GENETIC BASIS OF ACTIVITY METABOLISM. I. INHERITANCE OF SPEED, STAMINA, AND ANTIPREDATOR DISPLAYS IN THE GARTER SNAKE THAMNOPHIS SIRTALIS

Recent conceptual advances in physiological ecology emphasize the potential selective importance of whole‐animal performance. Empirical studies of locomotor performance in reptiles have revealed surprising amounts of individual variation in speed and stamina. The present study is the first in a series examining the genetic basis of variation in locomotor performance, activity metabolism, and associated behaviors in garter snakes. Maximal sprint crawling speed, treadmill endurance, and antipredator displays (Arnold and Bennett, 1984; exhibited as snakes reached exhaustion on the treadmill) were measured for approximately six offspring (presumed to be full siblings) from each of 46 wild‐caught gravid garter snakes (Thamnophis sirtalis). Each character was measured on two days; all were individually repeatable. Correlations of these characters with body mass, snout–vent length, age at testing, litter size, dam mass, and dam snout–vent length were removed by computing residuals from multiple‐regression equations. These residuals were used in subsequent genetic analyses. Approximate coefficients of variation of residuals were 17% for speed, 48% for endurance, and 31% for antipredator displays. Broad‐sense heritabilities were significant for all characters: speed h2 = 0.58; stamina h2 = 0.70; antipredator display h2 = 0.42. All three residual characters showed positive and statistically significant phenotypic correlations (r = 0.19–0.36). Genetic correlations (estimated and tested by restricted maximum likelihood) among residuals were positive and highly significant between speed and endurance (0.58), but nonsignificant between speed and antipredator display (0.43), and between endurance and antipredator display (0.26). All environmental correlations were nonsignificant. These data suggest that, contrary to expectations based on previous physiological studies, there may be no necessary evolutionary trade‐off between speed and stamina in these animals. This tentative conclusion will have important implications for future theoretical studies of the evolution of locomotor performance and associated antipredator behaviors.

[1]  M. Hildebrand Analysis of Vertebrate Structure , 1974 .

[2]  M. Bulmer The Mathematical Theory of Quantitative Genetics , 1981 .

[3]  S. J. Arnold,et al.  Behavioural variation in natural populations. III: Antipredator displays in the garter snake Thamnophis radix , 1984, Animal Behaviour.

[4]  R. Lande QUANTITATIVE GENETIC ANALYSIS OF MULTIVARIATE EVOLUTION, APPLIED TO BRAIN:BODY SIZE ALLOMETRY , 1979, Evolution; international journal of organic evolution.

[5]  W. Mosauer,et al.  How Fast Can Snakes Travel , 1935 .

[6]  Hilary Gonzalez,et al.  Functional Vertebrate Morphology , 1986, The Yale Journal of Biology and Medicine.

[7]  C. Bouchard,et al.  GENETICS FOR THE SPORT SCIENTIST: SELECTED METHODOLOGICAL CONSIDERATIONS , 1983, Exercise and sport sciences reviews.

[8]  G. Bartholomew,et al.  The role of natural history in contemporary biology , 1986 .

[9]  H. Grüneberg,et al.  Introduction to quantitative genetics , 1960 .

[10]  S. J. Arnold,et al.  Garter Snake Diets in a Fluctuating Environment: A Seven-Year Study , 1982 .

[11]  D. Reznick Costs of reproduction: an evaluation of the empirical evidence , 1985 .

[12]  T. Gleeson,et al.  Reptilian Skeletal Muscle: Fiber-type Composition and Enzymatic Profile in the Lizard, Iguana iguana , 1986 .

[13]  M. Rose Genetic Covariation in Drosophila Life History: Untangling the Data , 1984, The American Naturalist.

[14]  B. Jayne Kinematics of terrestrial snake locomotion , 1986 .

[15]  S. J. Arnold,et al.  Morphology, Performance and Fitness , 1983 .

