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A Quantitative-Genetics Perspective on Mammalian Development

William R. Atchley and Scott Newman
The American Naturalist
Vol. 134, No. 3 (Sep., 1989), pp. 486-512
Stable URL: http://www.jstor.org/stable/2462183
Page Count: 27
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A Quantitative-Genetics Perspective on Mammalian Development
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Abstract

These discussions are intended to describe some important aspects of evolutionary change in complex traits from a developmental quantitative-genetics perspective. These comments support the contention that information about the complexity of the trait, the dynamics of the underlying controlling factors, and an age-specific response to selection must be incorporated into discussions of evolutionary change by selection. The developmental complexity of a trait strongly influences attempts to ascertain its genetic architecture and its age-specific response to selection. The component parts are often under separate genetic control, and there is a substantial nonheritable component to many of these components. Recognition of this complexity permits variability in composite traits to be decomposed; the genetic architecture of the individual subunits is thus determined, yielding a more holistic picture of the genetic structure of the entire trait. Furthermore, it is clear that these complex traits could be altered by selection operating on any or all of the component parts. The magnitude and direction of selection response in complex traits are a function of the genetic-covariance structure among the component parts. As an additional consequence, it is possible that the same end-point phenotype can be obtained by changing different combinations of the component parts. If so, the correlated response to selection in other traits can be quite varied, depending on which component of the complex trait is changed by selection and on the genetic-covariance structure among the component parts within a trait and between traits. There are significant ontogenetic aspects of the underlying causal factors-that is, direct and indirect genetic factors-that are controlling each component part of a complex trait. The course of development in a complex trait involves coordination and integration of a number of separate biological processes that begin functioning during the early ontogeny of an organism. Genes influencing expression of these processes in mammals may arise from the individual's own genome and, as a result, contribute directly to production of the phenotype. In addition, during the prenatal and preweaning phases of ontogeny, the expression of genes in the individual's mother may contribute indirectly to the developmental expression of her progeny's phenotype. The interrelationship between direct and indirect maternal genetic factors has a decided ontogenetic aspect, since they contribute differentially during the prenatal, postnatal, and postweaning phases of development. Indeed, the magnitude and the direction of the contribution of these two separate but possibly correlated sets of genetic effects may change considerably as a function of the stage of ontogeny of the organism. The result of an ontogenetically changing set of genetic controlling factors is a much more complex response to selection than is predicted by the direct-effects genetic model. The size and magnitude of the genetic correlation between direct and maternal components of variability determine the direction and the rate of evolutionary change by selection. A negative genetic covariance between direct and maternal genetic components, which is common for many complex traits, greatly complicates the estimation of genetic parameters and the prediction of evolutionary change by selection. The actual components of a complex trait that is responding to selection may be strongly affected by the developmental age at which selection occurs. However, in addition to the qualitative aspects of selection response, developmental age may also have a quantitative component because of the age-dependent contribution of maternal effects. The earlier during ontogeny that selection is focused, the greater the potential contribution of maternal effects. Because of the potential for a negative covariance between direct and maternal genetic effects, the contribution to the selection response made by maternal effects can be quite complicated.

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