Environmental Biology of Fishes

, Volume 99, Issue 12, pp 975–981 | Cite as

Maternal effects in the inheritance of cold tolerance in blue tilapia (Oreochromis aureus)

  • Tali Nitzan
  • Tatiana Slosman
  • Dina Gutkovich
  • Joel I. Weller
  • Gideon Hulata
  • Tatyana Zak
  • Ayana Benet
  • Avner Cnaani
Article

Abstract

In accordance with their tropical origin, the optimal water temperature for most tilapia species is between 25 and 28 °C. The lethal temperature varies as a function of environmental effects, individual fish histories and genetic effects; however, the genetic basis of cold tolerance in tilapia has not been investigated in detail. Blue tilapia (Oreochromis aureus) is considered as one of the most cold-tolerant tilapia species, and, in this study, we have used a fish from a three-generation selective breeding program for enhanced cold tolerance. Four crosses within and between resistant and sensitive fish were used in this study. Forty families were challenged for cold tolerance, and a strong maternal effect was observed in two consecutive experiments. Expression patterns of the mitochondrial ATP6 gene were strongly correlated with cold tolerance; however, an analysis that applied an individual animal model restricted maximum likelihood on a three-generation pedigree, implies that an epigenetic effect rather than mitochondrial inheritance is the main source of the observed maternal effect. This study demonstrates that maternal effects can play a significant role in the inheritance of cold tolerance and that maternally-transferred genetic components should be targeted when adaptation to low temperature is studied in tilapia.

Keywords

Cichlidae Environmental stress Epigenetics Genetic imprinting Mitochondrial inheritance Temperature 

Notes

Acknowledgments

We would like to thank Ignacy Misztal for the use of the REML program. This research was supported by a grant from the Israeli Fish Breeders Association and by grant 863-0045 from the Chief Scientist of the Ministry of Agriculture and Rural Development.

