Parental identity influences progeny responses to incubation thermal stress in sockeye salmon Onchorhynchus nerka

Journal of Fish Biology

Volumn 80, Issue 2, 2012, Pages 444-462

  Burt, J M ^a   Hinch, S G ^a   Patterson, D A ^b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b SIMON FRASER UNIVERSITY   (Canada)

Author keywords

Early life history; Family effects; Maternal; Paternal; Reaction norm; Temperature

Indexed keywords

ANIMAL; ARTICLE; BODY SIZE; CANADA; ENVIRONMENT; FEMALE; LARVA; MALE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SALMON; TEMPERATURE;

ANIMALS; BODY SIZE; BRITISH COLUMBIA; ENVIRONMENT; FEMALE; LARVA; MALE; SALMON; STRESS, PHYSIOLOGICAL; TEMPERATURE;

ONCORHYNCHUS; ONCORHYNCHUS NERKA; SALMONIDAE;

EID: 84856208992     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2011.03190.x     Document Type: Article

References (79)

1. Angilletta, M. J., Steel, E. A., Bartz, K. K., Kingsolver, J. G., Scheuerell, M. D., Beckman, B. R. & Crozier, L. G. (2008). Big dams and salmon evolution: changes in thermal regimes and their potential evolutionary consequences. Evolutionary Applications 1, 286-299.
2. Beacham, T. D. (1988). A genetic analysis of early development in pink (Oncorhynchus gorbuscha) and chum salmon (Oncorhynchus keta) at three different temperatures. Genome 30, 89-96.
3. Beacham, T. D. & Murray, C. B. (1985). Effect of female size, egg size, and water temperature on developmental biology of chum salmon (Oncorhynchus keta) from the Nitinat River, British Columbia. Canadian Journal of Fisheries and Aquatic Sciences 42, 1755-1765.
4. Beacham, T. D. & Murray, C. B. (1986). Comparative developmental biology of chum salmon (Oncorhynchus keta) from the Fraser River, British Columbia. Canadian Journal of Fisheries and Aquatic Sciences 43, 252-262.
5. Beacham, T. D. & Murray, C. B. (1987). Effects of transferring pink (Oncorhynchus gorbuscha) and chum (Oncorhynchus keta) salmon embryos at different developmental stages to a low incubation temperature. Canadian Journal of Zoology 65, 96-105.
6. Beacham, T. D. & Murray, C. B. (1988). Variation in developmental biology of pink salmon (Oncorhynchus gorbuscha) in British Columbia. Canadian Journal of Zoology 66, 2634-2648.
7. Beacham, T. D. & Murray, C. B. (1989). Variation in developmental biology of sockeye salmon (Oncorhynchus nerka) and Chinook salmon (Oncorhynchus tshawytscha) in British Columbia. Canadian Journal of Zoology 67, 2081-2089.
8. Beacham, T. D. & Murray, C. B. (1990). Temperature, egg size, and development of embryos and alevins of five species of Pacific salmon: a comparative analysis. Transactions of the American Fisheries Society 119, 927-944.
9. Beacham, T. D. & Varnavskaya, N. V. (1991). Effect of parental heterozygosity on pink salmon (Oncorhynchus gorbuscha) embryonic and alevin survival and development at extreme temperatures. Canadian Journal of Zoology 69, 2485-2489.
10. Beacham, T. D., Candy, J. R., McIntosh, B., MacConnachie, C., Tabata, A., Kaukinen, K., Deng, L. T., Miller, K. M., Withler, R. E. & Varnavskaya, N. (2005). Estimation of stock composition and individual identification of sockeye salmon on a Pacific Rim basis using microsatellite and major histocompatibility complex variation. Transactions of the American Fisheries Society 134, 1124-1146.
11. Beckman, B. R., Gadberry, B., Parkins, P. & Larsen, D. A. (2008). The effect of Yakima River spring Chinook salmon sire life history type on emergence timing and size of progeny. Transactions of the American Fisheries Society 137, 1285-1291.
