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.
Highlights
The influential “frameshift” hypothesis postulates an evolutionary change in the phenotype of one or more digits in the lineage leading to birds (Wagner and Gauthier 1999; Stewart et al 2019)
In order to examine how digit IV became so reduced, we have studied the phalanx-forming region (Suzuki et al 2008; Huang et al 2016; Hiscock et al 2017), a collection of Sox9expressing mesenchyme cells at the tips of the digits, that is essential for digit growth and patterning (Suzuki et al 2008; Huang et al 2016; Hiscock et al 2017)
The apoptosis that we have demonstrated in wing digit IV, and loss of phalanxforming region, would explain why the polarizing region of the wing gives rise only to marginal soft tissue (Towers et al 2011)
Summary
The influential “frameshift” hypothesis postulates an evolutionary change in the phenotype of one or more digits in the lineage leading to birds (Wagner and Gauthier 1999; Stewart et al 2019). The hypothesis aimed to reconcile conflicting data from developmental biology (Welten et al 2005; Richardson 2012; de Bakker et al 2013) and paleontology (Wagner and Gauthier 1999) about the homologies of the wing digits. Developmental data suggest an evolutionary loss of digits I and V from the ancestral pentadactyl forelimb (KundraT et al 2002).
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