vol. 161, no. 6 the american naturalist june 2003 The Ontogeny of Fluctuating Asymmetry James R. Kellner * and Ross A. Alford † School of Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia Submitted July 22, 2002; Accepted November 23, 2002; Electronically published June 10, 2003 abstract: We tested seven hypotheses regarding the mechanisms by which fluctuating asymmetry (FA) originates. We did this by analyzing data on four bilateral characters measured repeatedly dur- ing the development of individual domestic fowl. Immediately post- hatching, there was substantial directional asymmetry, which rapidly decreased. We detected FA at significant levels in all characters in the majority of our measurements over the remainder of develop- ment. We also examined the effects of known environmental stressors (food and density stress) on levels of FA. At the levels we examined, changes in these stressors did not alter the degree of asymmetry we found in fowl. Time series of asymmetry for individuals did not exhibit regular oscillations, as much of the relevant literature predicts. Asymmetry levels reflected the combined effects of developmental noise, which was random in degree and direction, and feedback processes, which decreased asymmetry by altering growth rates on both sides of the body. Our findings best fit the predictions of the residual asymmetry and compensatory growth hypotheses, which suggest that levels of asymmetry reflect only recent growth history. Keywords: fluctuating asymmetry, bioindicator, ontogeny, develop- mental instability, stress. Developmental instability (DI) analysis can be used to make inferences about the general health of populations. It is based on the assumption that environmentally or genetically induced deviations from the ideal phenotype provide information about the precision of development, with lower precision reflecting the disruptive effects of environmental stressors, poor genetic quality, or both (re- viewed by Leary and Allendorf [1989]). The most com- monly used index of developmental instability is fluctu- * Present address: Pacific Biomedical Research Center, Kewalo Marine Lab- oratory, University of Hawaii at Manoa, Honolulu, Hawaii 96813; e-mail: james.kellner@graduates.jcu.edu.au. † Corresponding author; e-mail: ross.alford@jcu.edu.au. Am. Nat. 2003. Vol. 161, pp. 931–947.  2003 by The University of Chicago. 0003-0147/2003/16106-020269$15.00. All rights reserved. ating asymmetry (FA), the variance in right minus left ( ) values of bilaterally symmetrical structures (Pal- R  L i i mer and Strobeck 1992). Fluctuating asymmetry is char- acterized by a normal distribution of values about R  L i i a mean of 0. In addition to FA, two other types of bilateral asymmetry exist: directional asymmetry and antisymmetry (Van Valen 1962). Directional asymmetry occurs where there is a con- sistent bias for one side to become larger than the other side (e.g., the mammalian heart shows directional asym- metry, with the left side larger than the right; Van Valen 1962). Antisymmetry is characterized by a bimodal dis- tribution of with a mean of 0 (e.g., the signaling R  L i i claws of the male fiddler crab; Graham et al. 1993a). There is disagreement within the literature regarding whether the different types of asymmetry represent different products of the same underlying processes or result from funda- mentally different processes. Palmer and Strobeck (1992) argued that only FA is useful for studies of developmental instability. They suggested that because directional asym- metry and antisymmetry do not have an ideal state that is definable a priori, it is impossible to separate asymmetry caused by DI from that which has a genetic basis (Palmer and Strobeck 1992). However, antisymmetry was observed in Australian sheep blowflies Lucilia cuprina during their evolution to pesticide resistance (McKenzie and Clarke 1988), and Graham et al. (1993b) induced significant fluc- tuating asymmetry and directional asymmetry in Dro- sophila melanogaster exposed to high concentrations of benzene. The debate over which types of asymmetry can reflect DI is likely to remain unresolved until we under- stand the developmental origins of asymmetry of various types. Swaddle and Witter (1997) compiled a list of six hy- potheses that attempt to explain how asymmetry arises during growth and development: the directional external cues hypothesis, the “coin-toss” hypothesis, the magnifi- cation of asymmetry hypothesis, the accumulation of ac- cidents hypothesis, the persistent asymmetry hypothesis, and the compensatory growth hypothesis. We developed predictions from these hypotheses and added a seventh hypothesis, which we call the residual asymmetry hypoth- esis. We then designed experiments to distinguish among