C) was significantly lower than those of the thermally selected strain (30.0 °C) and the other Donaldson strain from Aomori (29.9 °C) (P < 0.05). The F1 generations, F1T and F1N, were produced by crossing thermally selected strain females with Nikko strain males and Nikko strain females with thermally selected strain males, respectively. No significant difference was observed in the CTM between F1T [30.1 ± 0.15 °C (n = 30)] and F1N [30.1 ± 0.16 °C (n = 30)] (P > 0.05) for fish acclimated to 20 °C, suggesting that the F1 offspring inherited the thermal tolerance trait from one thermally selected strain parent irrespective of whether it was the male or female. F2 offspring of F1T or F1N also showed the thermal tolerance trait. The coefficients of variation for CTM were also compared among all the datasets obtained in the present study and their values for F1 hybrids were lower than those of the parental generation of the Nikko strain (P < 0.05). In contrast, the coefficients of variation of F2s were the same as those of their parental generation. Furthermore, the thermally selected strain and Nikko strain as a reference family provide a F2 generation for segregating phenotypes, which is required for in-depth genetic analysis of the thermally selected rainbow trout strain.

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References

  • Anttila K, Dhillon RS, Boulding EG, Farrell AP, Glebe BD (2013) Variation in temperature tolerance among families of Atlantic salmon (Salmo salar) is associated with hypoxia tolerance, ventricle size and myoglobin level. J Exp Biol 216:1183–1190

    Article  PubMed  CAS  Google Scholar 

  • Becker CD, Genoway RG (1979) Evaluation of the critical thermal maximum for determining thermal tolerance of freshwater fish. Environ Biol Fish 4:245–256

    Article  Google Scholar 

  • Beitinger TL, Bennett WA, McCauley RW (2000) Temperature tolerances of North American freshwater fishes exposed to dynamic changes in temperature. Environ Biol Fish 58:237–275

    Article  Google Scholar 

  • Boettcher PJ, Stella A, Pizzi F, Gandini G (2005) The combined use of embryos and semen for cryogenic conservation of mammalian livestock genetic resources. Genet Sel Evol 37:657–675

    Article  PubMed  PubMed Central  Google Scholar 

  • Börner A (2006) Preservation of plant genetic resources in the biotechnology era. Biotechnol J 1:1393–1404

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Snow M, Lawrence CS, Church AR, Narum SR, Devlin RH, Farrell AP (2015) Selection for upper thermal tolerance in rainbow trout (Oncorhynchus mykiss Walbaum). J Exp Biol 218:803–812. https://doi.org/10.1242/jeb.113993

    Article  PubMed  Google Scholar 

  • Cox DK (1974) Effects of three heating rates on the critical thermal maximum of bluegill. In: Gibbons JW, Sharitz RR (eds) Thermal ecology Conference 730505. National Technical Information Service, Springfield, pp 158–163

    Google Scholar 

  • Currie RJ, Bennett WA, Beitinger TL (1998) Critical thermal minima and maxima of three freshwater game-fish species. Environ Biol Fish 51:187–200

    Article  Google Scholar 

  • Danzmann RG, Jackson TR, Ferguson MM (1999) Epistasis in allelic expression at upper temperature tolerance QTL in rainbow trout. Aquaculture 173:45–58

    Article  CAS  Google Scholar 

  • Donaldson LR, Olson PR (1955) Development of rainbow trout blood stock by selective breeding. Trans Am Fish Soc 85:93–101

    Article  Google Scholar 

  • Eliason EJ, Clark TD, Hague MJ, Hanson LM, Gallagher ZS, Jeffries KM, Gale MK, Patterson DA, Hinch SG, Farrell AP (2011) Differences in thermal tolerance among sockeye salmon populations. Science 332:109–112. https://doi.org/10.1126/sience.1199158

    Article  PubMed  CAS  Google Scholar 

  • Elliott JM (1981) Some aspects of thermal stress on freshwater teleosts. In: Pickering AC (ed) Stress and fish. Academic, London, pp 209–245

    Google Scholar 

  • Elliott JM (1991) Tolerance and resistance to thermal stress in juvenile Atlantic salmon, Salmo salar. Freshwater Biol 25:61–70

    Article  Google Scholar 

  • FAO/UNEP (1981) Conservation of the genetic resources of fish: problems and recommendations. Report of the Expert Consultation on the genetic resources of fish. FAO Fish Tech Pap 217:43

  • Fujio Y, Nakajima M, Nomura G (1995) Selection response on thermal resistance of the guppy Poecilia reticulata. Fish Sci 61:731–734

    Article  CAS  Google Scholar 

  • Galbreath PF, Adams ND, Sherrill LW, Martin TH (2006) Thermal tolerance of diploid versus triploid rainbow trout and brook trout assessed by time to chronic lethal maximum. Environ Biol Fish 75:183–193

