Rates of dinosaur limb evolution provide evidence for exceptional radiation in Mesozoic birds

Abstract

Birds are the most diverse living tetrapod group and are a model of large-scale adaptive radiation. Neontological studies suggest a radiation within the avian crown group, long after the origin of flight. However, deep time patterns of bird evolution remain obscure because only limited fossil data have been considered. We analyse cladogenesis and limb evolution on the entire tree of Mesozoic theropods, documenting the dinosaur-bird transition and immediate origins of powered flight. Mesozoic birds inherited constraints on forelimb evolution from non-flying ancestors, and species diversification rates did not accelerate in the earliest flying taxa. However, Early Cretaceous short-tailed birds exhibit both phenotypic release of the hindlimb and increased diversification rates, unparalleled in magnitude at any other time in the first 155 Myr of theropod evolution. Thus, a Cretaceous adaptive radiation of stem-group birds was enabled by restructuring of the terrestrial locomotor module, which represents a key innovation. Our results suggest two phases of radiation in Avialae: with the Cretaceous diversification overwritten by extinctions of stem-group birds at the Cretaceous-Palaeogene boundary, and subsequent diversification of the crown group. Our findings illustrate the importance of fossil data for understanding the macroevolutionary processes generating modern biodiversity.

Keywords: Mesozoic birds; adaptive radiation; evolutionary constraints; evolutionary rates; modularity.

Figure 1.

Triplots showing within-limb proportions of Mesozoic non-avialan (filled black circles) and avialan theropods (filled grey circles) and extant birds (open grey circles). (a) Forelimb (N_Mesozoic = 128; N_extant = 639); (b) hindlimb (N_Mesozoic = 153; N_extant = 708). Line drawings and extant bird values are from refs [12,13]. Line drawings are (left to right) Carnotaurus, Allosaurus, Archaeopteryx (forelimbs), Allosaurus, Phoenicopterus and Hesperornis (hindlimbs).

Figure 2.

Phylomorphospaces depicting (a) the Mesozoic theropod tree in fore- (N = 92) and (b) hindlimb (N = 107) shape spaces defined by PC2 and PC3 (table 1). Non-maniraptoran lineages are shown in black, non-avialan maniraptorans in dark grey (red) and Avialae in light grey (blue). Silhouettes are illustrative. (Online version in colour.)

Figure 3.

Rate of morphological evolution and cladogenesis. Posterior model-averaged rates (Brownian variance in (log10(mm))/(Myr)) of relative tibia length (hindlimb PC3) in Mesozoic theropods (N = 107) resulting from Bayesian estimation are shown by branch colours, according to the legend. Localized hindlimb PC3 rate shifts are indicated by circles at nodes and their posterior probabilities stated. Stars indicate significant tree imbalance on the complete tree (a pruned version is shown here) according to either Δ1 or Δ2 shift statistics [31], indicating diversification rate shifts among pygostylian birds. Grey stars are shifts recovered using a tree of only Early Cretaceous and younger taxa and black stars are shifts recovered from the tree including all taxa. Taxon ages are independently drawn from a uniform distribution within their substage of occurrence. (Online version in colour.)