The neck as a keystone structure in avian macroevolution and mosaicism

Abstract Background The origin of birds from non-avian theropod dinosaur ancestors required a comprehensive restructuring of the body plan to enable the evolution of powered flight. One of the proposed key mechanisms that allowed birds to acquire flight and modify the associated anatomical structure...

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Main Authors: Ryan D. Marek, Ryan N. Felice
Format: Article
Language:English
Published: BMC 2023-10-01
Series:BMC Biology
Subjects:
Online Access:https://doi.org/10.1186/s12915-023-01715-x
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author Ryan D. Marek
Ryan N. Felice
author_facet Ryan D. Marek
Ryan N. Felice
author_sort Ryan D. Marek
collection DOAJ
description Abstract Background The origin of birds from non-avian theropod dinosaur ancestors required a comprehensive restructuring of the body plan to enable the evolution of powered flight. One of the proposed key mechanisms that allowed birds to acquire flight and modify the associated anatomical structures into diverse forms is mosaic evolution, which describes the parcelization of phenotypic traits into separate modules that evolve with heterogeneous tempo and mode. Avian mosaicism has been investigated with a focus on the cranial and appendicular skeleton, and as such, we do not understand the role of the axial column in avian macroevolution. The long, flexible neck of extant birds lies between the cranial and pectoral modules and represents an opportunity to study the contribution of the axial skeleton to avian mosaicism. Results Here, we use 3D geometric morphometrics in tandem with phylogenetic comparative methods to provide, to our knowledge, the first integrative analysis of avian neck evolution in context with the head and wing and to interrogate how the interactions between these anatomical systems have influenced macroevolutionary trends across a broad sample of extant birds. We find that the neck is integrated with both the head and the forelimb. These patterns of integration are variable across clades, and only specific ecological groups exhibit either head-neck or neck-forelimb integration. Finally, we find that ecological groups that display head-neck and neck-forelimb integration tend to display significant shifts in the rate of neck morphological evolution. Conclusions Combined, these results suggest that the interaction between trophic ecology and head-neck-forelimb mosaicism influences the evolutionary variance of the avian neck. By linking together the biomechanical functions of these distinct anatomical systems, the cervical vertebral column serves as a keystone structure in avian mosaicism and macroevolution.
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spelling doaj.art-f036dd863229480db6de89dac65c8bf52023-11-20T10:55:42ZengBMCBMC Biology1741-70072023-10-0121111310.1186/s12915-023-01715-xThe neck as a keystone structure in avian macroevolution and mosaicismRyan D. Marek0Ryan N. Felice1Centre for Integrative Anatomy, Department of Cell and Developmental Biology, University College LondonCentre for Integrative Anatomy, Department of Cell and Developmental Biology, University College LondonAbstract Background The origin of birds from non-avian theropod dinosaur ancestors required a comprehensive restructuring of the body plan to enable the evolution of powered flight. One of the proposed key mechanisms that allowed birds to acquire flight and modify the associated anatomical structures into diverse forms is mosaic evolution, which describes the parcelization of phenotypic traits into separate modules that evolve with heterogeneous tempo and mode. Avian mosaicism has been investigated with a focus on the cranial and appendicular skeleton, and as such, we do not understand the role of the axial column in avian macroevolution. The long, flexible neck of extant birds lies between the cranial and pectoral modules and represents an opportunity to study the contribution of the axial skeleton to avian mosaicism. Results Here, we use 3D geometric morphometrics in tandem with phylogenetic comparative methods to provide, to our knowledge, the first integrative analysis of avian neck evolution in context with the head and wing and to interrogate how the interactions between these anatomical systems have influenced macroevolutionary trends across a broad sample of extant birds. We find that the neck is integrated with both the head and the forelimb. These patterns of integration are variable across clades, and only specific ecological groups exhibit either head-neck or neck-forelimb integration. Finally, we find that ecological groups that display head-neck and neck-forelimb integration tend to display significant shifts in the rate of neck morphological evolution. Conclusions Combined, these results suggest that the interaction between trophic ecology and head-neck-forelimb mosaicism influences the evolutionary variance of the avian neck. By linking together the biomechanical functions of these distinct anatomical systems, the cervical vertebral column serves as a keystone structure in avian mosaicism and macroevolution.https://doi.org/10.1186/s12915-023-01715-xAvianNeckAxial skeletonMosaicIntegration
spellingShingle Ryan D. Marek
Ryan N. Felice
The neck as a keystone structure in avian macroevolution and mosaicism
BMC Biology
Avian
Neck
Axial skeleton
Mosaic
Integration
title The neck as a keystone structure in avian macroevolution and mosaicism
title_full The neck as a keystone structure in avian macroevolution and mosaicism
title_fullStr The neck as a keystone structure in avian macroevolution and mosaicism
title_full_unstemmed The neck as a keystone structure in avian macroevolution and mosaicism
title_short The neck as a keystone structure in avian macroevolution and mosaicism
title_sort neck as a keystone structure in avian macroevolution and mosaicism
topic Avian
Neck
Axial skeleton
Mosaic
Integration
url https://doi.org/10.1186/s12915-023-01715-x
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