Transient role of the middle ear as a lower jaw support across mammals

Mammals articulate their jaws using a novel joint between the dentary and squamosal bones. In eutherian mammals, this joint forms in the embryo, supporting feeding and vocalisation from birth. In contrast, marsupials and monotremes exhibit extreme altriciality and are born before the bones of the novel mammalian jaw joint form. These mammals need to rely on other mechanisms to allow them to feed. Here, we show that this vital function is carried out by the earlier developing, cartilaginous incus of the middle ear, abutting the cranial base to form a cranio-mandibular articulation. The nature of this articulation varies between monotremes and marsupials, with juvenile monotremes retaining a double articulation, similar to that of the fossil mammaliaform Morganucodon, while marsupials use a versican-rich matrix to stabilise the jaw against the cranial base. These findings provide novel insight into the evolution of mammals and the changing relationship between the jaw and ear.
eLife digest The defining feature of all mammals is how the jaw works. Fish, reptiles and other animals with backbones have a lower jaw made of many bones fused together, one of which connects to the upper jaw. The lower jaw in mammals, however, is made of a single bone that connects with the upper jaw using a completely unique jaw joint. This new joint emerged as the ancestors of all mammals split from the reptiles around 200 million years ago. The bones that formed the original jaw joint ended up in the middle ear in mammals and switched to a role in hearing. Nowadays, there are three types of mammals: the placentals, marsupials and monotremes (the egg laying mammals). In mice, humans and other placental mammals, the skeleton of the adult jaw joint forms in the embryo before birth. However, marsupials (such as kangaroos and opossums) and monotremes (platypuses and echidnas) are born at a much earlier embryonic stage, before the adult jaw joint has formed. It is therefore unclear how newborn marsupials and monotremes are able to move their jaws to feed on milk from their mother. Anthwal et al. compared how the jaw develops in mice, opossums, platypuses and echidnas before and after the adult jaw joint becomes functional. The experiments showed that young echidnas, platypuses and opossums use their middle ear bones to articulate the lower jaw with the head before the adult jaw joint forms. In young opossums, the ear bones form a cushion to support the jaw. In juvenile platypuses a double joint is evident, with the ear bones forming a joint at the same time as the newly formed adult jaw joint, similar to the situation observed in fossils of mammal ancestors. The experiments also indicated that mice and other placental mammals may potentially use their ear bones to support the jaw before birth. These findings shed light on why the ear and jaw have such a close connection in mammals. In humans, the ear and jaw bones are still connected by ligaments, explaining why trauma to the jaw joint can cause dislocation of the ear bones. Similarly, defects in the development of the jaw can impact the ear, such as in Treacher Collins Syndrome, where in some cases the jaw joint fails to form and the ear bones appear to try and take this role. Understanding how the ear and jaw evolved will help us understand why they look like they do and why a defect in one can have knock-on consequences for the other.