Abstract
Bird necks display unparalleled levels of morphological diversity compared to other vertebrates, yet it is unclear what factors have structured this variation. Using three-dimensional geometric morphometrics and multivariate statistics, we show that the avian cervical column is a hierarchical morpho-functional appendage, with varying magnitudes of ecologically driven osteological variation at different scales of organization. Contrary to expectations given the widely varying ecological functions of necks in different species, we find that regional modularity of the avian neck is highly conserved, with an overall structural blueprint that is significantly altered only by the most mechanically demanding ecological functions. Nevertheless, the morphologies of vertebrae within subregions of the neck show more prominent signals of adaptation to ecological pressures. We also find that both neck length allometry and the nature of neck elongation in birds are different from other vertebrates. In contrast with mammals, neck length scales isometrically with head mass and, contrary to previous work, we show that neck elongation in birds is achieved predominantly by increasing vertebral lengths rather than counts. Birds therefore possess a cervical spine that may be unique in its versatility among extant vertebrates, one that, since the origin of flight, has adapted to function as a surrogate forelimb in varied ecological niches.
Highlights
Why and at what scale phenotypic variation arises in morphological structures are among the most important questions in evolutionary biology [1]
Our analyses highlight that the avian cervical column is a hierarchical morpho-functional appendage, with varying magnitudes of phenotypic variation at different scales
Contrary to previous expectations [5,6,54,55], that lengthening of vertebrae rather than cervicalization drives neck elongation in birds, and that neck length scales isometrically with both body and head size with little ecological signal
Summary
Why and at what scale phenotypic variation arises in morphological structures are among the most important questions in evolutionary biology [1]. Our analysis recovers five morphological sub-regions, consistent with Hox gene expression limits [10], in representative birds from all major extant taxonomic sub-groups, locomotor and tropic ecologies Analysis of this homologous five-region structure highlights a highly scale-dependent nature of phenotypic variation in the avian neck, with varying degrees of ecological adaptation at macro- to micro-morphological scales. To our knowledge, this is the first quantitative demonstration of hierarchical ecologically driven morphological organization of the vertebrate neck and suggests that similar assessments of anatomical variation at different scales could provide important insight into diversity and adaptation in the necks of other amniote groups and across the vertebrate skeleton
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