Abstract Mammalian humerus shape is strongly predicted by loading and other functional factors. This constraint is lifted for cetaceans and, therefore, it could reflect other, specific evolutionary trends. For testing this hypothesis, the three-dimensional shape of the humerus for 32 taxa of extinct and extant cetaceans was analyzed. The shape variance was aligned with the parallel progressive evolution of diverging baleen and toothed whales. It showed a gradual advance of aquatic locomotion, with the trends of humeral head twist, diaphysis shortening and straightening, and epiphyses enlargement. Meanwhile, the phylogenetic signal was also seen in the morphospace as developments in the size and position of the humeral head and greater tubercle and diaphysis proportions. Modularity and integration patterns consistently changed through deep time and were independent of allometry. Paleogene whales had the most modular humerus, while the humerus of baleen whales was the most integrated. Also, the evolution of Hox genes regulating the humerus shape corresponded to their anatomical transformations and showed relaxed selection in cetaceans. In overall, the observed pattern well illustrated a “fly in a tube model” and showed its importance as an environment of emerging evolutionary innovations.
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