Evolution of the avian digital pattern

Abstract

Variation in digit number has occurred multiple times in the history of archosaur evolution. The five digits of dinosaur limbs were reduced to three in bird forelimbs, and were further reduced in the vestigial forelimbs of the emu. Regulation of digit number has been investigated previously by examining genes involved in anterior-posterior patterning in forelimb buds among emu ( Dromaius novaehollandiae ), chicken ( Gallus gallus ) and zebra finch ( Taeniopygia guttata ). It was described that the expression of posterior genes are conserved among these three birds, whereas expression of anterior genes Gli3 and Alx4 varied significantly. Here we re-examined the expression pattern of Gli3 and Alx4 in the forelimb of emu, chicken and zebra finch. We found that Gli3 is expressed in the anterior region, although its range varied among species, and that the expression pattern of Alx4 in forelimb buds is broadly conserved in a stage-specific manner. We also found that the dynamic expression pattern of the BMP antagonist Gremlin1 ( Grem1 ) in limb buds, which is critical for autopodial expansion, was consistent with the digital pattern of emu, chicken and zebra finch. Furthermore, in emu, variation among individuals was observed in the width of Grem1 expression in forelimb buds, as well as in the adult skeletal pattern. Our results support the view that the signalling system that regulates the dynamic expression of Grem1 in the limb bud contributes substantially to variations in avian digital patterns.

Atavisms in the avian hindlimb and early developmental polarity of the limb

“…Scale bar: 5 mm shared characters among birds but also the transition from nonavian theropods to modern day birds. [32][33][34] The use of experimental perturbation of limb development in the chicken has played a central role in understanding developmental mechanisms of limb patterning and core mechanisms of limb variation in evolution. Identification of an experimental atavism that reveals the capacity to rekindle previous morphological relationships within the limb is an elegant tool in which to understand the changes that are sufficient to generate these lost morphologies, or conversely, the signals that restrict expression of the ancestral trait.…”

Regulation of vertebrate forelimb development and wing reduction in the flightless emu

“…Subsequently, domains of the chondrogenesis marker Sox9 can be observed, followed by cartilaginous condensations demarcating the typical three digit avian pattern, corresponding to digits II, III, and IV 3 . However, shortly after the formation of the cartilaginous condensations, they regress forming only a single ossified digit (III), present at hatching and persisting in adults 3,119 …”

“…Comparative limb patterning gene expression in chicken, zebra finch and emu revealed dynamic expression of GREM1, which mediates the SHH-FGF signaling axis. 119 Interestingly, it was noted that intraspecific variation in emu GREM1 expression domains corresponded with significant variation in adult wing structures, where some emus possess a remnant digit IV. 119,127 Overall, these subtle yet distinct expression changes support the notion that altered regulation of limb patterning genes underlies wing reduction in the emu.…”

“…This transition was accompanied by a reduction of five to three digits, which can be tracked across archosaur evolution 117 . Disparate avian digit patterns are thought to have arisen through altered limb polarizing activity, namely through altered regulation of hub genes, SHH , HOXD13 , GREM1 , GLI3 , and ALX4 3,118,119 . Additionally, the flightless palaeognath ratites (eg, emu, ostrich, cassowary, rhea, and kiwi) have further lost the ability for powered flight and display variable, lineage‐specific reductions in digit number and wing size (Figure 2).…”

“…Interestingly, these data suggest that emu forelimb digit loss may be achieved through reduced polarizing activity through diminished SHH signaling during the outgrowth and patterning stages of limb development. Comparative limb patterning gene expression in chicken, zebra finch and emu revealed dynamic expression of GREM1 , which mediates the SHH‐FGF signaling axis 119 . Interestingly, it was noted that intraspecific variation in emu GREM1 expression domains corresponded with significant variation in adult wing structures, where some emus possess a remnant digit IV 119,127 .…”