Bayesian tip dating reveals heterogeneous morphological clocks in Mesozoic birds

Abstract

Recently, comprehensive morphological datasets including nearly all the well-recognized Mesozoic birds became available, making it feasible for statistically rigorous methods to unveil finer evolutionary patterns during early avian evolution. Here, we exploited the advantage of Bayesian tip dating under relaxed morphological clocks to estimate both the divergence times and evolutionary rates while accounting for their uncertainties. We further subdivided the characters into six body regions (i.e. skull, axial skeleton, pectoral girdle and sternum, forelimb, pelvic girdle and hindlimb) to assess evolutionary rate heterogeneity both along the lineages and across partitions. We observed extremely high rates of morphological character changes during early avian evolution, and the clock rates are quite heterogeneous among the six regions. The branch subtending Pygostylia shows an extremely high rate in the axial skeleton, while the branches subtending Ornithothoraces and Enantiornithes show notably high rates in the pectoral girdle and sternum and moderately high rates in the forelimb. The extensive modifications in these body regions largely correspond to refinement of the flight capability. This study reveals the power and flexibility of Bayesian tip dating implemented in MrBayes to investigate evolutionary dynamics in deep time.

Keywords: Mesozoic birds; MrBayes; relaxed clock; tip dating.

Figure 1.

Dated phylogeny (time tree) of Mesozoic birds. The topology (majority-rule consensus tree) shown is inferred allowing fossil ancestors (r = 0) without partitioning the morphological characters. The node ages in the tree are the posterior medians and the shade of each circle represents the posterior probability of the corresponding clade. The colour of the branch represents the mean relative clock rate at that branch. The error bars on the top (in blue) at the internal nodes denote the 95% HPD intervals of age estimates. In comparison, the error bars below (if present, in cyan) denote the 95% HPD intervals when disallowing fossil ancestors (r = 1) under a single partition. Additionally, the error bars shown at the early avian diversifications (in green) are the 95% HPD intervals of age estimates when the characters are partitioned into six anatomical regions and disallowing fossil ancestors (r = 1). The two extant species (Anas and Gallus) were included in the analyses but not shown in the representation (as a sister clade of Vegavis).

Figure 2.

Posterior estimates of the relative clock rates along the branches subtending the major transitions of early avian evolution for six anatomical regions of the bird body. The dot and error bar denote the mean and 95% HPD interval for each estimate, respectively. The horizontal dashed line indicates the mean relative rate of 1.0 in the relaxed model.

Figure 3.

Boxplots summarizing the mean relative clock rates across branches in the Enantiornithes clade (left) and Ornithuromorpha clade (right), respectively, for the six anatomical regions. The box denotes the first, second (median) and third quartiles while the dots are the outliers. The horizontal dashed line indicates the mean relative rate of 1.0 in the relaxed clock model.