12. Benoit, H. P. & Pepin, P. (1999). Interaction of rearing temperature and maternal influence on egg development rates and larval size at hatch in yellowtail flounder (Pleuronectes ferrugineus). Canadian Journal of Fisheries and Aquatic Sciences 56, 785-794.
13. Blaxter, J. H. (1992). The effect of temperature on larval fishes. Netherlands Journal of Zoology 42, 336-357.
14. Burt, J. B. (2011). Influences of parental identity and elevated incubation temperature on the survival, development and early life history traits in sockeye salmon. MSc Thesis, University of British Columbia, Vancouver, BC.
15. Burt, J. B., Hinch, S. & Patterson, D. A. (2011). The importance of parentage in assessing temperature effects on fish early life history: a review of the experimental literature. Reviews in Fish Biology and Fisheries 21, 377-406.
16. Campbell, P. M., Pottinger, T. G. & Sumpter, J. P. (1992). Stress reduces the quality of gametes produced by rainbow trout. Biology of Reproduction 47, 1140-1150.
17. Combs, B. D. (1965). Effect of temperature on the development of salmon eggs. Progressive Fish- Culturist 27, 134-137.
18. Crozier, L. G., Hendry, A. P., Lawson, P. W., Quinn, T. P., Mantua, N. J., Battin, J., Shaw, R. G. & Huey, R. B. (2008). Potential responses to climate change in organisms with complex life histories: evolution and plasticity in Pacific salmon. Evolutionary Applications 1, 252-270.
19. Donelson, J. M., Munday, P. L. & McCormick, M. I. (2009). Parental effects on offspring life histories: when are they important? Biology Letters 5, 262-265.
20. Eilertsen, E. M., Bardsen, B. J., Liljedal, S., Rudolfsen, G. & Folstad, I. (2009). Experimental evidence for paternal effects on offspring growth rate in Arctic charr (Salvelinus alpinus). Proceedings of the Royal Society B 276, 129-136.
21. Einum, S. & Fleming, I. A. (1999). Maternal effects of egg size in brown trout (Salmo trutta): norms of reaction to environmental quality. Proceedings of the Royal Society B 266, 2095-2100.
22. Eriksen, M. S., Bakken, M., Espmark, A., Braastad, B. O. & Salte, R. (2006). Prespawning stress in farmed Atlantic salmon Salmo salar: maternal cortisol exposure and hyperthermia during embryonic development affect offspring survival, growth and incidence of malformations. Journal of Fish Biology 69, 114-129.
23. Fox, C. W. & Mousseau, T. A. (1996). Larval host plant affects fitness consequences of egg size variation in the seed beetle Stator limbatus. Oecologia 107, 541-548.
24. Gagliano, M. & McCormick, M. I. (2009). Hormonally mediated maternal effects shape offspring survival potential in stressful environments. Oecologia 160, 657-665.
25. Garant, D., Fontaine, P. M., Good, S. P., Dodson, J. J. & Bernatchez, L. (2002). The influence of male parental identity on growth and survival of offspring in Atlantic salmon (Salmo salar). Evolutionary Ecology Research 4, 537-549.
26. Green, B. S. (2008). Maternal effects in fish populations. In Advances in Marine Biology (Sims, D. W., ed.), pp. 1-105. San Diego, CA: Academic Press.
27. Groot, C. & Margolis, L. (1991). Pacific Salmon Life Histories. Vancouver, BC: UBC Press.
28. Gunnes, K. (1979). Survival and development of Atlantic salmon eggs and fry at 3 different temperatures. Aquaculture 16, 211-218.
29. Hague, M. J., Ferrari, M. R., Miller, J. R., Patterson, D. A., Russell, G. L., Farrell, A. P. & Hinch, S. (2011). Modelling the future hydroclimatology of the lower Fraser River and its impacts on the spawning migration survival of sockeye salmon. Global Change Biology 17, 87-98.
