Dataset Information

Selection on Phalanx Development in the Evolution of the Bird Wing.

ABSTRACT: The frameshift hypothesis is a widely accepted model of bird wing evolution. This hypothesis postulates a shift in positional values, or molecular-developmental identity, that caused a change in digit phenotype. The hypothesis synthesized developmental and paleontological data on wing digit homology. The "most anterior digit" (MAD) hypothesis presents an alternative view based on changes in transcriptional regulation in the limb. The molecular evidence for both hypotheses is that the MAD expresses Hoxd13 but not Hoxd11 and Hoxd12. This digit I "signature" is thought to characterize all amniotes. Here, we studied Hoxd expression patterns in a phylogenetic sample of 18 amniotes. Instead of a conserved molecular signature in digit I, we find wide variation of Hoxd11, Hoxd12, and Hoxd13 expression in digit I. Patterns of apoptosis, and Sox9 expression, a marker of the phalanx-forming region, suggest that phalanges were lost from wing digit IV because of early arrest of the phalanx-forming region followed by cell death. Finally, we show that multiple amniote lineages lost phalanges with no frameshift. Our findings suggest that the bird wing evolved by targeted loss of phalanges under selection. Consistent with our view, some recent phylogenies based on dinosaur fossils eliminate the need to postulate a frameshift in the first place. We suggest that the phenotype of the Archaeopteryx lithographica wing is also consistent with phalanx loss. More broadly, our results support a gradualist model of evolution based on tinkering with developmental gene expression.

SUBMITTER: de Bakker MAG

PROVIDER: S-EPMC8476175 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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Selection on Phalanx Development in the Evolution of the Bird Wing.

de Bakker Merijn A G MAG van der Vos Wessel W de Jager Kaylah K Chung Wing Yu WY Fowler Donald A DA Dondorp Esther E Spiekman Stephan N F SNF Chew Keng Yih KY Xie Bing B Jiménez Rafael R Bickelmann Constanze C Kuratani Shigeru S Blazek Radim R Kondrashov Peter P Renfree Marilyn B MB Richardson Michael K MK

Molecular biology and evolution 20210901 10

The frameshift hypothesis is a widely accepted model of bird wing evolution. This hypothesis postulates a shift in positional values, or molecular-developmental identity, that caused a change in digit phenotype. The hypothesis synthesized developmental and paleontological data on wing digit homology. The "most anterior digit" (MAD) hypothesis presents an alternative view based on changes in transcriptional regulation in the limb. The molecular evidence for both hypotheses is that the MAD express ...[more]

PMID: 34164688

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Project description:BackgroundBirds 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.ResultsWe 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.ConclusionSynthesizing 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.

Dataset Information

Selection on Phalanx Development in the Evolution of the Bird Wing.

Publications

Selection on Phalanx Development in the Evolution of the Bird Wing.

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