First anatomical network analysis of fore- and hindlimb musculoskeletal modularity in bonobos, common chimpanzees, and humans

Rui Diogo,Campbell Rolian,Julia L Molnar,Borja Esteve-Altava

doi:10.1038/s41598-018-25262-6

Rui Diogo, Campbell Rolian + Show 2 more

Open Access

https://doi.org/10.1038/s41598-018-25262-6

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Abstract

Studies of morphological integration and modularity, and of anatomical complexity in human evolution typically focus on skeletal tissues. Here we provide the first network analysis of the musculoskeletal anatomy of both the fore- and hindlimbs of the two species of chimpanzee and humans. Contra long-accepted ideas, network analysis reveals that the hindlimb displays a pattern opposite to that of the forelimb: Pan big toe is typically seen as more independently mobile, but humans are actually the ones that have a separate module exclusively related to its movements. Different fore- vs hindlimb patterns are also seen for anatomical network complexity (i.e., complexity in the arrangement of bones and muscles). For instance, the human hindlimb is as complex as that of chimpanzees but the human forelimb is less complex than in Pan. Importantly, in contrast to the analysis of morphological integration using morphometric approaches, network analyses do not support the prediction that forelimb and hindlimb are more dissimilar in species with functionally divergent limbs such as bipedal humans.

Highlights

Studies of morphological integration and modularity, and of anatomical complexity in human evolution typically focus on skeletal tissues
Primate limbs are morphologically diverse, and much of this variation in musculoskeletal anatomy correlates with locomotor function
In addition to external/ecological pressures, development may constrain the evolution of limb musculoskeletal anatomy

Summary

Pan paniscus forelimb

While in Homo sapiens the complexity is higher in the hindlimb (SI1 Table 15). At the skeletal level results are not conclusive, the values of C indicating that the forelimb is more complex than the hindlimb, but the values of D and L suggesting otherwise. The first concerns the evolution of human bipedalism and complexity: H1) does the complexity in bone-bone and muscle-bone connectivity in the fore- vs hindlimb correlate with the functional complexity of that specific limb, which we predicted would result in decreased network complexity of our hindlimbs compared to those of chimpanzees? At the skeletal level, the three species have the same topological organization in their forelimbs and hindlimbs, respectively, their forelimb-hindlimb similarity is the same This might suggest that there is not a clear division between humans and Pan regarding this feature, and that each species followed a different evolutionary trajectory, which in this context lead to humans and bonobos having a higher inter-limb similarity by convergence. We hope this paper will pave the way for such future works on the musculoskeletal network organization of the limbs of other primates, mammals and tetrapods

Materials and Methods

Findings

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