Convergent metatarsal fusion in jerboas and chickens is mediated by similarities and differences in the patterns of osteoblast and osteoclast activities

Abstract

The extraordinary malleability of the vertebrate limb supports a variety of locomotor functions including running and leaping in cursorial and saltatorial species. In many of these animals, the metatarsals and/or metacarpals are disproportionately elongated to increase stride length and fused into a single larger element, likely to resist fracture due to increased ground reaction forces. Despite the fact that metapodial fusion evolved convergently in modern birds, ungulates, and jerboas, the developmental basis has only been explored in chickens, which diverged from the mammalian lineage approximately 300 million years ago. Here, we use the lesser Egyptian jerboa, Jaculus jaculus, to understand the cellular processes that unite three distinct metatarsal elements into a single cannon bone in a mammal, and we revisit the developing chicken to assess similarities and differences in the localization of osteoblast and osteoclast activities. In both species, adjacent metatarsals align along flat surfaces, osteoblasts cross the periosteal membrane to unite the three elements in a single circumference, and osteoclasts resorb bone at the interfaces leaving a single marrow cavity. However, although spatial and temporal partitioning of osteoblast and osteoclast activities reshape three bones into one in both species, the localization of osteoclasts is distinct. While osteoclasts are uniformly distributed throughout the endosteum of chicken metatarsals, these catabolic cells are highly localized to resorb bone at the interfaces of neighboring jerboa metatarsals. Each species therefore provides an opportunity to better understand the mechanisms that partition osteoblasts and osteoclasts to alter the shape of bone during development and evolution.