Abstract
Selective mortality within a population, based on the phenotype of individuals, is the foundation of the theory of natural selection. We examined temperature-induced shifts in the relationships among early life history traits and survivorship over the embryonic and larval stages of a tropical damselfish, Pomacentrus amboinensis. Our experiments show that temperature determines the intensity of selective mortality, and that this changes with ontogeny. The size of energy stores determined survival through to hatching, after which egg size became a good indicator of fitness as predicted by theoretical models. Yet, the benefits associated with egg size were not uniform among test temperatures. Initial egg size positively influenced larval survival at control temperature (29 °C). However, this embryonic trait had no effect on post-hatching longevity of individuals reared at the higher (31 °C) and lower (25 °C) end of the temperature range. Overall, our findings indicate that the outcome of selective mortality is strongly dependent on the interaction between environment conditions and intrinsic developmental schedules.
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References
Bernardo J (1996) The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretation. Am Zool 36:216–236
Blaxter JHS (1988) Pattern and variety in development. In: Hoar WS, Randall DJ (eds) Fish physiology. Academic, New York, 11A:1–58
Bradford MJ, Cabana G (1997) Interannual variability in stage-specific survival rates and the causes of recruitment variation. In: Chambers RC, Trippel EA (eds) Early life history and recruitment in fish populations. Chapman & Hall, London, pp 469–493
Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789
Chambers RC, Leggett WC, Brown JA (1989) Egg size, female effects, and the correlation between early life history traits of capelin, Mallotus villosus: an appraisal at the individual level. Fish Bull 87:515–523
Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton, NJ
Collins LA, Nelson SG (1993) Effects of temperature on oxygen consumption, growth, and development of embryos and yolk-sac larvae of Siganus randalli (Pisces: Siganidae). Mar Biol 117:195–204
Cushing DH, Horwood JW (1994) The growth and death of fish larvae. J Plankton Res 16:291–300
Ehrlich KF, Muszynski G (1982) Effects of temperature on interactions of physiological and behavioural capacities of larval Californian grunion: adaptations to the planktonic environment. J Exp Mar Biol Ecol 60:223–244
Einum S, Fleming IA (1999) Maternal effects of egg size in brown trout (Salmo trutta): norms of reaction to environmental quality. Proc R Soc Lond B 266:2095–2100
Einum S, Fleming IA (2000) Highly fecund mothers sacrifice offspring survival to maximize fitness. Nature 405:565–567
Einum S, Fleming IA (2002) Egg-size evolution in aquatic environments: does oxygen availability constrain size. Proc R Soc Lond B 269:2325–2330
Fuiman LA, Higgs DM (1997) Ontogeny, growth and the recruitment process. In: Chambers CR, Trippel EA (eds) Early life history and recruitment in fish populations. Chapman & Hall, London, pp 225–249
Gagliano M, McCormick MI (2007) Maternal condition influences phenotypic selection on offspring. J Anim Ecol 76(1):174–182
Green BS, Fisher R (2004) Temperature influences whether bigger is really better? J Exp Mar Biol Ecol 299:115–132
Green BS, McCormick MI (2005) O2 replenishment to fish nests: males adjust brood care to ambient conditions and brood development. Behav Ecol 16:389–397
Heming TA, Buddington, RK (1988) Yolk absorption in embryonic and larval fishes. In: Hoar WS, Randall DJ (eds) Fish physiology. Academic, New York, 11A:407–446
Hendry AP, Day T, Cooper AB (2001) Optimal size and number of propagules: allowance for discrete stages and effect of maternal size on reproductive output and offspring fitness. Am Nat 157:387–407
Houde ED (1987) Fish early life dynamics and recruitment. Am Fish Soc Symp 2:17–29
Houde ED (1989) Comparative growth, mortality and energetics of marine fish larvae: temperature and implied latitudinal effects. Fish Bull 87:471–495
Hutchings JA (1991) Fitness consequences of variation in egg size and food abundance in brook trout Salvelinus fontinalis. Evolution 45:1162–1168
Johnston IA, Bennett AF (1996) Animals and temperature; phenotypic and evolutionary adaptation. Cambridge University Press, Cambridge, UK
Johnston TA, Leggett WC (2002) Maternal and environmental gradients in the egg size of an iteroparous fish. Ecology 83:1777–1791
