Anatomical network analysis of the
musculoskeletal system reveals integration
loss and parcellation boost during
the ﬁns-to-limbs transition
Julia L. Molnar,
John R. Hutchinson,
and Rui Diogo
Structure and Motion Lab, Department of Comparative Biomedical Sciences, Royal Veterinary College, United Kingdom
Department of Anatomy, Howard University College of Medicine, Washington, District of Columbia 20059
Department of Anatomy and Medical Imaging, University of Auckland, New Zealand
Received March 21, 2017
Accepted January 14, 2018
Tetrapods evolved from within the lobe-ﬁnned ﬁshes around 370 Ma. The evolution of limbs from lobe-ﬁns entailed a major
reorganization of the skeletal and muscular anatomy of appendages in early tetrapods. Concurrently, a degree of similarity
between pectoral and pelvic appendages also evolved. Here, we compared the anatomy of appendages in extant lobe-ﬁnned ﬁshes
(Latimeria and Neoceratodus) and anatomically plesiomorphic amphibians (Ambystoma, Salamandra) and amniotes (Sphenodon)
to trace and reconstruct the musculoskeletal changes that took place during the ﬁns-to-limbs transition. We quantiﬁed the anatomy
of appendages using network analysis. First, we built network models—in which nodes represent bones and muscles, and links
represent their anatomical connections—and then we measured network parameters related to their anatomical integration,
heterogeneity, and modularity. Our results reveal an evolutionary transition toward less integrated, more modular appendages.
We interpret this transition as a diversiﬁcation of muscle functions in tetrapods compared to lobe-ﬁnned ﬁshes. Limbs and lobe-ﬁns
show also a greater similarity between their pectoral and pelvic appendages than ray-ﬁns do. These ﬁndings on extant species
provide a basis for future quantitative and comprehensive reconstructions of the anatomy of limbs in early tetrapod fossils, and a
way to better understand the ﬁns-to-limbs transition.
Extant phylogenetic bracketing, pectoral-pelvic similarity, sarcopterygii, serial homology, similarity bottlenecks.
The limbs of tetrapods evolved from the lobe-fins of sarcoptery-
gian fishes around 370 Ma through a series of anatomical inno-
vations (Fig. 1A). Although at first sight the limbs and lobe-fins
of extant species look different, they share some deep similarities
in their anatomical organization—the way in which bones and
muscles are arranged together—that reveal their common origin.
The study of the origin of limbs involves working with uncer-
tain homologies between anatomical structures, reconstructing
soft tissue in transitional fossil taxa, and gathering information
from the few extant taxa close to the fins-to-limbs transition (e.g.,
Molnar et al. 2017). These circumstances present a challenge for
quantitative methods comparing the anatomical organization of
appendages, especially in very disparate forms.
To overcome this problem, here we propose to, and exem-
plify the use of, a systems biology approach to the study of the
fins-to-limbs transition. A systems biology approach to anatomy
focuses on the quantification and comparison of anatomical orga-
nization, which other properties such as integration, modularity,
and functioning depend on (Rasskin-Gutman and Esteve-Altava
2014). The intuitive notion of anatomical organization evokes a
group of parts establishing physical interactions that define the
overall structure and function of a system (Weiss 1971). Here,
we formalized the anatomical organization of fins and limbs us-
ing network models that capture the basic physical relationships
among bones and muscles. Working with network models of the
musculoskeletal anatomy of appendages allows us to directly
2018 The Author(s). Evolution published by Wiley Periodicals, Inc. on behalf of The Society for the Study of Evolution.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original
work is properly cited.
Evolution 72-3: 601–618