Developmental plasticity in covariance structure of the skull: effects of prenatal stress

Environmental perturbations of many kinds influence growth and development. Little is known, however, about the influence of environmental factors on the patterns of phenotypic integration observed in complex morphological traits. We analyze the changes in phenotypic variance-covariance structure of the rat skull throughout the early postnatal ontogeny (from birth to weaning) and evaluate the effect of intrauterine growth retardation (IUGR) on this structure. Using 2D coordinates taken from lateral radiographs obtained every 4 days, from birth to 21 days old, we show that the pattern of covariance is temporally dynamic from birth to 21 days. The environmental perturbation provoked during pregnancy altered the skull growth, and reduced the mean size of the IUGR group. These environmental effects persisted throughout lactancy, when the mothers of both groups received a standard diet. More strikingly, the effect grew larger beyond this point. Altering environmental conditions did not affect all traits equally, as revealed by the low correlations between covariance matrices of treatments at the same age. Finally, we found that the IUGR treatment increased morphological integration as measured by the scaled variance of eigenvalues. This increase coincided and is likely related to an increase in morphological variance in this group. This result is expected if somatic growth is a major determinant of covariance structure of the skull. In summary, our findings suggest that environmental perturbations experienced in early ontogeny alter fundamental developmental processes and are an important factor in shaping the variance-covariance structure of complex phenotypic traits.