The Effect of Dietary Adaption on Cranial Morphological Integration in Capuchins (Order Primates, Genus Cebus)

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.

Taxonomic Implications of Molar Morphology Variability in Capuchins

“…Similar adaptations to dietary preference might affect fitness-related characters (Kawecki and Ebert 2004), leading to incorrect estimates for phylogenetically distantly related taxa. The functional effect of mastication may also result in integration of molars with other craniofacial traits and, therefore, be affected by morphological changes in those regions (Makedonska et al 2012;Marroig et al 2009;Shirai and Marroig 2010;Smits and Evans 2012). Closely related species inhabiting close geographic areas are expected to show lower phenotypic diversity than more distantly related and geographically distant ones (Kamilar 2009), as observed in the Sapajus species from Caatinga and Cerrado, the Amazon basin and Atlantic forests (Silva 2001;Lynch Alfaro et al 2012a, b).…”

“…Analyses of morphological, ecological, biogeographic, behavioral, and molecular data have shown significant differences among capuchins, indicating that this group comprises two separate monophyletic clades: Cebus, or the gracile capuchins, and Sapajus, or the robust species (Lynch Alfaro et al 2012a, b;Makedonska et al 2012;Wright et al 2014). The taxonomy of capuchins is based mainly on a revision by Hershkovitz (1949Hershkovitz ( , 1955 and Hill (1960) and several publications have focused on the taxonomy and geographic variation of capuchin species (Groves 2001(Groves , 2005Rylands et al 2005Rylands et al , 2009Rylands et al , 2012.…”

“…The taxonomy of capuchins is based mainly on a revision by Hershkovitz (1949Hershkovitz ( , 1955 and Hill (1960) and several publications have focused on the taxonomy and geographic variation of capuchin species (Groves 2001(Groves , 2005Rylands et al 2005Rylands et al , 2009Rylands et al , 2012. Diverse studies have supported the division of Cebus into two genera based on morphological and genetic differences, (Lynch Alfaro et al 2012a, 2012bMakedonska et al 2012;Silva 2001;Springer et al 2012;Wright et al 2014;Fig. 1), although dividing the clade may constitute taxonomic inflation (Rosenberger 2012).…”

“…This taxonomy recognizes eight robust species, including an Atlantic capuchin clade with S. nigritus (black capuchin), S. robustus (crested capuchin), and S. xanthosternos (yellow-breasted or buffy-headed); an Amazonian group with S. apella (brown capuchin), S. cay (hooded capuchin), S. macrocephalus (large-headed capuchin) (Silva 2001), and S. flavius (blonde capuchin), the last rediscovered in northeastern Brazil (Oliveira and Langguth 2006); and S. libidinosus (bearded capuchin) from the Cerrado-Caatinga in Brazil. The robust capuchins show a sagittal crest in males and a relatively stronger musculoskeletal system than gracile capuchins (Lynch Alfaro et al 2012b;Makedonska et al 2012;Silva 2001;Wright 2005Wright , 2007Wright et al 2014). The diversification of the clade of Cebus occurred in the Amazonian forest.…”

“…For example, S. apella shows a more anteriorly placed attachment of the temporalis and masseter muscles and a wider incisor and greater mandibular corpus cross-sectional areas at the canines and molars than those of C. olivaceus (Wright 2005). These biomechanical differences would grant S. apella access to a greater variety of food resources as compared to Cebus (Byron 2009;Makedonska et al 2012;Taylor and Vinyard 2009;Wright 2005;Wright et al 2009). A study in Guyana, based on the factors that affect habitat use, showed low sighting rates of both species where they were found to be sympatric.…”