30. Hard, J. J. (1995). A quantitative genetic perspective on the conservation of intraspecific diversity. In Evolution and the Aquatic Ecosystem: Defining Unique Units in Population Conservation (Nielsen, J. L., ed.), pp. 304-326. Bethesda, MD: American Fisheries Society.
31. Haugen, T. O. & Vollestad, L. A. (2000). Population differences in early life-history traits in grayling. Journal of Evolutionary Biology 13, 897-905.
32. Heath, D. D., Bernier, N. J., Heath, J. W. & Iwama, G. K. (1993). Genetic, environmental, and interaction effects on growth and stress response of Chinook salmon (Oncorhynchus tshawytscha) fry. Canadian Journal of Fisheries and Aquatic Sciences 50, 435-442.
33. Heath, D. D., Fox, C. W. & Heath, J. W. (1999). Maternal effects on offspring size: variation through early development of Chinook salmon. Evolution 53, 1605-1611.
34. Hebert, K. P., Goddard, P. L., Smoker, W. W. & Gharrett, A. J. (1998). Quantitative genetic variation and genotype by environment interaction of embryo development rate in pink salmon (Oncorhynchus gorbuscha). Canadian Journal of Fisheries and Aquatic Sciences 55, 2048-2057.
35. Hendry, A. P., Hensleigh, J. E. & Reisenbichler, R. R. (1998). Incubation temperature, developmental biology, and the divergence of sockeye salmon (Oncorhynchus nerka) within Lake Washington. Canadian Journal of Fisheries and Aquatic Sciences 55, 1387-1394.
36. Hoffmann, A. A. & Parsons, P. A. (1991). Evolutionary Genetics and Environmental Stress. Oxford: Oxford University Press.
37. Hoie, H., Folkvord, A. & Johannessen, A. (1999). The influence of different parental combinations and incubation temperature on the RNA and DNA content of herring larvae at hatching: a pilot study. Journal of Fish Biology 55, 110-118.
38. Humpesch, U. H. (1985). Inter- and intra-specific variation in hatching success and embryonic development of five species of salmonids and Thymallus thymallus. Archiv für Hydrobiologie 104, 129-144.
39. Hutchings, J. A. (1991). Fitness consequences of variation in egg size and food abundance in brook trout Salvelinus fontinalis. Evolution 45, 1162-1168.
40. Hutchings, J. A. (2004). Norms of reaction and phenotypic plasticity in salmonid life history. In Evolution Illuminated: Salmon and Their Relatives (Hendry, A. P., ed.), pp. 154-175. New York, NY: Oxford University Press.
41. Hutchings, J. A. (2011). Old wine in new bottles: reaction norms in salmonid fishes. Heredity 106, 421-437.
42. Hutchings, J. A., Swain, D. P., Rowe, S., Eddington, J. D., Puvanendran, V. & Brown, J. A. (2007). Genetic variation in life-history reaction norms in a marine fish. Proceedings of the Royal Society B 274, 1693-1699.
43. Huuskonen, H., Penttinen, O. & Piironen, J. (2003). Effects of temperature and parental background on the embryonic survival and metabolic rate of newly hatched Arctic charr. In The Big Fish Bang: Proceedings of the 26th Annual Larval Fish Conference (Browman, H. I. & Skiftesvik, A. B., eds), pp. 35-44. Bergen: Institute of Marine Research.
44. Janhunen, M., Piironen, J. & Peuhkuri, N. (2010). Parental effects on embryonic viability and growth in Arctic charr Salvelinus alpinus at two incubation temperatures. Journal of Fish Biology 76, 2558-2570.
45. Jensen, L. F., Hansen, M. M., Pertoldi, C., Holdensgaard, G., Mensberg, K. L. D. & Loeschcke, V. (2008). Local adaptation in brown trout early life-history traits: implications for climate change adaptability. Proceedings of the Royal Society B 275, 2859-2868.
