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

Abstract

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.

Prenatal development of skull and brain in a mouse model of growth restriction

“…Developmental processes intervening in morphological differentiation are limited in number and tend to be more conservative . In support of this expectation, patterns of craniofacial morphological variation similar to those found here were observed in rats under comparable treatments of maternal malnutrition (Gonzalez et al, 2011c;Martínez-Abadías et al, 2012). Consequently, although more work is necessary, it is plausible that our results can be extrapolated at least to other murine models.…”

Analyzing Fluctuating Asymmetry with Geometric Morphometrics: Concepts, Methods, and Applications

“…The first such analysis used a distance measure calculated as one minus the matrix correlation between covariance matrices [177], and alternative measures were proposed subsequently [408,409]. The statistical properties of these distance measures are not well understood, but some empirical comparisons have found somewhat similar but not identical patterns [73,349]. This approach has been applied to comparisons involving fluctuating asymmetry and individual variation [62,73,117,177].…”

“…Some further evidence on the nature of developmental stability and canalization is available from comparisons of fluctuating asymmetry and individual variation over different ages [343][344][345][346][347][348]. Studies using the methods of geometric morphometrics found fluctuating asymmetry of fetal mice to decrease with age [251] or reported diminishing individual variation over early postnatal development in various rodents [219,349,350]. There is also unexplored potential for future analyses of the regulation of shape variation, because some studies used longitudinal data [349,351].…”

“…Studies using the methods of geometric morphometrics found fluctuating asymmetry of fetal mice to decrease with age [251] or reported diminishing individual variation over early postnatal development in various rodents [219,349,350]. There is also unexplored potential for future analyses of the regulation of shape variation, because some studies used longitudinal data [349,351]. Analyses that explicitly address the covariation among the changes between successive ontogenetic stages can shed light on regulatory phenomena, but so far have only been used with traditional morphometric data [352][353][354][355][356][357].…”

Craneofacial effect of prenatal growth retardation and postnatal undernutrition in craniofacial growth

“…Durante la infancia y la niñez la desnutrición crónica (talla baja para la edad), la desnutrición aguda severa y el retardo del crecimiento intrauterino, constituyen los principales factores de riesgo de mortalidad (Black et al, 2008). Entre las causas más frecuentes de retardo prenatal de crecimiento (RPC) figura la insuficiencia útero-placentaria, condición que provoca disminución en la tasa de crecimiento fetal y otros efectos negativos sobre la salud, tanto a corto como a largo plazo (Clausson et al, 2001;Gomez Roig, 2002;Schwitzgebel et al, 2009). Así, estudios epidemiológicos han demostrado la relación entre la deficiencia nutricional ocurrida durante las primeras etapas de vida y las diferentes enfermedades que se manifiestan durante la adultez, principalmente aquellas relacionadas con el metabolismo de la glucosa (Godfrey y Barker, 2000;Flanagan et al, 2000), la hipertensión y el daño cardiovascular (Hales et al, 1997;Ozanne y Hales, 1999).…”