References

  1. Battersby BJ, Moyes CD (1998) Influence of acclimation temperature on mitochondrial DNA, RNA, and enzymes in skeletal muscle. Am J Phys 275:R905–R912Google Scholar
  2. Behrends LL, Kingsley JB, Bulls MJ (1990) Cold tolerance in maternal mouthbrooding tilapias: phenotypic variation among species and hybrids. Aquaculture 85:271–280. doi: 10.1016/0044-8486(90)90026-J CrossRefGoogle Scholar
  3. Behrends LL, Kingsley JB, Bulls MJ (1996) Cold tolerance in maternal mouthbrooding tilapias: heritability estimates and correlated growth responses at suboptimal temperatures. In: Pullin RSV, Lazard J, Legendre M et al (eds) The third international symposium on tilapia in aquaculture. ICLARM, Manila, Philippines, pp. 257–265Google Scholar
  4. Charo-Karisa H, Rezk MA, Bovenhuis H (2004) Effects of rearing conditions on low-temperature tolerance of Nile tilapia, Oreochromis niloticus juveniles. In: Bolivar R, Mair GC, Fitzsimmons K (eds) The sixth international symposium on tilapia in aquaculture. ICLARM, Manila, Philippines, pp. 30–41Google Scholar
  5. Charo-Karisa H, Rezk MA, Bovenhuis H, Komen H (2005) Heritability of cold tolerance in Nile tilapia, Oreochromis niloticus, juveniles. Aquaculture 249:115–123CrossRefGoogle Scholar
  6. Chervinski J, Lahav M (1976) The effect of exposure to low temperature on fingerlings of local tilapia (Tilapia aurea)(Steindachner) and imported tilapia (Tilapia vulcani) (Trewavas) and Tilapia nilotica (Linne) in Israel. Isr J Aquac Bamidgeh 28:25–29Google Scholar
  7. Cnaani A, Gall GAE, Hulata G (2000) Cold tolerance of tilapia species and hybrids. Aquac Int 8:289–298CrossRefGoogle Scholar
  8. Cnaani A, Hallerman EM, Ron M et al (2003) Detection of a chromosomal region with two quantitative trait loci, affecting cold tolerance and fish size, in an F2 tilapia hybrid. Aquaculture 223:117–128. doi: 10.1016/S0044-8486(03)00163-7 CrossRefGoogle Scholar
  9. Dhillon RS, Schulte PM (2011) Intraspecific variation in the thermal plasticity of mitochondria in killifish. J Exp Biol 214:3639–3648. doi: 10.1242/jeb.057737 CrossRefPubMedGoogle Scholar
  10. El-Sayed AFM (2006) Tilapia culture. CABI Publishing, Preston, UK, 277 ppCrossRefGoogle Scholar
  11. Gracey AY, Fraser EJ, Li W et al (2004) Coping with cold: an integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. Proc Natl Acad Sci U S A 101:16970–16975. doi: 10.1073/pnas.0403627101 CrossRefPubMedPubMedCentralGoogle Scholar
  12. He A, Luo Y, Yang H et al (2011) Complete mitochondrial DNA sequences of the Nile tilapia (Oreochromis niloticus) and blue tilapia (Oreochromis aureus): genome characterization and phylogeny applications. Mol Biol Rep 38:2015–2021. doi: 10.1007/s11033-010-0324-7 CrossRefPubMedGoogle Scholar
  13. Henderson CR (1976) A simple method for computing the inverse of a numerator relationship matrix used in prediction of breeding values. Biometrics 32:69–83CrossRefGoogle Scholar
  14. Itoi S, Kinoshita S, Kikuchi K, Watabe S (2003) Changes of carp FoF1-ATPase in association with temperature acclimation. Am J Physiol Regul Integr Comp Physiol 284:R153–R163. doi: 10.1152/ajpregu.00182.2002 CrossRefPubMedGoogle Scholar
  15. Lucassen M, Koschnick N, Eckerle LG, Pörtner HO (2006) Mitochondrial mechanisms of cold adaptation in cod (Gadus morhua L.) populations from different climatic zones. J Exp Biol 209:2462–2471. doi: 10.1242/jeb.02268 CrossRefPubMedGoogle Scholar
  16. McCormick SD (1993) Methods for nonlethal gill biopsy and measurment of Na+, K+ − ATPase activity. Can J Fish Aquat Sci 50:656–658CrossRefGoogle Scholar
  17. O’Brien KM (2010) Mitochondrial biogenesis in cold-bodied fishes. J Exp Biol 214:275–285. doi: 10.1242/jeb.046854 CrossRefGoogle Scholar
  18. Schulte PM, Healy TM, Fangue NA (2011) Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integr Comp Biol 51:691–702. doi: 10.1093/icb/icr097 CrossRefPubMedGoogle Scholar
  19. Scott GR, Johnston IA (2012) Temperature during embryonic development has persistent effects on thermal acclimation capacity in zebrafish. Proc Natl Acad Sci U S A 109:14247–14252. doi: 10.1073/pnas.1205012109 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Sifa L, Chenhong L, Dey M et al (2002) Cold tolerance of three strains of Nile tilapia, Oreochromis niloticus, in China. Aquaculture 213:123–129. doi: 10.1016/S0044-8486(02)00068-6 CrossRefGoogle Scholar
  21. Starling SM, Bruckler RM, Strawn RK, Neill WH (1995) Predicting the lethality of fluctuating low temperatures to blue tilapia. Trans Am Fish Soc 124:112–117CrossRefGoogle Scholar
  22. Tave D, Jayaprakas V, Smitherman RO (1990) Effects of intraspecific hybridization in Tilapia nilotica on survival under ambient winter temperature in Alabama. J World Aquac Soc 21:201–209. doi: 10.1111/j.1749-7345.1990.tb01023.x CrossRefGoogle Scholar
  23. Thoa NP, Ninh NH, Hoa NT et al (2014) Additive genetic and heterotic effects in a 4 × 4 complete diallel cross-population of Nile tilapia (Oreochromis niloticus, Linnaeus, 1758) reared in different water temperature environments in northern Vietnam. Aquac Res. doi: 10.1111/are.12530 Google Scholar
  24. Thodesen J, Rye M, Wang YX et al (2013) Genetic improvement of tilapias in China: genetic parameters and selection responses in growth, pond survival and cold-water tolerance of blue tilapia (Oreochromis aureus) after four generations of multi-trait selection. Aquaculture 396-399:32–42CrossRefGoogle Scholar
  25. Trewavas E (1983) Tilapiine fishes of the genera Sarotherodon, Oreochromis and Danakilia. British Museum (Natural History), London, UK, 583 ppGoogle Scholar
  26. Velan A, Hulata G, Ron M, Cnaani A (2011) Comparative time-course study on pituitary and branchial response to salinity challenge in Mozambique tilapia (Oreochromis mossambicus) and Nile tilapia (O. niloticus). Fish Physiol Biochem 37:863–873. doi: 10.1007/s10695-011-9484-1 CrossRefPubMedGoogle Scholar
  27. Westell RA, Quaas RL, Van Vleck LD (1988) Genetic groups in an animal model. J Dairy Sci 71:1310–1318CrossRefGoogle Scholar
  28. Wohlfarth GW, Hulata G (1983) Applied genetics of tilapias. ICLARM Studies and Review 6, Manila, Philippines 26 ppGoogle Scholar
  29. Zak T, Deshev R, Benet-Perelberg A et al (2014) Genetic improvement of Israeli blue (Jordan) tilapia, Oreochromis aureus (Steindachner), through selective breeding for harvest weight. Aquac Res 45:546–557. doi: 10.1111/are.12072 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Institute of Animal ScienceAgricultural Research OrganizationRishon LetziyonIsrael
  2. 2.Ministry of Agriculture & Rural DevelopmentAquaculture Research Station - DorDorIsrael

Personalised recommendations