Abstract
Growth rate is an ecologically important trait, affecting the energy acquisition from, and provisioning to, the surrounding community. One of many costs suggested to counteract the evolution of increased intrinsic growth rate is an associated reduction in tolerance to conditions of nutrient stress. Here we test this concept with individuals possessing experimentally increased intrinsic growth rates (growth hormone transgenic coho salmon, Oncorhynchus kisutch) relative to wild genotypes. Using a series of three experiments, survival and growth of both genotypes were assessed on a physiological and behavioral level while varying food abundance, social interactions, and predation risk. Only in complete absence of exogenous food in newly emerged fry did the high intrinsic growth rate appear costly with a shorter average survival time compared to wild-type (Exp. 1). In experiment 2, genotypes with elevated intrinsic growth showed equal or higher survival and growth than wild-type genotypes In a third experiment, adding very limited amounts of food and allowing for social interactions in a simulated natural environment benefited transgenic individuals relative to wild-types, but at similar magnitudes in both the absence and presence of predators. Populations with transgenic individuals present did not crash under these competitive conditions as previously reported when studied in simple environments where hiding and attack escape were not possible. Our data suggest that transgenic fish have a greater scope for growth under most conditions, but are not obligated to use this capability. Physiological (e.g. appetite and conversion efficiency) and behavioral traits (e.g. competitive ability and risk-taking) found previously to correlate positively with intrinsic growth rate in the transgenic strain likely aided in their survival and growth, even under food limited conditions. Hence, at least in coho salmon, intrinsic growth rate does not appear to strongly affect survival under nutrient stress.
Similar content being viewed by others
References
Ali M, Nicieza AG, Wootton RJ (2003) Compensatory growth in fishes: a response to growth depression. Fish Fish 4:147–190
Arendt JD (1997) Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol 72:149–177
Arendt J, Wilson DS, Stark E (2001) Scale strength as a cost of rapid growth in sunfish. Oikos 93:95–100
Biro PA, Abrahams MV, Post JR et al (2004a) Predators select against high growth rates and risk-taking behaviour in domestic trout populations. Proc Roy Soc B Biol Sci 271:2233–2237
Biro PA, Morton AE, Post JR et al (2004b) Over-winter lipid depletion and mortality of age-0 rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 61:1513–1519
Björnsson BT (1997) The biology of salmon growth hormone: from daylight to dominance. Fish Physiol Biochem 17:9–24
Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Q Rev Biol 75:385–407
Buttery PJ, Dawson JM (1990) Growth promotion in farm animals. Proc Nutr Soc 49:459–466
Byström P, Andersson J, Kiessling A et al (2006) Size and temperature dependent foraging capacities and metabolism: consequences for winter starvation mortality in fish. Oikos 115:43
Case TJ (1978) On the evolution and adaptive significance of postnatal growth rates in the terrestrial vertebrates. Q Rev Biol 53:243–282
Clutton-Brock TH, Albon SD, Guinness FE (1985) Parental investment and sex differences in juvenile mortality in birds and mammals. Nature 313:131–133
Conover DO, Present TMC (1990) Countergradient variation in growth rate: compensation for length of the growing season among Atlantic silversides from different latitudes. Oecologia 83:316–324
Day T, Rowe L (2002) Developmental thresholds and the evolution of reaction norms for age and size at life-history transitions. Am Natur 159:338–350
Devlin RH, Yesaki TY, Biagi CA et al (1994) Extraordinary salmon growth. Nature 371:209–210
Devlin RH, Yesaki TY, Donaldson EM et al (1995) Transmission and phenotypic effects of an antifreeze GH gene construct in coho salmon (Oncorhynchus kisutch). Aquaculture 137:161–169
Devlin RH, Johnsson JI, Smailus DE et al (1999) Increased ability to compete for food by growth hormone-transgenic coho salmon Oncorhynchus kisutch (Walbaum). Aquacult Res 30:479–482
Devlin RH, Biagi CA, Yesaki TY et al (2001) Growth of domesticated transgenic fish. Nature 409:781–782
Devlin RH, Biagi CA, Yesaki TY (2004a) Growth, viability and genetic characteristics of GH transgenic coho salmon strains. Aquaculture 236:607–632
Devlin RH, D’Andrade M, Uh M et al (2004b) Population effects of growth hormone transgenic coho salmon depend on food availability and genotype by environment interactions. Proc Natl Acad Sci USA 101:9303–9308
Devlin RH, Sakhrani D, Tymchuk WE et al (2009) Domestication and growth hormone transgenesis cause similar changes in gene expression profiles in salmon. Proc Natl Acad Sci 106:3047–3052
Donaldson EM, Fagerlund UHM, Higgs DA et al (1979) Hormonal enhancement of growth. In: Hoar WS, Randall DJ, Brett WS (eds) Fish physiology: bioenergetics and growth. Academic Press, New York, pp 455–597
Einum S, Fleming IA (2000) Selection against late emergence and small offspring in Atlantic salmon (Salmo salar). Evolution 54:628–639
Gotthard K (2001) Growth strategies of ectothermic animals in temperate environments. In: Atkinson D, Thorndyke M (eds) Environment and animal development. BIOS Scientific, Oxford, pp 287–304
