Modularity of the Neck in Birds (Aves)

Abstract

The neck connects the head and the trunk and is the key structure allowing all movements of the head. The neck morphology of birds is the most variable among living tetrapods, including significant differences in the number and shape of the cervical vertebrae. Despite these differences, according to the literature, three morphofunctional regions (i.e., modules) have been identified along the neck. However, this regionalization has not been quantitatively tested through a geometric morphomet-ric approach applied to the cervical vertebrae. Based on the examination of 187 cervical vertebrae belonging to 16 species with various ecologies, we revealed a common modular structure of the neck using 3D surface geometric morphometrics. We adopted an approach without a priori clustering to identify modules along the neck. The phylogenetic influence on each module was tested. Then, each module was digitally reconstructed as a 3D vertebral model, and postural characteristics were studied. We characterized 9 modules: 7 are transpecific, being shared by at least 2 and up to 15 species. Two modules are specific to species with particularly long necks. The modularity pattern appears to be tightly linked to morphofunctional aspects and partially to phylogeny. In contrast, feeding ecology seems to be more closely related to the chaining of modules (the neck) than to the modules themselves. A study of postural properties revealed that each modular unit exhibits a characteristic curvature. Overall, the modular structure of the neck corresponds to the three traditional functional regions. However, the results also revealed unexpected pattern complexity, including subdivisions within these regions. The study of the patterns of modularity is therefore a relevant approach for challenging the three-functional-region hypothesis and allowed us to identify the structure of the diversity of the necks of birds.

Evolution of the Mammalian Neck from Developmental, Morpho-Functional, and Paleontological Perspectives

“…Neck modularity is a trend observable in other amniotes, too, but they have mostly more modules with smoother transition (morphologically) between adjacent modules (Boas 1929;Böhmer et al 2015;Böhmer and Werneburg 2017). Even in non-mammalian amniotes with a comparatively low number of cervical vertebrae (turtles: 8; broadbill: 11; cockatoo: 11; hummingbird: 11; woodpecker: 11; penguins: 12-13), four or more modules are identified (Guinard and Marchand 2010;Böhmer and Werneburg 2017;Terray et al 2020). In contrast, the number of modules does not increase in three-toed sloths (Bradypus) with nine cervical vertebrae and their penultimate eighth vertebra resembles the sixth of other mammals, although they have more cervical vertebrae than turtles (Varela-Lasheras et al 2011;Böhmer et al 2018).…”

Evolutionary versatility of the avian neck

“…A key unanswered question concerns the extent to which phenotypic variation of the avian cervical column is driven by adaptive responses to extrinsic (ecological) factors, or by intrinsic (scaling) constraints. This question has not been systematically addressed, due in part to continuing disagreement about how the avian cervical column should be compartmentalized into sub-regions [ 2 , 5 , 6 , 8 – 10 , 27 ] and subsequently compared across species. Over the past 90 years, the avian neck has been sub-divided into between 3 to 9 regions by different workers based on disparate methods, such as variation in joint motion [ 8 , 9 ], qualitative comparative anatomy [ 3 , 6 , 27 , 28 ] and quantitative shape analysis techniques [ 2 , 10 ].…”

“…How, why and at what scale phenotypic variation arises in morphological structures are among the most important questions in evolutionary biology [1]. The avian neck is a highly modular structure [2][3][4][5][6][7][8][9] that displays a wide array of morphological diversity. As the forelimbs are dedicated to flight, the neck has adopted the role of aiding the beak in environmental manipulation tasks [6,10,11].…”

“…Avian vertebral morphologies [3][4][5][6][7][8][9][10] and overall neck length [11] also display a wide diversity of form. However, no previous body of work has quantitatively addressed the ecomorphological signal in this variation, despite the clear functional significance and variability of the avian neck [2,17,18].…”

“…This question has not been systematically addressed, due in part to continuing disagreement about how the avian cervical column should be compartmentalized into sub-regions [2,5,6,[8][9][10]27] and subsequently compared across species. Over the past 90 years, the avian neck has been sub-divided into between 3 to 9 regions by different workers based on disparate methods, such as variation in joint motion [8,9], qualitative comparative anatomy [3,6,27,28] and quantitative shape analysis techniques [2,10]. Crucially, in all these cases the link between regionalization and the genetic and development homology of the neck remains unclear.…”