[16]  T. Garland,et al.  Time Budgets, Thermoregulation, and Maximal Locomotor Performance: Are Reptiles Olympians or Boy Scouts? , 1988 .

[17]  J. Cheverud,et al.  Quantitative genetics and developmental constraints on evolution by selection. , 1984, Journal of theoretical biology.

[18]  C. Bouchard,et al.  GENETICS OF PHYSIOLOGICAL FITNESS AND MOTOR PERFORMANCE , 1983, Exercise and sport sciences reviews.

[19]  T. Garland,et al.  Effects of endurance training and captivity on activity metabolism of lizards. , 1987, The American journal of physiology.

[20]  S. J. Arnold BEHAVIORAL VARIATION IN NATURAL POPULATIONS. I. PHENOTYPIC, GENETIC AND ENVIRONMENTAL CORRELATIONS BETWEEN CHEMORECEPTIVE RESPONSES TO PREY IN THE GARTER SNAKE, THAMNOPHIS ELEGANS , 1981, Evolution; international journal of organic evolution.

[21]  Robert D. Stevenson,et al.  Integrating Thermal Physiology and Ecology of Ectotherms: A Discussion of Approaches , 1979 .

[22]  S. J. Arnold,et al.  THE MEASUREMENT OF SELECTION ON CORRELATED CHARACTERS , 1983, Evolution; international journal of organic evolution.

[23]  S. Stearns HERITABILITY ESTIMATES FOR AGE AND LENGTH AT MATURITY IN TWO POPULATIONS OF MOSQUITOFISH THAT SHARED ANCESTORS IN 1905 , 1984, Evolution; international journal of organic evolution.

[24]  Theodore Garland,et al.  Comparative locomotor performance of marsupial and placental mammals , 1988 .

[25]  G. Burghardt,et al.  Development of Antipredator Responses in Snakes: I. Defensive and Open-Field Behaviors in Newborns and Adults of Three Species of Garter Snakes (Thamnophis melanogaster, T. sirtalis, T. butleri) , 1986 .

[26]  S. J. Arnold,et al.  Effects of a Full Stomach on Locomotory Performance of Juvenile Garter Snakes (Thamnophis elegans) , 1983 .

[27]  R. Bürger CONSTRAINTS FOR THE EVOLUTION OF FUNCTIONALLY COUPLED CHARACTERS: A NONLINEAR ANALYSIS OF A PHENOTYPIC MODEL , 1986, Evolution; international journal of organic evolution.

[28]  T. Garland,et al.  Seasonal, sexual, and individual variation in endurance and activity metabolism in lizards , 2002 .

[29]  J. Ruben MORPHOLOGICAL CORRELATES OF PREDATORY MODES IN THE COACHWHIP (MASTICOPHIS FLAGELLUM) AND ROSY BOA (LICHANURA ROSEOFUSCA)1 , 1977 .

[30]  R. Montgomerie Behavioral Energetics. The Cost of Survival in Vertebrates, Wayne P. Aspey, Sheldon I. Lustick (Eds.). Ohio State University Press, Columbus (1983), 300 , 1984 .

[31]  L. Dimichele,et al.  Physiological basis for swimming endurance differences between LDH-B genotypes of Fundulus heteroclitus. , 1982, Science.

[32]  T. Garland Physiological correlates of locomotory performance in a lizard: an allometric approach. , 1984, The American journal of physiology.

[33]  T. Marlowe,et al.  Heritability and repeatability of speed for 2- and 3-year-old standardbred racehorses. , 1983, Journal of animal science.

[34]  Alan C. Kamil,et al.  Foraging behavior: ecological, ethological, and psychological approaches , 1980 .

[35]  P. Boag THE HERITABILITY OF EXTERNAL MORPHOLOGY IN DARWIN'S GROUND FINCHES (GEOSPIZA) ON ISLA DAPHNE MAJOR, GALÁPAGOS , 1983, Evolution; international journal of organic evolution.

[36]  C. Prosser,et al.  Adaptational Biology: Molecules to Organisms , 1986 .