Kamler E (2002) Ontogeny of yolk-feeding fish: an ecological perspective. Rev Fish Biol Fish 12:79–103
Kerrigan BA (1997) Variability in larval development of the tropical reef fish Pomacentrus amboinensis (Pomacentridae): the parental legacy. Mar Biol 127:395–402
Klinkhardt MB, Straganov AA, Pavlov DA (1987) Motoricity of Atlantic salmon embryos (Salmo salar L.) at different temperatures. Aquaculture 64:219–236
Kolm N, Ahnesjö I (2005) Do egg size and parental care coevolve in fishes? J Fish Biol 66:1499–1515
Koumoundouros G, Divanach P, Anezaki L (2001) Temperature-induced ontogenetic plasticity in sea bass (Dicentrarchus labrax). Mar Biol 139:817–830
Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226
Lankford TE Jr, Billerbeck JM, Conover DO (2001) Evolution of intrinsic growth and energy acquisition rates. II. Trade-offs with vulnerability to predation in Menidia menidia. Evolution 55:1873–1881
Leggett WC, DeBlois EM (1994) Recruitment in marine fishes: is it regulated by starvation and predation in the egg and larval stages? Neth J Sea Res 32:119–134
Litvak MK, Leggett WC (1992) Age and size-selective predation on larval fishes: the bigger is better paradigm revisited. Mar Ecol Prog Ser 81:13–24
Lynch M, Gabriel W (1987) Environmental tolerance. Am Nat 129:283–303
McCormick MI (1999) Experimental test of the effect of maternal hormones on larval quality of a coral reef fish. Oecologia 118:412–422
McCormick MI, Nechaev I (2002) Influence of cortisol on developmental rhythms during embryogenesis in a tropical damselfish. J Exp Zool 293:456–466
McGurk MD (1986) Natural mortality of marine fish eggs and larvae: role of spatial patchiness. Mar Ecol Prog Ser 34:227–242
Metcalfe NB, Taylor AC, Thorpe JE (1995) Metabolic rate, social status and life-history strategies in Atlantic salmon. Anim Behav 49:431–436
Miller TJ, Crower LB, Rice JA, Marshall EA (1988) Larval size and recruitment mechanisms in fishes: toward a conceptual framework. Can J Fish Aquat Sci 45:1657–1670
Mousseau TA, Fox CW (1998) Maternal effects as adaptations. Oxford University Press, New York
Norry FM, Loeschcke V (2002) Temperature-induced shifts in associations of longevity with body size in Drosophila melanogaster. Evolution 56:299–306
Payne AG, Smith C, Campbell AC (2002) Filial cannibalism improves survival and development of beaugregory damselfish embryos. Proc R Soc Lond B 269:2095–2102
Pepin P, Myers RA (1991) Significance of egg and larval size to recruitment variability of temperate marine fish. Can J Fish Aquat Sci 48:1820–1828
Pepin P, Miller TJ (1993) Potential use and abuse of general empirical models of early life history processes in fish. Can J Fish Aquat Sci 50:1343–1345
Philippi T, Seger J (1989) Hedging one’s evolutionary bets, revisited. Trends Ecol Evol 4:41–44
Priede IG (1985) Metabolic scope in fishes. In: Tyler P, Calow P (eds) Fish energetics: new perspectives. Croom Helm, London, pp 33–64
Roff DA (1992) The evolution of life histories; theory and analysis. Chapman & Hall, New York
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford, UK
Stillwell RC, Fox CW (2005) Complex patterns of phenotypic plasticity: interactive effects of temperature during rearing and oviposition. Ecology 86:924–934
Yamagami K (1988) Mechanisms of hatching in fish. In: Hoar WS, Randall DJ (eds) Fish physiology. Academic, New York, 11A:447–499
Acknowledgments
We thank Vanessa Messmer and the staff at Lizard Island Research Station for assistance with the experiment, and Chris Chambers, Martial Depczynski, Charles Fox, Bridget Green and two anonymous reviewers for valuable comments on an earlier version of the manuscript. Financial support was provided by a Ph.D. fellowship from the AFUW-Qld (M.G.) and research funding from an Australian Research Council Discovery grant (M.I.M., M.G.M). This study was conducted under appropriate permits from the Great Barrier Reef Marine Park Authority and the JCU Animal Ethics Committee (Approval Number A836_03).
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Communicated by Martin Attrill.
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Gagliano, M., McCormick, M.I. & Meekan, M.G. Temperature-induced shifts in selective pressure at a critical developmental transition. Oecologia 152, 219–225 (2007). https://doi.org/10.1007/s00442-006-0647-1
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DOI: https://doi.org/10.1007/s00442-006-0647-1