EVOLUTION OF INTRINSIC GROWTH RATE: METABOLIC COSTS DRIVE TRADE‐OFFS BETWEEN GROWTH AND SWIMMING PERFORMANCE IN MENIDIA MENIDIA

Abstract There is strong evidence that genetic capacity for growth evolves toward an optimum rather than an absolute maximum. This implies that fast growth has a cost and that trade‐offs occur between growth and other life‐history traits, but the fundamental mechanisms are poorly understood. Previous work on the Atlantic silverside fish Menidia menidia has demonstrated a trade‐off between growth and swimming performance. We hypothesize that the trade‐off derives from the competing metabolic demands associated with growth and swimming activity. We tested this by measuring standard metabolic rate (MSTD), maximum sustainable metabolic rate (MACT) and metabolic scope of laboratory‐reared silversides originating from two geographically distinct populations with well‐documented differences in genetic capacity for growth. The fast‐growth genotype had a significantly greater MSTD than the slow‐growth genotype, but a similar MACT when swum to near exhaustion. The scope for activity of the fast‐growth genotype was lower than that of the slow‐growth genotype. Furthermore, the fast‐growth genotype eats larger meals, thereby incurring a greater postprandial oxygen demand. We conclude that a metabolic trade‐off occurs between growth and other metabolic demands and that this trade‐off provides a general mechanism underlying the evolution of growth rate.

[1]  C. M. Lessells,et al.  The Evolution of Life Histories , 1994 .

[2]  T. Case.  On the Evolution and Adaptive Significance of Postnatal Growth Rates in the Terrestrial Vertebrates , 1978, The Quarterly Review of Biology.

[3]  S. L. Lima,et al.  Behavioral decisions made under the risk of predation: a review and prospectus , 1990 .

[4]  M. Mangel,et al.  QUANTIFYING NATURAL SELECTION ON BODY SIZE FROM FIELD DATA: WINTER MORTALITY IN MENIDIA MENIDIA , 2003 .

[5]  L. Valente,et al.  Growth dynamics of white and red muscle fibres in fast- and slow-growing strains of rainbow trout , 1999 .

[6]  B. McNab,et al.  Food Habits, Energetics, and the Population Biology of Mammals , 1980, The American Naturalist.

[7]  J. Arendt,et al.  Adaptive Intrinsic Growth Rates: An Integration Across Taxa , 1997, The Quarterly Review of Biology.

[8]  R. James,et al.  Tradeoffs and the evolution of thermal reaction norms , 2003 .

[9]  A. H. Weatherley,et al.  Recruitment and maximal diameter of axial muscle fibres in teleosts and their relationship to somatic growth and ultimate size , 1988 .

[10]  Michael S. Johnson.  Biochemical Systematics of the Atherinid Genus Menidia , 1975 .

[11]  S. Munch,et al.  NONLINEAR GROWTH COST IN MENIDIA MENIDIA: THEORY AND EMPIRICAL EVIDENCE , 2004, Evolution; international journal of organic evolution.

[12]  L. Partridge,et al.  Demography of Dietary Restriction and Death in Drosophila , 2003, Science.

[13]  J. Davenport,et al.  Apparent Specific Dynamic Action of Food in the Fish Blennius pholis , 1979 .

[14]  N. Metcalfe,et al.  The stability of standard metabolic rate during a period of food deprivation in juvenile Atlantic salmon , 2000 .

[15]  R. Wootton.  The evolution of life histories: Theory and analysis , 1993, Reviews in Fish Biology and Fisheries.

[16]  D. Conover,et al.  Patterns in seasonal abundance, growth and biomass of the atlantic silverside, Menidia menidia, in a New England estuary , 1982 .

[17]  D. Conover,et al.  EVOLUTION OF INTRINSIC GROWTH AND ENERGY ACQUISITION RATES. II. TRADE-OFFS WITH VULNERABILITY TO PREDATION IN MENIDIA MENIDIA , 2001 .

[18]  RAPID GROWTH RESULTS IN INCREASED SUSCEPTIBILITY TO PREDATION IN MENIDIA MENIDIA , 2003, Evolution; international journal of organic evolution.

[19]  J. Lee,et al.  Metabolic ontogeny of teleost fishes , 1996 .

[20]  D. Conover,et al.  EVOLUTION OF INTRINSIC GROWTH AND ENERGY ACQUISITION RATES. I. TRADE‐OFFS WITH SWIMMING PERFORMANCE IN MENIDIA MENIDIA , 2001, Evolution; international journal of organic evolution.

