Nature, Nurture, and Noise: Developmental Instability, Fluctuating Asymmetry, and the Causes of Phenotypic Variation

Phenotypic variation arises from genetic and environmental variation, as well as random aspects of development. The genetic (nature) and environmental (nurture) components of this variation have been appreciated since at least 1900. The random developmental component (noise) has taken longer for quantitative geneticists to appreciate. Here, I sketch the historical development of the concepts of random developmental noise and developmental instability, and its quantification via fluctuating asymmetry. The unsung pioneers in this story are Hugo DeVries (fluctuating variation, 1909), C. H. Danforth (random variation between monozygotic twins, 1919), and Sewall Wright (random developmental variation in piebald guinea pigs, 1920). The first pioneering study of fluctuating asymmetry, by Sumner and Huestis in 1921, is seldom mentioned, possibly because it failed to connect the observed random asymmetry with random developmental variation. This early work was then synthesized by Boris Astaurov in 1930 and Wilhelm Ludwig in 1932, and then popularized by Drosophila geneticists beginning with Kenneth Mather in 1953. Population phenogeneticists are still trying to understand the origins and behavior of random developmental variation. Some of the developmental noise represents true stochastic behavior of molecules and cells, while some represents deterministic chaos, nonlinear feedback, and symmetry breaking.