Anatomical network analysis shows decoupling of modular lability and complexity in the evolution of the primate skull.

Borja Esteve-Altava,Julia C Boughner,Rui Diogo,Diego Rasskin-Gutman,Brian A Villmoare,Ricard V Solé

doi:10.1371/journal.pone.0127653

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.

Highlights

Modularity and complexity are two biological phenomena that occur together in the development and evolution of the skull in humans as well as in non-human primates [1]; PLOS ONE | DOI:10.1371/journal.pone.0127653 May 19, 2015Modularity and Complexity in Primate Skull Networks most studies tend to overlook the tight relationship between these two phenotypic features [2]
Phenotypic modularity varies among primate skulls in the number of modules, in the bones composing these modules, and, as a consequence, in the strength of modularity
The neurocranial module is present in all skull networks and always groups together the occipital, the temporals, and the parietals; often, the neurocranial module includes the sphenoid

Summary

Introduction

Modularity and complexity are two biological phenomena that occur together in the development and evolution of the skull in humans as well as in non-human primates [1]; PLOS ONE | DOI:10.1371/journal.pone.0127653 May 19, 2015Modularity and Complexity in Primate Skull Networks most studies tend to overlook the tight relationship between these two phenotypic features [2]. The study of phenotypic modularity is most commonly directed toward validating genetic, developmental, and functional hypotheses of morphological integration, through the analysis of shape covariation using geometric morphometrics [3]. This approach has been used in many cases to test for the division of the skull of primates in three modules: face, vault, and basicranium [4,5,6]. One might argue that the primate skull has become simpler due to the fusion of the frontal bones (from the last common ancestor of Primates to that of Haplorrhini), and the loss of premaxillary bones (from the last common ancestor of Hominoidea to Homo)

Methods

Results

Conclusion