Evolutionary assembly and disassembly of the mammalian sternum

Evolutionary transitions are frequently associated with novel anatomical structures,1 but the origins of the structures themselves are often poorly known. We use developmental, genetic, and paleontological data to demonstrate that the therian sternum was assembled from pre-existing elements. Imaging of the perinatal mouse reveals two paired sternal elements, both composed primarily of cells with lateral plate mesoderm origin. Location, articulations, and development identify them as homologs of the interclavicle and the sternal bands of synapsid outgroups. The interclavicle, not previously recognized in therians,2 articulates with the clavicle and differs from the sternal bands in both embryonic HOX expression and pattern of skeletal maturation. The sternal bands articulate with the ribs in two styles, most clearly differentiated by their association with sternebrae. Evolutionary trait mapping indicates that the interclavicle and sternal bands were independent elements throughout most of synapsid history. The differentiation of rib articulation styles and the subdivision of the sternal bands into sternebrae were key innovations likely associated with transitions in locomotor and respiratory mechanics.3,4 Fusion of the interclavicle and the anterior sternal bands to form a presternum anterior to the first sternebra was a historically recent innovation unique to therians. Subsequent disassembly of the radically reduced sternum of mysticete cetaceans was element specific, reflecting the constraints that conserved developmental programs exert on composite structures. [Display omitted] •The therian sternum is a composite that includes the ancestral interclavicle•Each element has an independent developmental program and evolutionary history•The stepwise addition and loss of elements can be traced in the fossil record•Retained ancestral elements highlight the conservatism of tissue interactions Brent et al. demonstrate that the therian sternum is composed of multiple elements, each with a unique developmental program and evolutionary history. The presence of the ancestral interclavicle in the sternum of living taxa highlights the conservatism of tissue-tissue interactions in vertebrate morphogenesis.