[21]  W. Wieser,et al.  Aerobic maximum for growth in the larvae and juveniles of a cyprinid fish, Rutilus rutilus (L.): implications for energy budgeting in small poikilotherms , 1990 .

[22]  D. Conover,et al.  Phenotypic similarity and the evolutionary significance of countergradient variation. , 1995, Trends in ecology & evolution.

[23]  P. Magnan,et al.  Relationship between individual variation in morphological characters and swimming costs in brook charr (Salvelinus fontinalis) and yellow perch (Perca flavescens). , 2002, The Journal of experimental biology.

[24]  I. Priede.  Natural selection for energetic efficiency and the relationship between activity level and mortality , 1977, Nature.

[25]  N. Metcalfe,et al.  Deferred costs of compensatory growth after autumnal food shortage in juvenile salmon , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  M. Abrahams,et al.  Predators select against high growth rates and risk–taking behaviour in domestic trout populations , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[27]  Imants G. Priede,et al.  Metabolic Scope in Fishes , 1985 .

[28]  S. Sogard.  Size-selective mortality in the juvenile stage of teleost fishes : A review , 1997 .

[29]  E. Houde,et al.  Predation on Eggs and Larvae of Marine Fishes and the Recruitment Problem , 1989 .

[30]  S. Q. Xie,et al.  Changes in Tissue Cellularity Are Associated with Growth Enhancement in Genetically Modified Arctic Char (Salvelinus alpinus L.) Carrying Recombinant Growth Hormone Gene , 2001, Marine Biotechnology.

[31]  D. Conover,et al.  Temperature-sensitive period of sex determination in the Atlantic silverside, Menidia menidia , 1986 .

[32]  D. Conover,et al.  Countergradient variation in growth rate: compensation for length of the growing season among Atlantic silversides from different latitudes , 1990, Oecologia.

[33]  M. Morgan,et al.  Consequences of life history for inbreeding depression and mating system evolution in plants , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[34]  Alsop,et al.  The interactive effects of feeding and exercise on oxygen consumption, swimming performance and protein usage in juvenile rainbow trout (Oncorhynchus mykiss) , 1997, The Journal of experimental biology.

[35]  N. Metcalfe,et al.  Compensation for a bad start: grow now, pay later? , 2001, Trends in ecology & evolution.

[36]  The energetics of starvation and growth after refeeding in juveniles of three cyprinid species , 1992 .

[37]  D. Conover,et al.  Physiological Basis of Latitudinal Growth Differences in Menidia menidia: Variation in Consumption or Efficiency? , 1992 .

[38]  J. R. Brett,et al.  6 – Physiological Energetics , 1979 .

[39]  W. Wieser,et al.  To Switch or Not to Switch: Partitioning of Energy between Growth and Activity in Larval Cyprinids (Cyprinidae: Teleostei) , 1988 .

[40]  D. Conover,et al.  Latitudinal differences in somatic energy storage: adaptive responses to seasonality in an estuarine fish (Atherinidae: Menidia menidia) , 1997, Oecologia.

[41]  D. Conover,et al.  EVOLUTION OF INTRINSIC GROWTH AND ENERGY ACQUISITION RATES. II. TRADE‐OFFS WITH VULNERABILITY TO PREDATION IN MENIDIA MENIDIA , 2001, Evolution; international journal of organic evolution.

[42]  S. Munch,et al.  Darwinian fishery science: lessons from the Atlantic silverside (Menidia menidia) , 2005 .

[43]  T. Pitcher.  Functions of Shoaling Behaviour in Teleosts , 1986 .

[44]  D. Conover.  The Relation between Capacity for Growth and Length of Growing Season: Evidence for and Implications of Countergradient Variation , 1990 .

[45]  D. R. Jones,et al.  Evaluation of the Swimming Performance of Several Fish Species from the Mackenzie River , 1974 .

[46]  N. Metcalfe,et al.  Juvenile Atlantic Salmon (Salmo salar) with relatively high standard metabolic rates have small metabolic scopes , 2002 .

[47]  C. Rollo.  Growth negatively impacts the life span of mammals , 2002, Evolution & development.

[48]  F.E.J. Fry,et al.  1 – The Effect of Environmental Factors on the Physiology of Fish , 1971 .

[49]  D. Conover,et al.  Adaptive variation in energy acquisition and allocation among latitudinal populations of the Atlantic silverside , 2000, Oecologia.