Rates of morphological evolution are heterogeneous in Early Cretaceous birds

Abstract

The Early Cretaceous is a critical interval in the early history of birds. Exceptional fossils indicate that important evolutionary novelties such as a pygostyle and a keeled sternum had already arisen in Early Cretaceous taxa, bridging much of the morphological gap between Archaeopteryx and crown birds. However, detailed features of basal bird evolution remain obscure because of both the small sample of fossil taxa previously considered and a lack of quantitative studies assessing rates of morphological evolution. Here we apply a recently available phylogenetic method and associated sensitivity tests to a large data matrix of morphological characters to quantify rates of morphological evolution in Early Cretaceous birds. Our results reveal that although rates were highly heterogeneous between different Early Cretaceous avian lineages, consistent patterns of significantly high or low rates were harder to pinpoint. Nevertheless, evidence for accelerated evolutionary rates is strongest at the point when Ornithuromorpha (the clade comprises all extant birds and descendants from their most recent common ancestors) split from Enantiornithes (a diverse clade that went extinct at the end-Cretaceous), consistent with the hypothesis that this key split opened up new niches and ultimately led to greater diversity for these two dominant clades of Mesozoic birds.

Keywords: Aves; Cretaceous; evolutionary rates; phylogeny; tempo.

Figure 1.

Time-scaled phylogeny of Mesozoic birds. The cladogram is the strict consensus tree obtained from the phylogenetic analysis. The thicker lines represent the dating of upper and lower boundaries of terminal taxon-bearing deposits. The zero-length branches are rescaled using the ‘mbl’ method and a minimum branch length of 1 Ma. See electronic supplementary material, figure S3, for the results using the ‘equal’ method. (Online version in colour.)

Figure 2.

Evolutionary rate analysis of Early Cretaceous birds using the ‘mbl’ scaling method and a minimum branch length of 1 Ma. (a) Result of branch likelihood test for the first most parsimonious tree where branches are not treated separately; (b) result of branch likelihood test for the same tree where terminal and internal branches are treated separately. See electronic supplementary material, figure S4, for the same analysis where the Late Cretaceous birds are included. For complete results of tests using the ‘mbl’ and ‘equal’ methods please see our Dryad data. Pie charts indicate the proportional distribution of results in 100 replicates of randomized dated trees, where red indicates branches or clades with significantly high rates, blue significantly low rates, and white non-significant (average) rates. In all cases, the null hypothesis of a single rate of evolution across the entire tree was rejected at an α of 0.01. (Online version in colour.)

Figure 3.

Evolutionary rate analysis of Early Cretaceous birds using the ‘equal’ method and a root length of 2 Ma. (a) Result of branch likelihood test for the first most parsimonious tree where branches are not treated separately; (b) result of branch likelihood test for the same tree where terminal and internal branches are treated separately. See electronic supplementary material, figure S5, for the same analysis where the Late Cretaceous birds are included. For all plots, the colour scheme repeats that of figure 2. (Online version in colour.)

Figure 4.

Morphological character changes during early avian evolution. The morphological characters have been subdivided into six anatomical regions, including the skull, axial skeleton, pectoral girdle, forelimb, pelvis, and hindlimb. The numbers of character change are retained using the likelihood re-rooting method. The morphological changes of the skull along the branch to Aves are simplified by sketch reconstructions of Linheraptor exquisitus (Theropod: Dromaeosauridae) and Archaeopteryx lithographica (Aves: Archaeopterygidae); the pectoral girdle and forelimb changes along the branch leading to Enantiornithes are simplified by comparison between Confuciusornis sanctus (Aves: Pygostylia), Sapeornis chaoyangensis (Aves: Pygostylia), and Parabohaiornis martini (Aves: Enantiornithes). Phylogenetic relationships of these taxa are depicted in figure 1. (Online version in colour.)