Hox genes, digit identities and the theropod/bird transition

Vargas and Fallon (2005. J Exp Zool (Mol Dev Evol) 304B:86-90) propose that Hox gene expression patterns indicate that the most anterior digit in bird wings is homologous to digit 1 rather than to digit 2 in other amniotes. This interpretation is based on the presence of Hoxd13 expression in combination with the absence of Hoxd12 expression in the second digit condensation from which this digit develops (the first condensation is transiently present). This is a pattern that is similar to that in the developing digit 1 of the chicken foot and the mouse hand and foot. They have tested this new hypothesis by analysing Hoxd12 and Hoxd13 expression patterns in two polydactylous chicken mutants, Silkie and talpid2. They conclude that the data support the notion that the most anterior remaining digit of the bird wing is homologous to digit 1 in other amniotes either in a standard phylogenetic sense, or alternatively in a (limited) developmental sense in agreement with the Frameshift Hypothesis of Wagner and Gautier (1999, i.e., that the developmental pathway is homologous to the one that leads to a digit 1 identity in other amniotes, although it occurs in the second instead of the first digit condensation). We argue that the Hoxd12 and Hoxd13 expression patterns found for these and other limb mutants do not allow distinguishing between the hypothesis of Vargas and Fallon (2005. J Exp Zool (Mol Dev Evol) 304B:86-90) and the alternative one, i.e., the most anterior digit in bird wings is homologous to digit 2 in other amniotes, in a phylogenetic or developmental sense. Therefore, at the moment the data on limb mutants does not present a challenge to the hypothesis, based on other developmental data (Holmgren, 1955. Acta Zool 36:243-328; Hinchliffe, 1984. In: Hecht M, Ostrom JH, Viohl G, Wellnhofer P, editors. The beginnings of birds. Eichstätt: Freunde des Jura-Museum. p 141-147; Burke and Feduccia, 1997. Science 278:666-668; Kundrát et al., 2002. J Exp Zool (Mol Dev Evol) 294B:151-159; Larsson and Wagner, 2002. J Exp Zool (Mol Dev Evol) 294B:146-151; Feduccia and Nowicki, 2002. Naturwissenschaften 89:391-393), that the digits of bird wings are homologous to digits 2,3,4 in amniotes. We recommend further testing of the hypothesis by comparing Hoxd expression patterns in different taxa.