46. Johnston, I. A. (2006). Environment and plasticity of myogenesis in teleost fish. Journal of Experimental Biology 209, 2249-2264.
47. Johnston, I. A. & McLay, H. A. (1997). Temperature and family effects on muscle cellularity at hatch and first feeding in Atlantic salmon (Salmo salar L). Canadian Journal of Zoology 75, 64-74.
48. Kamler, E. (2005). Parent-egg-progeny relationships in teleost fishes: an energetics perspective. Reviews in Fish Biology and Fisheries 15, 399-421.
49. Kamler, E. (2008). Resource allocation in yolk-feeding fish. Reviews in Fish Biology and Fisheries 18, 143-200.
50. Macqueen, D. J., Robb, D. H. F., Olsen, T., Melstveit, L., Paxton, C. G. M. & Johnston, I. A. (2008). Temperature until the 'eyed stage' of embryogenesis programmes the growth trajectory and muscle phenotype of adult Atlantic salmon. Biology Letters 4, 294-298.
51. Marshall, D. J., Allen, R. M. & Crean, A. J. (2008). The ecological and evolutionary importance of maternal effects in the sea. In Oceanography and Marine Biology: An Annual Review (Gibson, R. N., Atkinson, R. J. A. & Gordon, J. D. M., eds), pp. 203-250. Boca Raton, FL: CRC Press.
52. Martell, D. J. & Kieffer, J. D. (2007). Persistent effects of incubation temperature on muscle development in larval haddock (Melanogrammus aeglefinus L.). Journal of Experimental Biology 210, 1170-1182.
53. Martell, D. J., Kieffer, J. D. & Trippel, E. A. (2005). Effects of temperature during early life history on embryonic and larval development and growth in haddock. Journal of Fish Biology 66, 1558-1575.
54. McCullough, D., Spalding, S., Sturdevant, D. & Hicks, M. (2001). Summary of technical literature examining the physiological effects of temperature on salmonids. Environmental Protection Agency Issue Paper 5 EPA-910-D-01-005. 1-113.
55. Morasse, S., Guderley, H. & Dodson, J. J. (2008). Paternal reproductive strategy influences metabolic capacities and muscle development of Atlantic salmon (Salmo salar L.) embryos. Physiological and Biochemical Zoology 81, 402-413.
56. Mousseau, T. A. & Fox, C. W. (1998). The Adaptive Significance of Maternal Effects. New York, NY: Oxford University Press.
57. Murray, C. B. & Beacham, T. D. (1986). Effect of varying temperature regimes on the development of pink salmon (Oncorhynchus gorbuscha) eggs and alevins. Canadian Journal of Zoology 64, 670-676.
58. Murray, C. B. & Beacham, T. D. (1987). The development of Chinook (Oncorhynchus tshawytscha) and chum salmon (Oncorhynchus keta) embryos and alevins under varying temperature regimes. Canadian Journal of Zoology 65, 2672-2681.
59. Murray, C. B. & McPhail, J. D. (1988). Effect of incubation temperature on the development of five species of Pacific salmon (Oncorhynchus) embryos and alevins. Canadian Journal of Zoology 66, 266-273.
60. Murray, C. B., Beacham, T. D. & McPhail, J. D. (1990). Influence of parental stock and incubation temperature on the early development of coho salmon (Oncorhynchus kisutch) in British Columbia. Canadian Journal of Zoology 68, 347-358.
61. Nadeau, P. S., Hinch, S. G., Pon, L. B. & Patterson, D. A. (2009). Persistent parental effects on the survival and size, but not burst swimming performance of juvenile sockeye salmon (Oncorhynchus nerka). Journal of Fish Biology 75, 538-551.
