High rates of evolution preceded the origin of birds

Abstract

The origin of birds (Aves) is one of the great evolutionary transitions. Fossils show that many unique morphological features of modern birds, such as feathers, reduction in body size, and the semilunate carpal, long preceded the origin of clade Aves, but some may be unique to Aves, such as relative elongation of the forelimb. We study the evolution of body size and forelimb length across the phylogeny of coelurosaurian theropods and Mesozoic Aves. Using recently developed phylogenetic comparative methods, we find an increase in rates of body size and body size dependent forelimb evolution leading to small body size relative to forelimb length in Paraves, the wider clade comprising Aves and Deinonychosauria. The high evolutionary rates arose primarily from a reduction in body size, as there were no increased rates of forelimb evolution. In line with a recent study, we find evidence that Aves appear to have a unique relationship between body size and forelimb dimensions. Traits associated with Aves evolved before their origin, at high rates, and support the notion that numerous lineages of paravians were experimenting with different modes of flight through the Late Jurassic and Early Cretaceous.

Keywords: Aves; birds; dinosaurs; evolution; flight; morphology.

Figure 1

Rates of femur and forelimb evolution in Theropoda. Branch lengths are scaled, (i) red branch leading to the Paraves indicating an ∼200-fold rate increase relative to the background rate and (ii) yellow branches to Microraptorinae indicating an approximately eightfold rate increase relative to the background rate (not scaled relative to evolutionary rate). The original time-calibrated phylogeny is shown in dark gray. Circular rings indicate 5 Ma time intervals from the KPg boundary. Silhouettes drawn by Scott Hartman, Matt Martyniuk, Emily Willoughby, Jaime Headon, and Craig Dylke or modified by T. Michael Keesey were downloaded from http://phylopic.org.

Figure 2

The relationship between body size and forelimb length. When the phylogeny is split into three regimes (A and B), Aves (gray), Paraves (black), and other theropods (red), differences are seen between the main phylogeny in the slope for Aves and the phylogeny of Godefroit et al. (2013) in which a shallower slope for Aves is seen. These differences appear to be due to species being moved from the Aves and Paraves; Godefroit et al. (2013) place Xiaotingia and Anchiornis in Paraves, whereas in the main phylogeny they are placed in Aves. When the phylogenies are split into two portions, Aves and non-Aves, (C and D) differences are once again seen between the trees. The main phylogeny, following conclusions from Dececchi and Larrson (2013), shows a smaller Aves intercept, indicative of an allometric change in scaling between body size and forelimb length (see Table 1). Again, differences are seen in the alternative phylogeny of Godefroit (D) where this lower Aves intercept is not found. Models that split the phylogenies into three portions (A and B) are better-fitting models (according to AICc scores) and explain more of the variance in the data (according to higher R-squared values) than models that split the phylogenies into Aves and non-Aves (C and D).