1,2,3 = 2,3,4: a solution to the problem of the homology of the digits in the avian hand

Abstract

Persistent contradictions in well supported empirical findings usually point to important scientific problems and may even lead to exciting new insights. One of the most enduring problems in evolutionary biology is the apparent conflict between paleontological and embryological evidence regarding the homology of the digits in the avian hand (1, 2). We propose that this problem highlights an important feature of morphological change: namely, the possible dissociation between the developmental origin of a particular repeated element and its subsequent individualization into a fully functional character. We argue that, although comparative embryological evidence correctly identifies the homology of the primordial condensations in avians as CII, CIII, and CIV, subsequent anatomical differentiation reflects a frame shift in the developmental identities of the avian digit anlagen in later ontogeny such that CII becomes DI, CIII becomes DII, and CIV becomes DIII.

Figure 1

Consensus cladogram depicting phylogenetic relationships among select bird-line archosaurs based on refs. and –, showing stem along which proposed frame shift is hypothesized to have occurred. Archosauria, node-based name for the crown clade stemming from the last common ancestor Aves shared with Crocodylia; Ornithosuchia, stem-based name for Aves plus all other archosaurs more closely related to Aves than to Crocodylia; Dinosauria, node-based name for the clade stemming from the last common ancestor shared by Aves and Ornithischia; Theropoda, stem-based name for the clade including Aves and all dinosaurs more closely related to Aves than to Sauropoda; Maniraptora, stem-based name for the clade including Aves and all theropods more closely related to Aves than to Ornithomimidae; Avialae, node-based name for the clade stemming from the last common ancestor shared by Archaeopteryx and Aves; Aves, node-based name for the crown clade stemming from the last common ancestor shared by Palaeognathae and Neognathae.

Figure 2

Dorsal view of left hand of maniraptor theropods. (a) Deinonychus antirrhopus. Shown is a composite of YPM 5206 (manus) and YPM 5208 (semilunate carpal). (b) Archaeopteryx lithographica (Berlin specimen). (c) Nothura maculosa (YPM-OST 2086; DI is missing the ungual phalanx). DI—III, digits; C1–3, distal carpals comprising semilunate carpal; r, radiale.

Figure 3

Ventral view of metacarpals and select wrist bones in palm of theropod hand. (a) Herrerasaurus ischigualastensis (after ref. 58); left metacarpals (reversed). (b) Coelophysis bauri (MCZ 4331); right metacarpals and compound distal carpal. (c) Allosaurus fragilis (YPM 4944); left metacarpals (reversed). (d) Deinonychus antirrhopus (YPM 5206); left metacarpals and YPM 5208, left semilunate carpal (reversed). (e) Archaeopteryx lithographica (Eichstätt specimen); left metacarpals and wrist bones. (f) Nothura maculosa (YPM-OST 2086); left carpometacarpus (reversed). I–V, metacarpals; C1–3, distal carpals; r, radiale; TC, trochlea carpalis.

Figure 4

Semidiagrammatic representations of developmental sequences from forelimbs of Alligator after ref. (a) and Ostrich after ref. (b) showing patterns of connectivity among condrogenic condensations. CI–CV, condensations; ∗, metapterygial axis.

Figure 5

Dorsal view of left hands of late embryos of Hoatzin (Opisthocomus: Neognathae) after ref. (a) and Kiwis (Apteryx: Palaeognathae) after ref. (b and c). DI–III, digits; CII–IV, condensations; MCI–III, metacarpals.

Figure 6

Hypothesis about the phylogenetic transformation of digit development leading from an ancestral five-digit theropod hand (e.g., Herrerasaurus) to the three-digit hand of Allosaurus and the maniraptorans including living birds. (A) Herrerasaurus has five digits (DI–DV), but only three are functional (DI–DIII, bold) and the remaining are vestigial (DIV and DV, outlined) (see also Fig. 3a). We assume that Herrerasaurus followed the usual amniote pattern in which condensation CI develops into digit DI, etc. (B) The next stage of evolution is the loss of digit DV, as exemplified by Coelophysis (see Figs. 1 and 3b). Coelophysis has three functional digits, DI–DIII, and one vestigial digit, DIV. We assume that this step is because of a secondary loss of digit DV in which condensation CV forms but fails to differentiate into a digit. Condensation CV still forms during hand development of living birds (1) but fails to fully chondrify and is eventually absorbed. Occasionally, a remnant of DV is found in a few individuals of Coelophysis (59), demonstrating that CV is retained from early theropods into living birds. (C) The transition from a four- to a three-digit hand, represented by Allosaurus, eventually leads to the loss of condensation CI, as shown in the development of living birds. During this transition, we hypothesize a frame shift that forces CII in to the developmental trajectory of digit DI, CIII into DII, and CIV into DIII. This hypothesis reconciles the findings of comparative anatomy, which show that the remaining three digits of birds are digits DI, DII, and DIII and the embryological data that demonstrate that these digits develop from condensations CII, CIII, and CIV.