62. Nagler, J. J., Parsons, J. E. & Cloud, J. G. (2000). Single pair mating indicates maternal effects on embryo survival in rainbow trout, Oncorhynchus mykiss. Aquaculture 184, 177-183.
63. Pakkasmaa, S., Penttinen, O. P. & Piironen, J. (2006). Metabolic rate of Arctic charr eggs depends on their parentage. Journal of Comparative Physiology B 176, 387-391.
64. Parichy, D. M. & Kaplan, R. H. (1992). Maternal effects on offspring growth and development depend on environmental quality in the frog Bombina orientalis. Oecologia 91, 579-586.
65. Patterson, D. A., Guderley, H., Bouchard, P., Macdonald, J. S. & Farrell, A. P. (2004). Maternal influence and population differences in activities of mitochondrial and glycolytic enzymes in emergent sockeye salmon (Oncorhynchus nerka) fry. Canadian Journal of Fisheries and Aquatic Sciences 61, 1225-1234.
66. Pitcher, T. E. & Neff, B. D. (2007). Genetic quality and offspring performance in Chinook salmon: implications for supportive breeding. Conservation Genetics 8, 607-616.
67. Purchase, C. F., Butts, I. A. E., Alfonso-Fernandez, A. & Trippel, E. A. (2010). Thermal reaction norms in sperm performance of Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 67, 498-510.
68. Rasanen, K. & Kruuk, L. E. B. (2007). Maternal effects and evolution at ecological time-scales. Functional Ecology 21, 408-421.
69. Rombough, P. J. (1985). Initial egg weight, time to maximum alevin wet weight, and optimal ponding times for Chinook salmon (Oncorhynchus tshawytscha). Canadian Journal of Fisheries and Aquatic Sciences 42, 287-291.
70. Rossiter, M. C. (1998). The role of environmental variation in parental effects expression. In Maternal Effects as Adaptations (Mousseau, T. A. & Fox, C. J., eds), pp. 112-134. New York, NY: Oxford University Press.
71. Rudolfsen, G., Figenschou, L., Folstad, I., Nordeide, J. T. & Soreng, E. (2005). Potential fitness benefits from mate selection in the Atlantic cod (Gadus morhua). Journal of Evolutionary Biology 18, 172-179.
72. Rutherford, S. L. (2000). From genotype to phenotype: buffering mechanisms and the storage of genetic information. Bioessays 22, 1095-1105.
73. Rutherford, S. L. & Lindquist, S. (1998). Hsp90 as a capacitor for morphological evolution. Nature 396, 336-342.
74. Schlichting, C. D. & Pigliucci, M. (1998). Phenotypic Evolution: A Reaction Norm Perspective. Sunderland, MA: Sinauer Associates Inc.
75. Takle, H., Baeverfjord, G. & Andersen, O. (2004). Identification of stress sensitive genes in hyperthermic Atlantic salmon (Salmo salar) embryos by RAP-PCR. Fish Physiology and Biochemistry 30, 275-281.
76. Turner, M. A., Viant, M. R., Teh, S. J. & Johnson, M. L. (2007). Developmental rates, structural asymmetry, and metabolic fingerprints of steelhead trout (Oncorhynchus mykiss) eggs incubated at two temperatures. Fish Physiology and Biochemistry 33, 59-72.
77. Wargelius, A., Fjelldal, P. G. & Hansen, T. (2005). Heat shock during early somitogenesis induces caudal vertebral column defects in Atlantic salmon (Salmo salar). Development Genes and Evolution 215, 350-357.
78. Wedekind, C., Evanno, G., Urbach, D., Jacob, A. & Muller, R. (2008). 'Good-genes' and 'compatible-genes' effects in an Alpine whitefish and the information content of breeding tubercles over the course of the spawning season. Genetica 134, 21-30.
79. Willmore, K. E. & Hallgrimsson, B. (2005). Within individual variation: developmental noise versus developmental stability. In Variation: A Central Concept in Biology (Hallgrimsson, B. & Hall, B. K., eds), pp. 191-218. London: Elsevier Academic Press.