    Article  Google Scholar 

  • Hartman KJ, Porto MA (2014) Thermal performance of three rainbow trout strains at above-optimal temperatures. Trans Am Fish Soc 143:1445–1454

    Article  Google Scholar 

  • Henryon M, Berg P, Olesen NJ, Kjaer TE, Slierendrecht WJ, Jokumsen A, Lund I (2005) Selective breeding provides an approach to increase resistance of rainbow trout (Oncorhynchus mykiss) to the diseases, enteric redmouth disease, rainbow trout fry syndrome, and viral haemorrhagic septicaemia. Aquaculture 250:621–636. https://doi.org/10.1016/j.aquaculture.2004.12.022

    Article  Google Scholar 

  • Hill WG, Mulder HA (2010) Genetic analysis of environmental variation. Genet Res Camb 92:381–395. https://doi.org/10.1017/S0016672310000546

    Article  PubMed  Google Scholar 

  • Ibáñez-Escriche N, Moreno A, Nieto B, Piquears P, Salgado C, Gutiérrez JP (2008) Genetic parameters related to environmental variability of weight traits in a selection experiment for weight gain in mice: signs of correlated canalised response. Genet Sel Evol 40:279–293

    PubMed  PubMed Central  Google Scholar 

  • Ikeguchi K, Ineno T, Itoi S, Kondo H, Kinoshita S, Watabe S (2006) Increased levels of mitochondrial gene transcripts in the thermally selected rainbow trout (Oncorhynchus mykiss) strain during embryonic development. Mar Biotechnol 8:178–188

    Article  PubMed  CAS  Google Scholar 

  • Ineno T, Tsuchida S, Kanda M, Watabe S (2005) Thermal tolerance of a rainbow trout Oncorhynchus mykiss strain selected by high-temperature breeding. Fish Sci 71:767–775

    Article  CAS  Google Scholar 

  • Itoi S, Ineno T, Kinoshita S, Hirayama Y, Nakaya M, Kakinuma M, Watabe S (2001) Analysis on serum proteins from rainbow trout Oncorhynchus mykiss exposed to high temperature. Fish Sci 67:191–193

    Article  CAS  Google Scholar 

  • Jackson TR, Ferguson MM, Danzmann RG, Fishback AG, Ihssen PE, O’Connell M, Crease TJ (1998) Identification of two QTL influencing upper temperature tolerance in rainbow trout (Oncorhynchus mykiss). Heredity 80:143–151

    Article  Google Scholar 

  • Janhunen M, Kause A, Vehvilainen H, Jarvisalo O (2012) Genetics of microenvironmental sensitivity of body weight in rainbow trout (Oncorhynchus mykiss) selected for improved growth. PLoS One 7(6):e38766. https://doi.org/10.1371/journal.pone.0038766

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kause A, Paananen T, Ritola O, Koskinen H (2007) Direct and indirect selection of visceral lipid weight, fillet weight, and fillet percentage in a rainbow trout breeding program. J Anim Sci 85:3218–3227. https://doi.org/10.2527/jas.2007-0332

    Article  PubMed  CAS  Google Scholar 

  • Kudo H, Inoguchi N, Kijima A (2001) Estimation of heritability of tolerance to high water temperature by factorial mating system in rainbow trout (Oncorhynchus mykiss). Suisanzoshoku 49:405–411 (in Japanese)

    Google Scholar 

  • Lahnsteiner F (2000) Semen cryopreservation in the Salmonidae and in the northern pike. Aquac Res 31:245–258

    Article  Google Scholar 

  • Lee CG, Farrell AP, Lotto A, MacNutt MJ, Hinch SG, Healey MC (2003) The effect of temperature on swimming performance and oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks. J Exp Biol 206:3239–3251

    Article  PubMed  CAS  Google Scholar 

  • Leeds TD, Silverstein JT, Weber GM, Vallejo RL, Palti Y, Rexroad CE 3rd, Evenhuis J, Hadidi S, Welch TJ, Wiens GD (2010) Response to selection for bacterial cold water disease resistance in rainbow trout. J Anim Sci 88:1936–1946. https://doi.org/10.2527/jas.2009-2538

    Article  PubMed  CAS  Google Scholar 

  • Leung LK, Jamieson BG (1991) Live preservation of fish gametes. In: Jamieson BG (ed) Fish evolution and systematics: evidence from spermatozoa. Cambridge University Press, Cambridge, pp 245–269

    Google Scholar 

  • Lund SG, Caissie D, Cunjak RA, Vijayan MM, Tuft BL (2002) The effects of environmental heat stress on heat shock mRNA and protein expression in Miramichi Atlantic salmon (Salmo salar) Parr. Can J Fish Aquat Sci 59:1553–1562

