Evolution and development of the bird chondrocranium

Abstract

Background Birds exhibit an enormous diversity in adult skull shape (disparity), while their embryonic chondrocrania are considered to be conserved across species. However, there may be chondrocranial features that are diagnostic for bird clades or for Aves as a whole. We synthesized and analyzed information on the sequence of chondrification of 23 elements in ten bird species and five outgroups. Moreover, we critically considered the developmental morphology of the chondrocrania of 21 bird species and examined whether the diversity in adult skull shape is reflected in the development of the embryonic skull, and whether there are group-specific developmental patterns. Results We found that chondrocranial morphology is largely uniform in its major features, with some variation in the presence or absence of fenestrae and other parts. In kiwis (Apteryx), the unique morphology of the bony skull in the orbito-nasal region is reflected in its chondrocranial anatomy. Finally, differences in morphology and chondrification sequence may distinguish between different Palaeognathae and Neognathae and between the Galloanserae and Neoaves. The sequence of chondrification is largely conserved in birds, but with some variation in most regions. The peri- and prechordal areas in the base of the chondrocranium are largely conserved. In contrast to the outgroups, chondrification in birds starts in the acrochordal cartilage and the basicranial fenestra is formed secondarily. Further differences concern the orbital region, including early chondrification of the pila antotica and the late formation of the planum supraseptale. Conclusion Synthesizing information on chondrocranial development confronts terminological issues and a lack of comparable methods used (e.g., different staining; whole-mounts versus histology). These issues were taken into consideration when assessing differences across species. The summary of works on avian chondrocranial development, covered more than a century, and a comparison of the chondrification sequence among birds could be conducted. Future studies could test the hypothesis that chondrocranial disparity in Aves, in terms of the shape and proportion of individual elements, could be as large as adult skull disparity, despite conserved developmental patterns and the richness of forms in other (dermal) portions of the skull.

Sequence of chondrocranial development in basal anurans—Let’s make a cranium

“…We used data from earlier studies describing the chondrogenesis in X. laevis [ 21 ] and B. orientalis [ 25 ] to compare our recent results. We scored additional cartilaginous features in both species to build a uniform database for future comparison with a wider range of species.…”

“…The sequences were updated from Lukas and Olsson [ 21 , 25 ] and the updated tables are presented here (Tables 2 , 3 ).…”

“…An admandibular cartilage is present in a similar condition as described in other species of Discoglossus [ 28 , 30 ], the closely related Alytes [ 29 , 30 ], and the basalmost neobatrachian Heleophryne [ 31 – 33 ]. Among Discoglossoids, species of Bombina lack this cartilage [ 25 , 29 ]. Therefore, the presence of the admandibular cartilage might be an apomorphic feature of the Alytidae (comprising Alytinae and Discoglossinae) and distinguish them from the Bombinatoridae, as also suggested by recent molecular based phylogenies [ 34 – 36 ].…”

“…The sequence of development for chondrocranium elements was recently studied for two basal frog species ( Xenopus laevis and Bombina orientalis ). These studies identified several patterns which may be candidates for the basal pattern of cartilage formation in anurans [ 21 , 25 ]. (1) The first mesenchymal Anlage which appears during the chondrocranial development is the Anlage of the ceratohyal, which is also the first structure that chondrifies.…”

“…1 ). X. laevis and B. orientalis were previously described [ 21 , 25 ] and we only updated their developmental sequences where needed. The chondrocranium development of D. scovazzi will be described in detail.…”