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.

Distal spinal nerve development and divergence of avian groups

“…During proper development, somites form as discrete units. However, segregation anomalies, where somites fail to establish proper borders, can ultimately lead to fully or partially fused vertebrae 8,21,22 , and thus could affect the number of pygostyle specific elements. To test whether somite segregation failure occurs in the pygostyle region, we examined distal somite morphology in the chick embryo.…”

“…Mutational analyses have demonstrated that proper development of certain structures is critical to formation of a full length and/or unfused tail 8 . These structures include (but are not limited to) somites, intervertebral discs, intersomitic blood vessels, notochord, neural tube, cartilage, and neural crest; their breadth underscores the wide variety of genetic modifications that can result in a truncated tail and/or fused caudal vertebrae.…”

Evolutionary changes in pubic orientation in dinosaurs are more strongly correlated with the ventilation system than with herbivory

“…), and tails are shown in left lateral view with the distal end towards the top (modified from Rashid et al . ). The arrows indicate the appearance of the features along the phylogenetic lineage leading to birds.…”

Ontogeny of the anuran urostyle and the developmental context of evolutionary novelty

“…It has been hypothesized that having polyurals (more than two ural elements) is more primitive compared to the diural condition (60); all individuals go through some fusion of the urals after they are formed as individual centra, and fish ural fusion progresses as a slow process (60,63). Avian tails have also undergone considerable changes, from the plesiomorphic long tails of nonavian dinosaurs to the short tails with a fused pygostyle of birds (the group Pygostylia; this includes modern birds) as an adaptation for flight (64)(65)(66). During the embryonic period, pygostyle vertebrae chondrify, mineralize, and then fuse once the bird hatches (66).…”