The developmental evolution of avian digit homology: an update.

The identity of avian digits has been unresolved since the beginning of evolutionary morphology in the mid-19th century, i.e. as soon as questions of phylogenetic homology have been raised. The main source of concern is the persistent discrepancy between anatomical/paleontological and embryological evidence over the identity of avian digits. In this paper, recent evidence pertaining to the question of avian digit homology is reviewed and the various ideas of how to resolve the disagreement among developmental and phylogenetic evidence are evaluated. Paleontological evidence unequivocally supports the hypothesis that the fully formed digits of maniraptoran theropods are digits DI, DII, and DIII, because the phylogenetic position of Herrerasaurus is resolved, even when hand characters are excluded from the analysis. Regarding the developmental origin of the three digits of the avian hand the discovery of an anterior digit condensation in the limb bud of chickens and ostriches conclusively shows that these three digits are developing from condensations CII, CIII, and CIV. The existence of this additional anterior condensation has been confirmed in four different labs, using four different methods: Alcian blue staining, PNA affinity histochemistry, micro-capillary regression and Sox9 expression. Finally, recent evidence shows that the digit developing from condensation CII has a Hox gene expression pattern that is found in digit DI of mice forelimb and chick hind limbs. The sum of these data supports the idea that digit identity has shifted relative to the location of condensations, known as Frame Shift Hypothesis, such that condensation CII develops into digit DI and condensation CIII develops into digit DII, etc. A review of the literature on the digit identity of the Italian Three-toed Skink or Luscengola (Chalcides chalcides), shows that digit identity frame shifts may not be limited to the bird hand but may be characteristic of "adaptive" digit reduction in amniotes (sensu Steiner, H., Anders, G., 1946. Zur Frage der Entstehung von Rudimenten. Die Reduktion der Gliedmassen von Chalcides tridactylus Laur. Rev. Suisse Zool. 53, 537-546) in general. In this mode of evolution two digits are lost, in the course of the adaptation of the three anterior digits to a function that does not require the two posterior digits. This evidence suggests that the evolution of digits in tetrapods can proceed at least on two distinct levels of integration, the level of digit condensations and that of adult digits.