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 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.

The role of many-to-one mapping of vertebral form to function in Psittaciform tripedal locomotion

“…The findings presented here for parrots may have implications for the mechanisms behind broader avian neck evolution, as the ecological signal in cervical morphological variation is similarly low across Aves (3,20,30). The similarly weak influence of ecology on neck morphology across all birds suggests that many-to-one mapping may be present across Aves.…”

“…We then performed morphological analyses on a pooled dataset that contained all vertebrae (C2, C25%, C50%, C75% and the last cervical vertebrae) for all species, as well as separate analyses for each vertebral level. This allowed us to study morphological evolution across the entire parrot neck and at the level of individual vertebrae across the cervical spine (31). We calculated multivariate Blomberg’s K (K mult ) using the function physig() within the ‘geomorph’ R package to estimate the impact of phylogeny on the morphological variation of parrot cervical vertebrae (43).…”

“…Scans for all 48 species were segmented in Amira 3D (version 2021.1, Visualization Science Group, Thermo Fisher Scientific) and the digital models outputted were cleaned and further processed in MeshLab (32). To account for the variation in total cervical vertebral counts between species we analysed 2 homologous vertebrae (the second cervical vertebrae, C2, and the last cervical vertebrae) as well as 3 ‘functionally homologous’ vertebrae (vertebrae at 25%, 50% and 75% along the cervical column) (20,33,34). A vertebral landmark scheme consisting of 22 fixed landmarks (Supplementary Figure 1, Supplementary Table 2) was constructed based on schemes from prior avian vertebral morphometric studies (3,20,35,36).…”

“…To account for the variation in total cervical vertebral counts between species we analysed 2 homologous vertebrae (the second cervical vertebrae, C2, and the last cervical vertebrae) as well as 3 ‘functionally homologous’ vertebrae (vertebrae at 25%, 50% and 75% along the cervical column) (20,33,34). A vertebral landmark scheme consisting of 22 fixed landmarks (Supplementary Figure 1, Supplementary Table 2) was constructed based on schemes from prior avian vertebral morphometric studies (3,20,35,36). We next calculated head volumes by subjecting digital skull models for each species to an α-shape fitting algorithm that is part of an in-house modified version of the ‘alphavol’ package for MatLab (3,37).…”

“…This decoupling allows for one morphological trait to accommodate multiple functions, and highlights that the morphological form does not always directly correlate with function (17,19). Many-to-one mapping may be exemplified by the avian neck as it performs a wide range of functions despite a similarity in its overall structure between species, and this is evidenced by recent work which observed that the regional modularity of the avian neck is conserved across many species, only adapting to highly specialised functions such as carnivory (3,20). Here we investigate whether the psittaciform neck breaks this pattern of conservatism in avian neck morphology in order to adapt to function during locomotion, or if many-to-one mapping and changes to neuronal control of parrot neck musculature are responsible for this novel behaviour.…”