Paula N. Gonzalez

Rediscovering Waddington in the post‐genomic age

Conrad Hal Waddington was a revolutionary interdisciplinary thinker well ahead of his time. Many of his ideas have been subsumed into our current understanding of developmental biology [1]. His pioneering theories, first published in the mid-20th century, continue to find validation 50 years later in the molecular era of developmental genetics [2]. Among his many contributions, Waddington [3] introduced the term epigenetics to describe the full variety of emergent developmental phenomena above the level of the genome, and elegantly expressed these ideas in the form of his widely recognised and explicitly evolutionary epigenetic landscape metaphor [3]. These emergent phenomena bridge the gap between genotype and phenotype, and comprise the epigenotype [5]. Because of this close relationship between development and evolution, it is important to grasp how such epigenetic mechanisms function. The diverse use of the term epigenetics in the subsequent literature has led to substantial disagreement about what exactly is being discussed, and at which level(s) of inquiry, despite several attempts to achieve consensus [6, 7]. In most contemporary biological contexts, epigenetics refers to chromatin modification [8]. Not only does Waddington’s more inclusive definition appear to have been largely abandoned, also the different uses of his term have coincided with the near disappearance of the original concept of epigenetics from models of evolutionary change [9]. We see this as a potentially significant problem for evolutionary biologists. In this essay our focus is on the theoretical concepts originally specified by Waddington’s epigenetics. We argue that, in this age of powerful postgenomic laboratory and bioinformatics tools, epigenetics sensu Waddington is more informative and instructive than it has been for decades. Waddington’s epigenetics has the potential to shed new light on the means by which both selectable variation and innovation, two key features of evolutionary theory, are

Effects of Environmental Perturbations During Postnatal Development on the Phenotypic Integration of the Skull

Integration and modularity are fundamental determinants of how natural selection effects evolutionary change in complex multivariate traits. Interest in the study of the specific developmental basis of integration through experimental approaches is fairly recent and it has mainly focused on its genetic determinants. In this study, we present evidence that postnatal environmental perturbations can modify the covariance structure by influencing the variance of some developmental processes relative to the variances of other processes that contribute to such structure. We analyzed the effects of the reduction of nutrient supply in different ontogenetic stages (i.e. before and after weaning, and from birth to adulthood) in Rattus norvegicus. Our results show that this environmental perturbation alters the phenotypic variation/covariation structure of the principal modules of the skull (base, vault, and face). The covariance matrices of different treatment groups exhibit low correlations and are significantly different, indicating that the treatments influence covariance structure. Postnatal nutrient restriction also increases the variance of somatic growth. This increased variance drives an increase in overall integration of cranial morphology through the correlated allometric effects of size variation. The extent of this increase in integration depends on the time and duration of the nutritional restriction. These results support the conclusion that environmental perturbations can influence integration and thus covariance structure via developmental plasticity.

Ontogenetic Allometry and Cranial Shape Diversification Among Human Populations From South America

Modifications of ontogenetic allometries play an important role in patterning the shape differentiation among populations. This study evaluates the influence of size variation on craniofacial shape disparity among human populations from South America and assesses whether the morphological disparity observed at the interpopulation level resulted from a variable extension of the same ontogenetic allometry, or whether it arose as a result of divergences in the pattern of size‐related shape changes. The size and shape of 282 adult and subadult crania were described by geometric morphometric‐based techniques. Multivariate regressions were used to evaluate the influence of size on shape differentiation between and within populations, and phylogenetic comparative methods were used to take into account the shared evolutionary history among populations. The phylogenetic generalized least‐squares models showed that size accounts for a significant amount of shape variation among populations for the vault and face but not for the base, suggesting that the three modules did not exhibit a uniform response to changes in overall growth. The common slope test indicated that patterns of evolutionary and ontogenetic allometry for the vault and face were similar and characterized by a heightening of the face and a lengthening of the vault with increasing size. The conservation of the same pattern of shape changes with size suggests that differences in the extent of growth contributed to the interpopulation cranial shape variation and that certain directions of morphological change were favored by the trait covariation along ontogeny. Anat Rec, 2011.

Ecological and evolutionary factors in dental morphological diversification among modern human populations from southern South America

The knowledge of processes involved in morphological variation requires the integrated analysis of evolutionary and ecological factors. Here, we investigate the factors responsible for dental variation among human populations from southern South America. The aim of this work is to test the correspondence of dental size and shape variation with geographical, molecular (i.e. mtDNA) and ecological (i.e. climate, diet and food preparation) variables employing comparative phylogenetic methods, which have not previously been extensively applied at a within-species level. The results of the Procrustes analysis show a significant association of shape variables with molecular distance and geography, whereas dental size is not associated with molecular or geographical distances among groups. Phylogenetic generalized least-squares analysis, which takes into account the evolutionary autocorrelation among populations, shows a significant relationship between dental size variation and diet, while temperature and pottery do not correspond with dental size or shape. Specifically, groups with diets rich in carbohydrates, as well as the maritime hunter-gatherers, have the smallest teeth. In summary, our results support ecological factors as the dominant factor on dental size diversification in this region, while evolutionary relationships account for variation in dental shape.

