Borja Esteve-Altava

Grist for Riedl's mill: a network model perspective on the integration and modularity of the human skull.

Riedls concept of burden neatly links development and evolution by ascertaining that structures that show a high degree of developmental co-dependencies with other structures are more constrained in evolution. The human skull can be precisely modeled as an articulated complex system of bones connected by sutures, forming a network of structural co-dependencies. We present a quantitative analysis of the morphological integration, modularity, and hierarchical organization of this human skull network model. Our overall results show that the human skull is a small-world network, with two well-delimited connectivity modules: one facial organized around the ethmoid bone, and one cranial organized around the sphenoid bone. Geometric morphometrics further support this two-module division, stressing the direct relationship between the developmental information enclosed in connectivity patterns and skull shape. Whereas the facial module shows a hierarchy of clustered blocks of bones, the bones of the cranial modules show a regular pattern of connections. We analyze the significance of these arrangements by hypothesizing specific structural roles for the most important bones involved in the formation of both modules, in the context of Riedls burden. We conclude that it is the morphological integration of each group of bones that defines the semi-hierarchical organization of the human skull, reflecting fundamental differences in the ontogenetic patterns of growth and the structural constraints that generate each module. Our study also demonstrates the adequacy of network analysis as an innovative tool to understand the morphological complexity of anatomical systems.

Structural Constraints in the Evolution of the Tetrapod Skull Complexity: Williston’s Law Revisited Using Network Models

Ever since the appearance of the first land vertebrates, the skull has undergone a simplification by loss and fusion of bones in all major groups. This well-documented evolutionary trend is known as “Williston’s Law”. Both loss and fusion of bones are developmental events that generate, at large evolutionary scales, a net reduction in the number of skull bones. We reassess this evolutionary trend by analyzing the patterns of skull organization captured in network models in which nodes represent bones and links represent suture joints. We also evaluate the compensatory process of anisomerism (bone specialization) suggested to occur as a result of this reduction by quantifying the heterogeneity and the ratio of unpaired bones in real skulls. Finally, we perform simulations to test the differential effect of bone losses in skull evolution. We show that the reduction in bone number during evolution is accompanied by a trend toward a more complex organization, rather than toward simplification. Our results indicate that the processes by which bones are lost or fused during development are central to explain the evolution of the morphology of the skull. Our simulations suggest that the evolutionary trend of increasing morphological complexity can be caused as a result of a structural constraint, the systematic loss of less connected bones during development.

Anatomical networks reveal the musculoskeletal modularity of the human head

Mosaic evolution is a key mechanism that promotes robustness and evolvability in living beings. For the human head, to have a modular organization would imply that each phenotypic module could grow and function semi-independently. Delimiting the boundaries of head modules, and even assessing their existence, is essential to understand human evolution. Here we provide the first study of the human head using anatomical network analysis (AnNA), offering the most complete overview of the modularity of the head to date. Our analysis integrates the many biological dependences that tie hard and soft tissues together, arising as a consequence of development, growth, stresses and loads, and motion. We created an anatomical network model of the human head, where nodes represent anatomical units and links represent their physical articulations. The analysis of the human head network uncovers the presence of 10 musculoskeletal modules, deep-rooted in these biological dependences, of developmental and evolutionary significance. In sum, this study uncovers new anatomical and functional modules of the human head using a novel quantitative method that enables a more comprehensive understanding of the evolutionary anatomy of our lineage, including the evolution of facial expression and facial asymmetry.

Network Models in Anatomical Systems

Network theory has been extensively used to model the underlying structure of biological processes. From genetics to ecology, network thinking is changing our understanding of complex systems, specifically how their internal structure determines their overall behavior. Concepts such as hubs, scale-free or small-world networks, common in the complexity literature, are now used more and more in sociology, neurosciences, as well as other anthropological fields. Even though the use of network models is nowadays so widely applied, few attempts have been carried out to enrich our understanding in the classical morphological sciences such as in comparative anatomy or physical anthropology. The purpose of this article is to introduce the usage of network tools in morphology; specifically by building anatomical networks, dealing with the most common analyses and problems, and interpreting their outcome.

In search of morphological modules: a systematic review

Morphological modularity arises in complex living beings due to a semi‐independent inheritance, development, and function of body parts. Modularity helps us to understand the evolvability and plasticity of organismal form, and how morphological variation is structured during evolution and development. For this reason, delimiting morphological modules and establishing the factors involved in their origins is a lively field of inquiry in biology today. Although it is thought that modularity is pervasive in all living beings, actually we do not know how often modularity is present in different morphological systems. We also do not know whether some methodological approaches tend to reveal modular patterns more easily than others, or whether some factors are more related to the formation of modules or the integration of the whole phenotype. This systematic review seeks to answer these type of questions through an examination of research investigating morphological modularity from 1958 to present. More than 200 original research articles were gathered in order to reach a quantitative appraisal on what is studied, how it is studied, and how the results are explained. The results reveal an heterogeneous picture, where some taxa, systems, and approaches are over‐studied, while others receive minor attention. Thus, this review points out various trends and gaps in the study of morphological modularity, offering a broad picture of current knowledge and where we can direct future research efforts.

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

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.

