Anatomical Network Analysis Shows Decoupling of Modular Lability and Complexity in the Evolution of the Primate Skull

Abstract

Modularity and complexity go hand in hand in the evolution of the skull of primates. Because analyses of these two parameters often use different approaches, we do not know yet how modularity evolves within, or as a consequence of, an also-evolving complex organization. Here we use a novel network theory-based approach (Anatomical Network Analysis) to assess how the organization of skull bones constrains the co-evolution of modularity and complexity among primates. We used the pattern of bone contacts modeled as networks to identify connectivity modules and quantify morphological complexity. We analyzed whether modularity and complexity evolved coordinately in the skull of primates. Specifically, we tested Herbert Simon’s general theory of near-decomposability, which states that modularity promotes the evolution of complexity. We found that the skulls of extant primates divide into one conserved cranial module and up to three labile facial modules, whose composition varies among primates. Despite changes in modularity, statistical analyses reject a positive feedback between modularity and complexity. Our results suggest a decoupling of complexity and modularity that translates to varying levels of constraint on the morphological evolvability of the primate skull. This study has methodological and conceptual implications for grasping the constraints that underlie the developmental and functional integration of the skull of humans and other primates.

Morphological integration affects the evolution of midline cranial base, lateral basicranium, and face across primates

“…Our results therefore underline the importance of the definition of module boundaries in the interpretation of integration analyses (Goswami & Polly, ; Klingenberg, ). A corpus of studies based on anatomical network analyses (ANA), also found a greater modularity between facial and basicranial structures (Esteve‐Altava, ; Esteve‐Altava, Boughner, Diogo, Villmoare, & Rasskin‐Gutman, ; Esteve‐Altava, Marugán‐Lobón, Botella, Bastir, & Rasskin‐Gutman, ). This type of study differs from GMM approaches by defining modularity based on the topological relations (i.e., physical articulations) among bones in a predefined network model.…”

Comparative Myology and Evolution of Marsupials and Other Vertebrates, With Notes on Complexity, Bauplan, and “Scala Naturae”

“…Therefore, it is likely the organization of motor systems was the subject of broad functional changes during the transition to and evolutionary history of mammals, and that in at least some cases fewer musculoskeletal structures have finer motor control due to a more complex neural organization. Also, in recent years we have been working to develop alternative ways of measuring morphological complexity in the organization of body parts, such as anatomical network analyses that take into account not only the number and presence/absence of anatomical structures but also their topological connectivity (e.g., Esteve‐Altava, ; Diogo et al, ). We plan to apply such tools to the data obtained in the present article in future works, in order to compare “pure complexity” from comparative studies with the organizational complexity of systems biology data obtained from anatomical network analyses.…”

Evolutionary developmental pathology and anthropology: A new field linking development, comparative anatomy, human evolution, morphological variations and defects, and medicine

“…For instance, the reduction of several skull bones (Williston's law) is a macroevolutionary trend (found across the ecologically diverse tetrapod clade) that can be explained by internal bias favoring the loss of the least connected bones (Esteve‐Altava et al, ). We have recently expanded anatomical network analyses to include also muscle–muscle and muscle–bone connections, and to study human pathology as well (Esteve‐Altava et al, ; Smith et al, ). Other recent studies on modularity, for instance about the modular heterochrony of dermal vs. endochondral bones, have also provided examples of internal constraints that might have been particularly important in vertebrate macroevolution (Koyabu et al, ).…”