    Article  CAS  Google Scholar 

  • Myrick CA, Cech JJ Jr (2005) Effects of temperature on the growth, food consumption, and thermal tolerance of age-0 nimbus-strain steelhead. N Am J Aquac 67:324–330

    Article  Google Scholar 

  • Ojima N, Mekuchi M, Ineno T, Tamaki K, Kera A, Kinoshita S, Asakawa S, Watabe S (2012) Differential expression of heat-shock proteins in F2 offspring from F1 hybrids produced between thermally selected and normal rainbow trout strains. Fish Sci 78:1051–1057

    Article  CAS  Google Scholar 

  • Perry GML, Danzmann RG, Ferguson MM, Gibson JP (2001) Quantitative trait loci for upper thermal tolerance in outbred strains of rainbow trout (Oncorhynchus mykiss). Heredity 86:333–341

    Article  PubMed  CAS  Google Scholar 

  • Pickering AD (1992) Rainbow trout husbandry: management of the stress response. Aquaculture 100:125–139

    Article  Google Scholar 

  • Sae-Lim P, Komen H, Kause A, Van Arendonk JM, Barfoot AJ, Martin KE, Parsons JE (2012) Defining desired genetic gains for rainbow trout breeding objective using analytic hierarchy process. J Anim Sci 90:1766–1776

    Article  PubMed  CAS  Google Scholar 

  • Schindler DW (2001) The cumulative effects of climate warming and other human stresses on Canadian freshwaters in the new millennium. Can J Fish Aquat Sci 58:18–29

    Article  Google Scholar 

  • Tan E, Kinoshita S, Suzuki Y, Ineno T, Tamaki K, Kera A, Muto K, Yada T, Kitamura S, Asakawa S, Watabe S (2016) Different gene expression profiles between normal and thermally selected strains of rainbow trout, Oncorhynchus mykiss, as revealed by comprehensive transcriptome analysis. Gene 576:637–643

    Article  PubMed  CAS  Google Scholar 

  • Tang E, Wongwarangkana C, Kinoshita S, Suzuki Y, Oshima K, Hattori M, Ineno T, Tamaki K, Kera A, Muto K, Yada T, Kitamura S, Asakawa S, Watabe S (2012) Global gene expression analysis of gill tissues from normal and thermally selected strains of rainbow trout. Fish Sci 78:1041–1049

    Article  CAS  Google Scholar 

  • Tsujimura A, Taniguchi N (1996) Reduction of phenotypic variation in reproductive traits of clonal strains of ayu Plecoglossusa ltivelis. Nippon Suisan Gakkaishi 62:393–398

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported in part by a grant from the Ministry of Agriculture, Forestry, and Fisheries of Japan. We are grateful to the researchers at Aomori Prefectural Industrial Technology Research Center, Freshwater Fisheries Research Institute, for providing the rainbow trout. We also thank Mr. T. Setoguma and Ms. Y. Yoshino of the Marine Ecology Research Institute Central Laboratory for rearing the rainbow trout.

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Authors and Affiliations

  1. Aquaculture Research Institute, Shingu Station, Kindai University, 1330 Takata, Shingu, Wakayama, 647-1101, Japan

    Toshinao Ineno

  2. Miyazaki Prefectural Fisheries Research Institute Freshwater Branch, Kobayashi, Miyazaki, 886-0005, Japan

    Toshinao Ineno, Koichi Tamaki, Kazuya Yamada & Ryusuke Kodama

  3. Marine Ecology Research Institute Central Laboratory, Onjuku, Chiba, 299-5105, Japan

    Shuji Tsuchida

  4. Laboratory of Aquatic Molecular Biology and Biotechnology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo, Tokyo, 113-8657, Japan

    Engkong Tan, Shigeharu Kinoshita, Shuichi Asakawa & Shugo Watabe

  5. Nikko Station, National Research Institute of Aquaculture, Fisheries Research Agency, Tochigi, 321-1661, Japan

    Koji Muto, Takashi Yada & Shoji Kitamura

  6. School of Marine Biosciences, Kitasato University, Sagamihara, Kanagawa, 252-0373, Japan

    Shugo Watabe

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  1. Toshinao Ineno
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  3. Kazuya Yamada
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  9. Takashi Yada
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  12. Shugo Watabe
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Correspondence to Toshinao Ineno.

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Ineno, T., Tamaki, K., Yamada, K. et al. Thermal tolerance of a thermally selected strain of rainbow trout Oncorhynchus mykiss and the pedigrees of its F1 and F2 generations indicated by their critical thermal maxima. Fish Sci 84, 671–679 (2018). https://doi.org/10.1007/s12562-018-1217-2

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