[37]  S. J. Arnold BEHAVIORAL VARIATION IN NATURAL POPULATIONS. II. THE INHERITANCE OF A FEEDING RESPONSE IN CROSSES BETWEEN GEOGRAPHIC RACES OF THE GARTER SNAKE, THAMNOPHIS ELEGANS , 1981, Evolution; international journal of organic evolution.

[38]  A. F. Bennett The thermal dependence of lizard behaviour , 1980, Animal Behaviour.

[39]  A. F. Bennett,et al.  Histochemical, enzymatic, and contractile proper of skeletal muscles of three anuran amphibians. , 1983, The American journal of physiology.

[40]  M. C. Devine Copulatory plugs, restricted mating opportunities and reproductive competition among male garter snakes , 1977, Nature.

[41]  D. Crews,et al.  Influence of the seminal plug on mating behaviour in the garter snake , 1977, Nature.

[42]  R. Huey,et al.  Locomotor capacity and foraging behaviour of kalahari lacertid lizards , 1984, Animal Behaviour.

[43]  R. Huey,et al.  REPEATABILITY OF LOCOMOTOR PERFORMANCE IN NATURAL POPULATIONS OF THE LIZARD SCELOPORUS MERRIAMI , 1987, Evolution; international journal of organic evolution.

[44]  M. E. Johnson,et al.  A Comparative Study of Tests for Homogeneity of Variances, with Applications to the Outer Continental Shelf Bidding Data , 1981 .

[45]  P V Komi,et al.  Physiological and Biomechanical Correlates of Muscle Function: Effects of Muscle Structure and Stretch—Shortening Cycle on Force and Speed , 1984, Exercise and sport sciences reviews.

[46]  J. Rutledge,et al.  Quantitative Genetics in Natural Plant Populations: A Review of the Theory , 1986, The American Naturalist.

[47]  Joan E. Ryan The inheritance of track performance in greyhounds , 1977 .

[48]  J. T. Giesel Genetic Correlation Structure of Life History Variables in Outbred, Wild Drosophila melanogaster: Effects of Photoperiod Regimen , 1986, The American Naturalist.

[49]  B. Langlois Heritability of racing ability in thoroughbreds — A review , 1980 .

[50]  R. Hintz,et al.  Genetics of performance in the horse. , 1980, Journal of animal science.

[51]  R. Huey,et al.  Effects of Body Size and Slope on Acceleration of a Lizard (Stellio Stellio) , 1984 .

[52]  S A Glantz,et al.  Multiple regression for physiological data analysis: the problem of multicollinearity. , 1985, The American journal of physiology.

[53]  R. Greenberg Biometry , 1969, The Yale Journal of Biology and Medicine.

[54]  R. Huey Phylogenetic and Ontogenetic determinants of sprint performance in some diurnal Kalahari Lizards , 1982 .

[55]  R. Shaw MAXIMUM‐LIKELIHOOD APPROACHES APPLIED TO QUANTITATIVE GENETICS OF NATURAL POPULATIONS , 1987, Evolution; international journal of organic evolution.

[56]  H. Herzog,et al.  Development of Antipredator Responses in Snakes: II. Effects of Recent Feeding on Defensive Behaviors of Juvenile Garter Snakes (Thamnophis sirtalis} , 1987 .

[57]  Neil B. Ford,et al.  Effects of Variation in Food Intake on Locomotory Performance of Juvenile Garter Snakes , 1986 .

[58]  MEASURING THE COST OF REPRODUCTION: A COMMENT ON PAPERS BY BELL , 1986, Evolution; international journal of organic evolution.

[59]  S. J. Arnold,et al.  Behavioural variation in natural populations. V. Morphological correlates of locomotion in the garter snake (Thamnophis radix) , 1988 .

[60]  Joyce S. Tsuji,et al.  Inter‐familiar differences in sprint speed of hatchling Sceloporus occidentalis (Reptilia: Iguanidae) , 1987 .