Developmental Interactions and the Constituents of Quantitative Variation

Abstract

Abstract. Development is the process by which genotypes are transformed into phenotypes. Consequently, development determines the relationship between allelic and phenotypic variation in a population and, therefore, the patterns of quantitative genetic variation and covariation of traits. Understanding the developmental basis of quantitative traits may lead to insights into the origin and evolution of quantitative genetic variation, the evolutionary fate of populations, and, more generally, the relationship between development and evolution. Herein, we assume a hierarchical, modular structure of trait development and consider how epigenetic interactions among modules during ontogeny affect patterns of phenotypic and genetic variation. We explore two developmental models, one in which the epigenetic interactions between modules result in additive effects on character expression and a second model in which these epigenetic interactions produce nonadditive effects. Using a phenotype landscape approach, we show how changes in the developmental processes underlying phenotypic expression can alter the magnitude and pattern of quantitative genetic variation. Additive epigenetic effects influence genetic variances and covariances, but allow trait means to evolve independently of the genetic variances and covariances, so that phenotypic evolution can proceed without changing the genetic covariance structure that determines future evolutionary response. Nonadditive epigenetic effects, however, can lead to evolution of genetic variances and covariances as the mean phenotype evolves. Our model suggests that an understanding of multivariate evolution can be considerably enriched by knowledge of the mechanistic basis of character development. Adaptive evolution proceeds by selection acting on phenotypes, thereby altering the pattern of allelic variation in a population. The relationship between allelic and phenotypic variation is structured by ontogeny (Cheverud 1988;. Consequently, development plays a critical role in determining how allelic variation is translated into quantitative genetic variation and covariation (Rice 2000) and, thus, how allelic variation can contribute to the evolutionary change in a trait. Although researchers stressed a central role for development in evolution for several decades (e.g., de Beer 1940;Goldschmidt 1940;Schmalhausen 1949;Waddington 1957;Wright 1968;Gould 1977; Gilbert et al. 1996), the connection between particular developmental mechanisms and the process of microevolutionary change have been examined explicitly only relatively recently (Atchley 1984;Cheverud 1984;Riska 1986;Slatkin 1987;Wagner et al. 1997;Rice 1998Rice , 2000.Quantitative genetic models are the primary tools that have been used to understand how selection on phenotypes translates into the genetic changes that alter phenotype distributions across generations (e.g., Lande 1979). Fundamental to these quantitative genetic models is the partitioning of phe-2 Present address: Department of Anatomy and Neurobiology, Washingto...

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