Beyond the functional matrix hypothesis: a network null model of human skull growth for the formation of bone articulations

Craniofacial sutures and synchondroses form the boundaries among bones in the human skull, providing functional, developmental and evolutionary information. Bone articulations in the skull arise due to interactions between genetic regulatory mechanisms and epigenetic factors such as functional matrices (soft tissues and cranial cavities), which mediate bone growth. These matrices are largely acknowledged for their influence on shaping the bones of the skull; however, it is not fully understood to what extent functional matrices mediate the formation of bone articulations. Aiming to identify whether or not functional matrices are key developmental factors guiding the formation of bone articulations, we have built a network null model of the skull that simulates unconstrained bone growth. This null model predicts bone articulations that arise due to a process of bone growth that is uniform in rate, direction and timing. By comparing predicted articulations with the actual bone articulations of the human skull, we have identified which boundaries specifically need the presence of functional matrices for their formation. We show that functional matrices are necessary to connect facial bones, whereas an unconstrained bone growth is sufficient to connect non‐facial bones. This finding challenges the role of the brain in the formation of boundaries between bones in the braincase without neglecting its effect on skull shape. Ultimately, our null model suggests where to look for modified developmental mechanisms promoting changes in bone growth patterns that could affect the development and evolution of the head skeleton.

Characteristic tetrapod musculoskeletal limb phenotype emerged more than 400 MYA in basal lobe-finned fishes

Previous accounts of the origin of tetrapod limbs have postulated a relatively sudden change, after the split between extant lobe-finned fish and tetrapods, from a very simple fin phenotype with only two muscles to the highly complex tetrapod condition. The evolutionary changes that led to the muscular anatomy of tetrapod limbs have therefore remained relatively unexplored. We performed dissections, histological sections, and MRI scans of the closest living relatives of tetrapods: coelacanths and lungfish. Combined with previous comparative, developmental and paleontological information, our findings suggest that the characteristic tetrapod musculoskeletal limb phenotype was already present in the Silurian last common ancestor of extant sarcopterygians, with the exception of the autopod (hand/foot) structures, which have no clear correspondence with fish structures. Remarkably, the two major steps in this long process – leading to the ancestral fin anatomy of extant sarcopterygians and limb anatomy of extant tetrapods, respectively – occurred at the same nodes as the two major similarity bottlenecks that led to the striking derived myological similarity between the pectoral and pelvic appendages within each taxon. Our identification of probable homologies between appendicular muscles of sarcopterygian fish and tetrapods will allow more detailed reconstructions of muscle anatomy in early tetrapods and their relatives.

Evo-Devo insights from pathological networks: exploring craniosynostosis as a developmental mechanism for modularity and complexity in the human skull

Bone fusion has occurred repeatedly during skull evolution in all tetrapod lineages, leading to a reduction in the number of bones and an increase in their morphological complexity. The ontogeny of the human skull includes also bone fusions as part of its normal developmental process. However, several disruptions might cause premature closure of cranial sutures (craniosynostosis), reducing the number of bones and producing new skull growth patterns that causes shape changes. Here, we compare skull network models of a normal newborn with different craniosynostosis conditions, the normal adult stage, and phylogenetically reconstructed forms of a primitive tetrapod, a synapsid, and a placental mammal. Changes in morphological complexity of newborn-to-synostosed skulls are two to three times less than in newborn-to-adult; and even smaller when we compare them to the increases among the reconstructed ancestors in the evolutionary transitions. In addition, normal, synostosed, and adult human skulls show the same connectivity modules: facial and cranial. Differences arise in the internal structure of these modules. In the adult skull the facial module has an internal hierarchical organization, whereas the cranial module has a regular network organization. However, all newborn forms, normal and synostosed, do not reach such kind of internal organization. We conclude that the subtle changes in skull complexity at the developmental scale can change the modular substructure of the newborn skull to more integrated modules in the adult skull, but is not enough to generate radical changes as it occurs at a macroevolutionary scale. The timing of closure of craniofacial sutures, together with the conserved patterns of morphological modularity, highlights a potential relation between the premature fusion of bones and the evolution of the shape of the skull in hominids.

Random Loss and Selective Fusion of Bones Originate Morphological Complexity Trends in Tetrapod Skull Networks

The tetrapod skull has undergone a reduction in number of bones in all major lineages since the origin of vertebrates, an evolutionary trend known as Williston’s Law. Using connectivity relations between bones as a proxy for morphological complexity we showed that this reduction in number of bones generated an evolutionary trend toward more complex skulls. This would imply that connectivity patterns among bones impose structural constraints on bone loss and fusion that increase bone burden due to the formation of new functional and developmental dependencies; thus, the higher the number of connections, the higher the burden. Here, we test this hypothesis by exploring plausible evolutionary scenarios based on selective versus random processes of bone loss and fusion. To do this, we have built a computational model that reduces iteratively the number of bones by loss and fusion, starting from hypothetical ancestral skulls represented as Gabriel networks in which bones are nodes and suture connections are links. Simulation results indicate that losses and fusions of bones affect skull structure differently whether they target bones at random or selectively depending on the number of bone connections. Our findings support a mixed scenario for Williston’s Law: the random loss of poorly connected bones and the selective fusion of the most connected ones. This evolutionary scenario offers a new explanation for the increase of morphological complexity in the tetrapod skull by reduction of bones during development.