Developmental Processes, Evolvability, and Dental Diversification of New World Monkeys

The developmental processes that contribute to variation of morphological traits are the subject of considerable interest when attempting to understand phenotypic evolution. It is well demonstrated that most characteristics of tooth pattern can be modified by tinkering conserved signal pathways involved in dental development. This effect can be evaluated by comparing developmental models with naturally occurring variation within explicit phylogenetic contexts. Here, we assess whether evolutionary changes in lower molar (M) ratios among platyrrhines were channelled by alterations in the balance of activators and inhibitors as predicted by the inhibitory cascade (IC) model (Kavanagh et al. in Nature 449:427–432, 2007). Ordinary linear regression adjusted to M2/M1 versus M3/M1 ratios of 38 species of platyrrhines indicated that the slope and intercept were significantly different from the IC model. Conversely, when the phylogeny was incorporated into the regression analyses (PGLS), variation in molar ratios did not differ from the developmental model. PGLS also showed that changes in molar proportions are not an allometric effect associated with body size. Discrepancies between phylogenetically corrected and non-corrected analyses are mainly due to the departure of Callitrichines from the predicted values. This subfamily displays agenesis of M3 with higher than expected M2/M1 ratios, indicating that M3 fails to develop even when the inhibition by M1 on the subsequent molars is not increased. Our results show that evolution in molar ratios is concordant with slight changes in the proportion of activators and inhibitors that regulate molar development; however, other processes are required to account for variation in the number of teeth.

Variabilidad de las proporciones molares en poblaciones humanas: un abordaje empleando modelos del desarrollo y experimentales

espanolLos datos sobre la variacion dental interpoblacional y sobre los mecanismos que regulan el desarrollo dental aportados por estudios experimentales aun no han sido integrados en el contexto de investigaciones antropobiologicas. En este sentido, el presente trabajo se propone: a) evaluar la consistencia entre la variacion de las proporciones molares en poblaciones humanas que exhiben gran variacion en el tamano dental con las predicciones derivadas de un modelo de desarrollo dental de cascada inhibitoria, y b) analizar el efecto de los factores sistemicos que controlan el crecimiento del organismo sobre las proporciones de los molares inferiores empleando cepas de Mus musculus. Se calcularon las areas de los molares inferiores mediante los diametros bucolingual y mesiodistal. La variacion interpoblacional en las proporciones M2/M1 y M3/M1 fue concordante con las expectativas derivadas del modelo y la mayoria de los grupos exhibieron una tendencia a la reduccion del tamano en sentido antero-posterior. Asimismo, se observo una asociacion significativa y positiva entre el area molar total y las proporciones molares. En los modelos experimentales la alteracion del crecimiento por factores sistemicos (subnutricion proteica y reduccion de la hormona de crecimiento) resulto en la disminucion del area molar total y cambios en las proporciones molares. Estos ultimos, consistentes con el incremento del efecto inhibitorio en sentido antero-posterior. En conjunto, los resultados sugieren que la modificacion de los factores sistemicos que regulan el area molar total podria conducir a cambios en la proporcion de activadores-inhibidores y contribuir a la diferenciacion interpoblacional en las proporciones molares. EnglishData on dental variation among human populations and the mechanisms regulating tooth development elucidated by experimental studies have not yet been integrated in the context of biological anthropology. In this sense, this paper proposes: a) to evaluate the consistency between changes in molar proportions in human populations that exhibit a wide variation in tooth size and the predictions derived from an inhibitory cascade model of dental development, and b) to analyze the effect of the systemic factors controlling the growth of the organism on the lower molars proportions using strains of Mus musculus. The crown area of the mandibular molars was estimated from the bucco-lingual and mesio-distal diameters. The results obtained for human populations showed that the pattern of variation in molar proportions is consistent with expectations derived from the inhibitory cascade model and that most groups exhibit a general trend towards molar size reduction in the antero-posterior direction. Also, a significant positive association between the total molar area and the molar ratios M2/M1 and M3/M1 was observed. In the experimental models, growth alteration caused by systemic factors (protein subnutrition and reduced growth hormone) resulted in a reduction of total molar area associated with changes in molar proportions. The latter are consistent with an increased antero-posterior inhibition. Overall, these results suggest that alterations in the systemic factors that control molar area can produce changes in the proportion of activators and inhibitors, and contribute in turn to inter-population differentiation in molar proportions.