Gotthard K, Nylin S, Wiklund C (1994) Adaptive variation in growth rate: life history costs and consequences in the speckled wood butterfly, Pararge aegeria. Oecologia 99:281–289
Grant PR, Grant BR (2002) Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296:707–711
Grant J, Kramer D (1990) Territory size as a predictor of the upper limit to population density of juvenile salmonids in streams. Can J Fish Aquat Sci 47:1724–1737
Havenstein G, Ferket P, Qureshi M (2003) Growth, livability, and feed conversion of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poult Sci 82:1500–1508
Hetzel DJS, Crocos PJ, Davis GP et al (2000) Response to selection and heritability for growth in the Kuruma prawn, Penaeus japonicus. Aquaculture 181:215–223
Hill JA, Kiessling A, Devlin RH (2000) Coho salmon (Oncorhynchus kisutch) transgenic for a growth hormone gene construct exhibit increased rates of muscle hyperplasia and detectable levels of differential gene expression. Can J Fish Aquat Sci 57:939–950
Huang H, Brown DD (2000) Overexpression of Xenopus laevis growth hormone stimulates growth of tadpoles and frogs. Proc Natl Acad Sci USA 97:190–194
Leggatt RA, Devlin RH, Farrell AP et al (2003) Oxygen uptake of growth hormone transgenic coho salmon during starvation and feeding. J Fish Biol 62:1053–1066
Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation—a review and prospectus. Can J Zool 68:619–640
Lindstedt SL, Boyce MS (1985) Seasonality, fasting endurance, and body size in mammals. Am Natur 125:873–878
McCue MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol Part A Mol Integr Physiol 156:1–18
Metcalfe NB, Monaghan P (2003) Growth versus lifespan: perspectives from evolutionary ecology. Exp Gerontol 38:935–940
Owen M, Black JM (1989) Factors affecting the survival of barnacle geese on migration from the breeding grounds. J Anim Ecol 58:603–617
Priyadarshana T, Asaeda T, Manatunge J (2006) Hunger-induced foraging behavior of two cyprinid fish: Pseudorasbora parva and Rasbora daniconius. Hydrobiologia 568:341–352
Rauw WM, Kanis E, Noordhuizen-Stassen EN et al (1998) Undesirable side effects of selection for high production efficiency in farm animals: a review. Livest Prod Sci 56:15–33
Raven PA, Devlin RH, Higgs DA (2006) Influence of dietary digestible energy content on growth, protein and energy utilization and body composition of growth hormone transgenic and non-transgenic coho salmon (Oncorhynchus kisutch). Aquaculture 254:730–747
Schluter D, Price TD, Rowe L (1991) Conflicting selection pressures and life history trade-offs. Proc Roy Soc B Biol Sci 246:11–17
Smith RJ (2002) Effect of larval body size on overwinter survival and emerging adult size in the burying beetle, Nicrophorus investigator. Can J Zool 80:1588–1593
Sogard SM (1997) Size-selective mortality in the juvenile stage of teleost fishes: a review. Bull Mar Sci 60:1129–1157
Speakman JR, Hambly C (2007) Starving for life: what animal studies can and cannot tell us about the use of caloric restriction to prolong human lifespan. J Nutr 137:1078–1086
Sundström LF, Lõhmus M, Johnsson JI et al (2004) Growth hormone transgenic salmon pay for growth potential with increased predation mortality. Proc Roy Soc B Biol Sci 271:S350–S352
Sundström LF, Lõhmus M, Devlin RH (2005) Selection on increased intrinsic growth rates in coho salmon Oncorhynchus kisutch. Evolution 59:1560–1569
Sundström LF, Lõhmus M, Johnsson JI et al (2007a) Dispersal potential is affected by growth-hormone transgenesis in coho salmon (Oncorhynchus kisutch). Ethology 113:403–410
Sundström LF, Lõhmus M, Tymchuk WE et al (2007b) Gene-environment interactions influence ecological consequences of transgenic animals. Proc Natl Acad Sci USA 104:3889–3894
Tymchuk WE, Devlin RH (2005) Growth differences among first and second generation hybrids of domesticated and wild rainbow trout (Oncorhynchus mykiss). Aquaculture 245:295–300
Tymchuk WEV, Abrahams MV, Devlin RH (2005) Competitive ability and mortality of growth-enhanced transgenic coho salmon fry and presmolts when foraging for food. Trans Am Fish Soc 134:381–389
Van Buskirk J (2001) Specific induced responses to different predator species in anuran larvae. J Evol Biol 14:482–489
Webb EC, Casey NH (2010) Physiological limits to growth and the related effects on meat quality. Livestock Science (in press, Corrected Proof)
Wilson PN, Osbourn DF (1960) Compensatory growth after undernutrition in mammals and birds. Biol Rev 35:324–361
Acknowledgments
Thanks to Henry Kwok, Nicole Hofs, Benjamin Goh, Morgan Williams, Ki-Whan Eom, Mare Lõhmus, Geoff Harrison, Wendy Tymchuk, and Carlo Biagi for assistance during parts of the experiments. The work was carried out with financial support from the Canadian Regulatory System for Biotechnology (RHD). LFS was funded by a post-doctoral grant from the Swedish Research Council FORMAS and as a Marie Curie Outgoing International Fellowship under contract MOIF-CT-2005-8141 from the European Community’s Sixth Framework Programme. The present work does not necessarily reflect the Community’s views and in no way anticipates its future policy in this area.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sundström, L.F., Devlin, R.H. Increased intrinsic growth rate is advantageous even under ecologically stressful conditions in coho salmon (Oncorhynchus kisutch). Evol Ecol 25, 447–460 (2011). https://doi.org/10.1007/s10682-010-9406-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-010-9406-1