Homology and Potential Cellular and Molecular Mechanisms for the Development of Unique Feather Morphologies in Early Birds

Abstract

At least two lineages of Mesozoic birds are known to have possessed a distinct feather morphotype for which there is no neornithine (modern) equivalent. The early stepwise evolution of apparently modern feathers occurred within Maniraptora, basal to the avian transition, with asymmetrical pennaceous feathers suited for flight present in the most basal recognized avian, Archaeopteryx lithographica. The number of extinct primitive feather morphotypes recognized among non-avian dinosaurs continues to increase with new discoveries; some of these resemble feathers present in basal birds. As a result, feathers between phylogenetically widely separated taxa have been described as homologous. Here we examine the extinct feather morphotypes recognized within Aves and compare these structures with those found in non-avian dinosaurs. We conclude that the "rachis dominated" tail feathers of Confuciusornis sanctus and some enantiornithines are not equivalent to the "proximally ribbon-like" pennaceous feathers of the juvenile oviraptorosaur Similicaudipteryx yixianensis. Close morphological analysis of these unusual rectrices in basal birds supports the interpretation that they are modified pennaceous feathers. Because this feather morphotype is not seen in living birds, we build on current understanding of modern feather molecular morphogenesis to suggest a hypothetical molecular developmental model for the formation of the rachis dominated feathers of extinct basal birds.

Keywords: Confuciusornis; Mesozoic birds; Similicaudipteryx; dinosaur integument; feathers; molecular development; rectrix.

Figure 1

A simplified tree of archosaurian relationships [–31] showing the known distribution of “proto-feathers” and feathers within Archosauria. Feathers (as opposed to filaments) are defined by the presence of a rachis.

Figure 2

Proximally ribbon-like pennaceous feathers (PRPFs) in the juvenile specimen of Similicaudipteryx yixianensis STM4-1: (A) close up photograph; (B) interpretive drawing.

Figure 3

(A) Holotype of Epidexipteryx hui IVPP V15471; (B) close up of the tail feathers.

Figure 4

Detail photographs of elongate tail feathers in Confuciusornis sanctus:(A) holotype of C. feducciai DNHM D2454 (this specimen is considered a junior synonym of C. sanctus [45,51]); (B) close up of rectrices in DNHM D2454; (C) close up of rectrix in DNHM D2859.

Figure 5

(A) Photograph of the holotype of Protopteryx fengningensis IVPP V11665 with elongate tail feathers; (B) photograph of the holotype of Eoenantiornis buhleri IVPP 11537 with no elongate tail feathers; (C) close up of two isolated contour feathers in IVPP V11665.

Figure 6

Elongate tail feathers in enantiornithine Dapingfangornis sentisorhinus LPM 000039: (A) full feathers; (B) distal left rectrix; (C) interpretative drawing showing transition from unbranched to branched vanes.

Figure 7

Enantiornithes indet. GSGM-07-CM-001: (A) full slab; (B) detail photograph of paired elongate tail feathers.

Figure 8

Illustration depicting important stages in the formation of the modern pennaceous feather: (A) opening up of the epithelial cylinder via localized apoptosis produces branches; (B) anterior-posterior axis forms through a Wnt3a gradient—combination of (A) and (B) converts a three-dimensional appendage into a two-dimensional, planar structure;(C) regulating rachis/barb ratio through BMP activity; (D) modulation of stem cells to form different morphology along the distal-proximal-distal axis, which is made temporally from the distal to the proximal end.

Figure 9

Illustration of the formation of the rachis-dominated modified pennaceous feather of basal birds. (A,B) formation and initial growth of the feather bud; (C) barb ridge formation; (D) barbs fuse to form a rachis; (E) as feather continues to form, apoptosis ceases, vane becomes undifferentiated; (F,G) illustrate the conversion of a three-dimensional structure into the two-dimensional feather.