Musculoskeletal networks reveal topological disparity in mammalian neck evolution

Abstract Background The increase in locomotor and metabolic performance during mammalian evolution was accompanied by the limitation of the number of cervical vertebrae to only seven. In turn, nuchal muscles underwent a reorganization while forelimb muscles expanded into the neck region. As variatio...

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Main Authors: Patrick Arnold, Borja Esteve-Altava, Martin S. Fischer
Format: Article
Language:English
Published: BMC 2017-12-01
Series:BMC Evolutionary Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12862-017-1101-1
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spelling doaj-4694edf01f994977b50b0e3da938627a2021-09-02T09:57:19ZengBMCBMC Evolutionary Biology1471-21482017-12-0117111810.1186/s12862-017-1101-1Musculoskeletal networks reveal topological disparity in mammalian neck evolutionPatrick Arnold0Borja Esteve-Altava1Martin S. Fischer2Department of Human Evolution, Max Planck Institute for Evolutionary AnthropologyStructure & Motion Lab, Department of Comparative Biomedical Sciences, Royal Veterinary CollegeDepartment of Human Evolution, Max Planck Institute for Evolutionary AnthropologyAbstract Background The increase in locomotor and metabolic performance during mammalian evolution was accompanied by the limitation of the number of cervical vertebrae to only seven. In turn, nuchal muscles underwent a reorganization while forelimb muscles expanded into the neck region. As variation in the cervical spine is low, the variation in the arrangement of the neck muscles and their attachment sites (i.e., the variability of the neck’s musculoskeletal organization) is thus proposed to be an important source of neck disparity across mammals. Anatomical network analysis provides a novel framework to study the organization of the anatomical arrangement, or connectivity pattern, of the bones and muscles that constitute the mammalian neck in an evolutionary context. Results Neck organization in mammals is characterized by a combination of conserved and highly variable network properties. We uncovered a conserved regionalization of the musculoskeletal organization of the neck into upper, mid and lower cervical modules. In contrast, there is a varying degree of complexity or specialization and of the integration of the pectoral elements. The musculoskeletal organization of the monotreme neck is distinctively different from that of therian mammals. Conclusions Our findings reveal that the limited number of vertebrae in the mammalian neck does not result in a low musculoskeletal disparity when examined in an evolutionary context. However, this disparity evolved late in mammalian history in parallel with the radiation of certain lineages (e.g., cetartiodactyls, xenarthrans). Disparity is further facilitated by the enhanced incorporation of forelimb muscles into the neck and their variability in attachment sites.http://link.springer.com/article/10.1186/s12862-017-1101-1Anatomical network analysisNetwork theoryForelimb evolutionMammalian cervical spineSlothsMeristic constraints
collection DOAJ
language English
format Article
sources DOAJ
author Patrick Arnold
Borja Esteve-Altava
Martin S. Fischer
spellingShingle Patrick Arnold
Borja Esteve-Altava
Martin S. Fischer
Musculoskeletal networks reveal topological disparity in mammalian neck evolution
BMC Evolutionary Biology
Anatomical network analysis
Network theory
Forelimb evolution
Mammalian cervical spine
Sloths
Meristic constraints
author_facet Patrick Arnold
Borja Esteve-Altava
Martin S. Fischer
author_sort Patrick Arnold
title Musculoskeletal networks reveal topological disparity in mammalian neck evolution
title_short Musculoskeletal networks reveal topological disparity in mammalian neck evolution
title_full Musculoskeletal networks reveal topological disparity in mammalian neck evolution
title_fullStr Musculoskeletal networks reveal topological disparity in mammalian neck evolution
title_full_unstemmed Musculoskeletal networks reveal topological disparity in mammalian neck evolution
title_sort musculoskeletal networks reveal topological disparity in mammalian neck evolution
publisher BMC
series BMC Evolutionary Biology
issn 1471-2148
publishDate 2017-12-01
description Abstract Background The increase in locomotor and metabolic performance during mammalian evolution was accompanied by the limitation of the number of cervical vertebrae to only seven. In turn, nuchal muscles underwent a reorganization while forelimb muscles expanded into the neck region. As variation in the cervical spine is low, the variation in the arrangement of the neck muscles and their attachment sites (i.e., the variability of the neck’s musculoskeletal organization) is thus proposed to be an important source of neck disparity across mammals. Anatomical network analysis provides a novel framework to study the organization of the anatomical arrangement, or connectivity pattern, of the bones and muscles that constitute the mammalian neck in an evolutionary context. Results Neck organization in mammals is characterized by a combination of conserved and highly variable network properties. We uncovered a conserved regionalization of the musculoskeletal organization of the neck into upper, mid and lower cervical modules. In contrast, there is a varying degree of complexity or specialization and of the integration of the pectoral elements. The musculoskeletal organization of the monotreme neck is distinctively different from that of therian mammals. Conclusions Our findings reveal that the limited number of vertebrae in the mammalian neck does not result in a low musculoskeletal disparity when examined in an evolutionary context. However, this disparity evolved late in mammalian history in parallel with the radiation of certain lineages (e.g., cetartiodactyls, xenarthrans). Disparity is further facilitated by the enhanced incorporation of forelimb muscles into the neck and their variability in attachment sites.
topic Anatomical network analysis
Network theory
Forelimb evolution
Mammalian cervical spine
Sloths
Meristic constraints
url http://link.springer.com/article/10.1186/s12862-017-1101-1
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