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, 281 (1788), 20140765

The Developmental Origin of Zygodactyl Feet and Its Possible Loss in the Evolution of Passeriformes

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The Developmental Origin of Zygodactyl Feet and Its Possible Loss in the Evolution of Passeriformes

João Francisco Botelho et al. Proc Biol Sci.

Abstract

The zygodactyl orientation of toes (digits II and III pointing forwards, digits I and IV pointing backwards) evolved independently in different extant bird taxa. To understand the origin of this trait in modern birds, we investigated the development of the zygodactyl foot of the budgerigar (Psittaciformes). We compared its muscular development with that of the anisodactyl quail (Galliformes) and show that while the musculus abductor digiti IV (ABDIV) becomes strongly developed at HH36 in both species, the musculus extensor brevis digiti IV (EBDIV) degenerates and almost disappears only in the budgerigar. The asymmetric action of those muscles early in the development of the budgerigar foot causes retroversion of digit IV (dIV). Paralysed budgerigar embryos do not revert dIV and are anisodactyl. Both molecular phylogenetic analysis and palaeontological information suggest that the ancestor of passerines could have been zygodactyl. We followed the development of the zebra finch (Passeriformes) foot muscles and found that in this species, both the primordia of the ABDIV and of the EBDIV fail to develop. These data suggest that loss of asymmetric forces of muscular activity exerted on dIV, caused by the absence of the ABDIV, could have resulted in secondary anisodactyly in Passeriformes.

Keywords: Passeriformes; Psittaciformes; anisodactyly; myogenesis; zygodactily.

Figures

Figure 1.
Figure 1.
(a) The anatomy of budgerigar early foot development. (b) The anatomy of budgerigar early hindlimb skeletal development. Cartilages stained with Alcian Blue, bones stained with Alizarin Red. (c) The trochlea accessoria (TrA) at different stages. MtIV has been isolated and photographed in lateral view. (d) Diagram picturing the change of dIV orientation during development. Scale bars: (a,b) 1 mm; (c) 200 μm. (Online version in colour.)
Figure 2.
Figure 2.
Immunohistochemical reaction against myosin 2 showing the early development of dorsal and ventral foot muscles in (a) quails and (b) budgerigars. Black arrows indicate the EBDIV. (Online version in colour.)
Figure 3.
Figure 3.
(a) Immunohistochemical reaction against myosin 2 showing the late disposition of the ABDIV (black arrows) in relation to changes in the orientation of dIV in budgerigars. (b) Immunohistochemical reaction against tenascin showing the insertion of the tendon of the ABDIV (white arrows) during budgerigar development. (c) Morphology of dIV in paralysed embryos; (c′) detail of the trochlea accessoria. (d) Diagram illustrating the development of the musculoskeletal system in the budgerigar. FDL, flexor digitorum longus; EDL, extensor digitorum longus; FPDIV, flexor perforatus digiti IV. (Online version in colour. In (d), muscles are shown in red, skeleton in blue.)
Figure 4.
Figure 4.
Immunohistochemical reaction against myosin 2 showing the early development of dorsal and ventral foot muscles in zebra finch. Most muscles disappear at HH37. Arrows, EBDIV; arrow heads, ABDIV. (Online version in colour.)
Figure 5.
Figure 5.
Phylogeny of Telluraves plus Cuculidae and Musophagidae, depicting the position of Zygodactylidae and the loss of the intrinsic muscles of dIV. Clades depicted were congruently obtained by the earlier studies [–37]. The position of Zygodactylidae and stem Psittaciformes follow [–40]. (Online version in colour.)
Figure 6.
Figure 6.
The topology of dIV tendons. (a) Anisodactyl, (b) zygodactyl with EBDIV and (c) zygodactyl lacking the EBDIV. In (b), the EBDIV does not pass through the canalis interosseus distalis. In (c), the tendon is absent. Modified from [11]. (Online version in colour.)
Figure 7.
Figure 7.
The distribution of dIV intrinsic muscles in (a) the primary anisodactyl quail, (b) the zygodactyl budgerigar and (c) the putative secondary anisodactyl zebra finch. Budgerigar lost the EBDIV but conserves the ABDIV. Both muscles are absent in the zebra finch. (Online version in colour. Muscles are shown in red, skeleton in blue.)

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