Clade-specific evolutionary diversification along ontogenetic major axes in avian limb skeleton

The evolutionary diversification of birds has been facilitated by specializations for various locomotor modes, with which the proportion of the limb skeleton is closely associated. However, recent studies have identified phylogenetic signals in this system, suggesting the presence of historical factors that have affected its evolutionary variability. In this study, in order to explore potential roles of ontogenetic integration in biasing the evolution in the avian limb skeleton, evolutionary diversification patterns in six avian families (Anatidae, Procellariidae, Ardeidae, Phalacrocoracidae, Laridae, and Alcidae) were examined and compared to the postnatal ontogenetic trajectories in those taxa, based on measurement of 2641 specimens and recently collected ontogenetic series, supplemented by published data. Morphometric analyses of lengths of six limb bones (humerus, ulna, carpometacarpus, femur, tibiotarsus, and tarsometatarsus) demonstrated that: 1) ontogenetic trajectories are diverse among families; 2) evolutionary diversification is significantly anisotropic; and, most importantly, 3) major axes of evolutionary diversification are correlated with clade-specific ontogenetic major axes in the shape space. These results imply that the evolutionary variability of the avian limbs has been biased along the clade-specific ontogenetic trajectories. It may explain peculiar diversification patterns characteristic to some avian groups, including the long-leggedness in Ardeidae and tendency for flightlessness in Anatidae.