From dinosaurs to birds: a tail of evolution

Abstract

A particularly critical event in avian evolution was the transition from long- to short-tailed birds. Primitive bird tails underwent significant alteration, most notably reduction of the number of caudal vertebrae and fusion of the distal caudal vertebrae into an ossified pygostyle. These changes, among others, occurred over a very short evolutionary interval, which brings into focus the underlying mechanisms behind those changes. Despite the wealth of studies delving into avian evolution, virtually nothing is understood about the genetic and developmental events responsible for the emergence of short, fused tails. In this review, we summarize the current understanding of the signaling pathways and morphological events that contribute to tail extension and termination and examine how mutations affecting the genes that control these pathways might influence the evolution of the avian tail. To generate a list of candidate genes that may have been modulated in the transition to short-tailed birds, we analyzed a comprehensive set of mouse mutants. Interestingly, a prevalent pleiotropic effect of mutations that cause fused caudal vertebral bodies (as in the pygostyles of birds) is tail truncation. We identified 23 mutations in this class, and these were primarily restricted to genes involved in axial extension. At least half of the mutations that cause short, fused tails lie in the Notch/Wnt pathway of somite boundary formation or differentiation, leading to changes in somite number or size. Several of the mutations also cause additional bone fusions in the trunk skeleton, reminiscent of those observed in primitive and modern birds. All of our findings were correlated to the fossil record. An open question is whether the relatively sudden appearance of short-tailed birds in the fossil record could be accounted for, at least in part, by the pleiotropic effects generated by a relatively small number of mutational events.

Keywords: Archaeopteryx; Avian; Bird evolution; Confuciusornis; Dinosaur; Jeholornis; Sapeornis; Somitogenesis; Tail.

Figure 1

Evolutionary tree of Paraves showing important evolutionary changes. Although several other groups of dinosaurs evolved a pygostyle (fused posterior tail vertebrae) independently, note that the first birds had long tails and that the fossil record documents a short temporal duration of both long- and short-tailed birds followed thereafter exclusively by birds with truncated, distally fused tails.

Figure 2

Comparison of tail skeletons between Archaeopteryx, Sapeornis, Confuciusornis, and chicken (Gallus gallus). The Archaeopteryx tail was modeled after Gatesy and Dial (1996), as well as the Bavarian, Solnhofen, #11, and Thermopolis specimens. For Sapeornis, the tail was reconstructed from specimens IVPP V13276, STM 15-15, and DNHM-D3078. The Confuciusornis tail was modeled after Chiappe (2007) and specimens GMV-2131, GMV-2132, and GMV-2133. Pygostyles are indicated by arrows. Scale bars equal 2 cm.

Figure 3

Evolutionary correlation between the pygostyle, tail length, and possible display behavior. This mirror tree, constructed in Mesquite [49], shows the correspondence between tail adaptations in theropod dinosaurs, with presence (black) or absence (white) of a pygostyle mapped onto the left tree, and presence (black) or absence (white) of evidence that the tail may have been used in display on the right tree. Note that the tails of species in bold have shortened tails relative to basal theropods.

Figure 4

Structures in the embryonic vertebrate tail. (A) Three-dimensional (3-D) reconstruction of an extending vertebrate embryo tail. Axial structures include the NT and Nc; lateral to these are the paraxial somites and PSM. Somites are the embryonic precursors to skeletal muscle, ribs, and bony vertebrae; motor and interneurons are derived from the NT; the CNH is the remnant of Hensen's node and contains pluripotent cells; the PSM is the source of cells from which somites arise; and mesenchyme cells (M) at the distal tip of the tail feed into the CNH. Not shown: neural crest and ventral structures. Axis indicates Anterior, A; Posterior, P; Dorsal, D; and Ventral, V. (B) Lateral schematic of tail structures. The axial NT and Nc and paraxial somites and PSM lie dorsal to the TG, which in turn is dorsal to the VER. The VER is the remnant of the Hensen's node and a source of growth-promoting signals. Not shown: neural crest and PSM. (C) Chick embryo tail stage HH23 stained for somites with FITC-phalloidin. Abbreviations: CNH, chordoneural hinge; M, mesenchyme, Nc, notochord; NT, neural tube; PSM, presomitic mesoderm; S, somite; TG, tailgut; VER, ventral ectodermal ridge.

Figure 5

Tail extension and axial termination signaling schematic. During tail extension (depicted on left), somitogenesis is actively proceeding, with new somites forming from PSM at the determination front. Activities from Cdx proteins, Wnts, and Fgfs establish a posterior Wnt3a/Fgf8 gradient, which opposes an anterior RA gradient. These opposing gradients allow the creation of the determination front, and activation of the Notch pathway. Cycling expression patterns of Wnt, Fgf, and Notch pathway genes follow a clock wave-front model, promoting somite induction, segmentation and differentiation in successive waves, to add somites sequentially, rostral to caudal, down the vertebrate axis. During tail termination (right), the RA gradient is unopposed, due to progressively decreasing concentrations of Wnts and Fgfs. Contributions from RA (increased in chick via RALDH2), Hox genes, decreased concentrations of Cyp26a1 (mouse), Wnts and Fgfs, inhibition of the Notch pathway, apoptosis, and loss of cell division and cell recruitment in the CNH act to terminate the tail. Abbreviations: CNH, chordoneural hinge; RA, retinoic acid.

Figure 6

Experimental manipulations affecting the length of the vertebrate tail. (A) Increasing RA exposure in mouse embryos leads to progressive loss of caudal and sacral vertebrae. s1 indicates first sacral vertebrae and c1 indicates first caudal vertebrae. Data adapted from Shum et al. 1999 [93]. (B)Hoxb13 knockout (Hoxb13KO) in the mouse increases caudal vertebrae number by 2 and causes more barrel-shaped as opposed to hourglass-shaped vertebrae. Bars indicate experimental marking of equivalent numbered vertebrae; arrowheads indicate caudal vertebra #30 in both wildtype (WT) and Hoxb13KO; asterisks indicate two additional caudal vertebrae. Data adapted from Economides et al. 2003 [90]. (C) Precocious ectopic overexpression of Hoxb13 in the mouse causes prematurely truncated tails. Data adapted from Young et al. 2009 [81]. RA, retinoic acid.

Figure 7

Embryonic events during the termination of the chick embryo tail. Embryonic day, E12 to E17 chondrified skeletons (blue) of chick embryos, with ossified cells (red) detectable from E14 to E17. Compare the E17 chondrified skeleton and the adult skeleton showing the fused synsacrum and bony plate in the latter; the 5 free caudal vertebrae and the pygostyle already patterned during somitogenesis.

Figure 8

The Araucana rumpless chicken mutant. Adult skeletons showing the pelvis, synsacrum and caudal vertebrae. (A) In the homozygous mutant no caudal vertebrae develop (circle). The synsacrum develops normally and the bony plate over the fused vertebrae forms as expected. There is a hole in the final vertebra leaving the neural tube exposed. (B) In the heterozygote, 2 to 4 fused elements form beyond the synsacrum, in place of the free caudal vertebrae.