Natural selection operates on organismal-level traits that are usually manifestations of the integrated functioning of a suite of organs and organ systems. Some of the most intensively studied of these traits are indices of overall physiological vigor or ‘quality’, such as locomotor performance (sprint speed, endurance, etc.) and aerobic capacity (Taylor and Weibel, 1981; Weibel, 1984; Chappell and Snyder, 1984; Garland and Else, 1987; Hammond et al., 1994; Chappell and Bachman, 1995). Theoretically, locomotor and aerobic performance limits might be set by peripheral effectors (primarily skeletal muscle) or by the visceral infrastructure (the digestive, pulmonary, cardiovascular or excretory organs) that supports the peripheral effectors. These views represent the ‘peripheral limitation hypothesis’ and the ‘central limitation hypothesis’, respectively (Peterson et al., 1990; Weiner, 1993). An alternative model is that all components of whole-animal performance traits are optimally scaled such that no one component is limiting and there is no expensive ‘excess capacity’. This concept, called ‘symmorphosis’, has been extensively promoted for the mammalian oxygen delivery system (e.g. Taylor and Weibel, 1981; Weibel, 1984; Weibel et al., 1991). Nevertheless, there is surprisingly little consensus on what organ systems or other factors limit aerobic or locomotor performance, even for the much-studied aerobic pathway in mammals. These questions can be investigated by making use of the natural variation typical of essentially all physiological traits. The repeatability and heritability of inter-individual differences are critical in determining how (or if) a performance trait can be affected by natural selection (e.g. Jayne and Bennett, 1990; Garland and Bennett, 1990). From a mechanistic perspective, analyses of variation at different levels of integration (e.g. enzymes, organelles, cells, organs, organ systems and the intact animal) can provide useful insights into the functional basis of whole-animal performance (e.g. Else and Hulbert, 1981; Hulbert and Else, 1981; Chappell and Snyder, 1984; Garland, 1984; Weibel, 1984; Bennett, 1997). We have used this approach in a study of aerobic performance in red junglefowl (Gallus gallus). These birds show substantial and repeatable variation in aerobic capacity (Chappell et al., 1996, 1998, 1999b). In addition to variability within each sex, the species exhibits striking sexual dimorphism in aerobic performance, with the aerobic capacity of males greatly exceeding that of females (Chappell et al., 1996). An intuitively attractive explanation for this difference is that neither sex engages in sustained flight but that, unlike 2053 The Journal of Experimental Biology 203,2053–2064 (2000) Printed in Great Britain © The Company of Biologists Limited 2000 JEB2752 We examined aerobic performance, organ and muscle mass and enzymatic activity in red junglefowl (Gallus gallus). We tested three models of performance limitation (central limits, peripheral limits, symmorphosis) and explored relationships between basal metabolic rate (BMR), aerobic capacity (V . O ∑ max ) and social rank. Males had a lower BMR, a higher V . O ∑ max and a greater aerobic scope than females. Females possessed larger peritoneal and reproductive organs, while males had larger hearts, lungs and leg muscles. In females, BMR was correlated with spleen mass and V . O ∑ max was correlated with hematocrit and large intestine mass. Male BMR was correlated with intestinal tract and lung mass, and V . O ∑ max was correlated with heart and pectoralis mass. Male citrate synthase activity averaged 57 % higher than that of females and was correlated with V . O ∑ max (this correlation was not significant in females). Female social status was not correlated with any variable, but male dominance was associated with higher aerobic scope, larger heart and lungs, smaller peritoneal organs and greater leg citrate synthase activity. We conclude that aerobic capacity is controlled by system-wide limitations (symmorphosis) in males, while in females it is controlled by central organs. In neither sex is elevated aerobic capacity associated with increased maintenance costs. Key words: aerobic performance, citrate synthase, symmorphosis, metabolic rate, social rank, muscle mass, red junglefowl, Gallus gallus. Summary Introduction THE MECHANISTIC BASIS OF AEROBIC PERFORMANCE VARIATION IN RED JUNGLEFOWL KIMBERLY A. HAMMOND*, MARK A. CHAPPELL, RICHARD A. CARDULLO, RUEI-SHIUAN LIN AND TORGEIR S. JOHNSEN Biology Department, University of California, Riverside, CA 92521, USA *e-mail: khammond@citrus.ucr.edu Accepted 6 April; published on WWW 13 June 2000