Abstract
A fundamental challenge of morphology is to identify the underlying evolutionary and developmental mechanisms leading to correlated phenotypic characters. Patterns and magnitudes of morphological integration and their association with environmental variables are essential for understanding the evolution of complex phenotypes, yet the nature of the relevant selective pressures remains poorly understood. In this study, the adaptive significance of morphological integration was evaluated through the association between feeding mechanics, ingestive behavior and craniofacial variation. Five capuchin species were examined, Cebus apella sensu stricto, Cebus libidinosus, Cebus nigritus, Cebus olivaceus and Cebus albifrons. Twenty three-dimensional landmarks were chosen to sample facial regions experiencing high strains during feeding, characteristics affecting muscular mechanical advantage and basicranial regions. Integration structure and magnitude between and within the oral and zygomatic subunits, between and within blocks maximizing modularity and within the face, the basicranium and the cranium were examined using partial-least squares, eigenvalue variance, integration indices compared inter-specifically at a common level of sampled population variance and cluster analyses. Results are consistent with previous findings reporting a relative constancy of facial and cranial correlation patterns across mammals, while covariance magnitudes vary. Results further suggest that food material properties structure integration among functionally-linked facial elements and possibly integration between the face and the basicranium. Hard-object-feeding capuchins, especially C.apella s.s., whose faces experience particularly high biomechanical loads are characterized by higher facial and cranial integration especially compared to C.albifrons, likely because morphotypes compromising feeding performance are selected against in species relying on obdurate fallback foods. This is the first study to report a link between food material properties and facial and cranial integration. Furthermore, results do not identify the consistent presence of cranial modules yielding support to suggestions that despite the distinct embryological imprints of its elements the cranium of placental mammals is not characterized by a modular architecture.
Highlights
Morphological integration represents a widespread phenomenon, manifested in the coordinated change among phenotypic characters of an organism (e.g., [1,2,3,4,5,6])
The apelloid capuchins are characterized by higher between-block RV coefficients than C. albifrons and C. olivaceus under the oral-zygomatic Partial Least-Squares analyses (PLS) containing an allometric component or carried out on residuals regressed on centroid size, and under the maximum facial modularity PLS containing an allometric component
We further report that some aspects of the face of C. olivaceus are reminiscent of the apelloids and might be more biomechanically advantageous relative to C. albifrons, C. olivaceus is characterized by a shorter lower face and by more posteromedially positioned zygomatic roots
Summary
Morphological integration represents a widespread phenomenon, manifested in the coordinated change among phenotypic characters of an organism (e.g., [1,2,3,4,5,6]). Functionally-linked characters are expected to evolve a common genetic basis, because genetic integration among these traits may avoid deleterious independent variation (which would disrupt functional systems), and so facilitate evolution by natural selection [11]. Cheverud [12,13,14,15,5], Lande [16,17,18] and Wagner et al [19] suggest that quantitative genetic theory is consistent with Olson and Miller’s [6] prediction that adaptively favorable coordinated units of evolution exist, and that the underlying pattern of genetic correlation depends on the patterns of stabilizing selection and new variation/covariation produced by mutation
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