Coevolution of the Mammalian Middle Ear and Neocortex Timothy Rowe Phylogenetic analysis with x-ray computed tomography of fossilized and recent crania implicates differential growth of the neocortex in the evolution and development of the mammalian middle ear. In premammalian tetrapods, the middle ear evolved as a chain of bones attached to the mandible and cranium, but in adult mammals the chain is detached from the mandible and lies behind it. The neocortex evolved concurrently with detachment of the chain. In mammalian development the auditory chain arises con- nected to the mandible but later detaches, recapitulating the phylogenetic transforma- tion. In modern didelphid development, the auditory chain reaches mature size by the third week after birth and is then separated from the jaw and displaced caudally as the neocortex grows for another 9 weeks. T h e mammalian middle ear contains a chain of tinv ossicles whose ~arallel histo- ries in ontogeny and phylogeny are among the most famous in comparative biology (1, 2). The middle ear arose in premam- malian history (1-6) as an integrated com- ponent of the mandible, where it partici- pated in a continuous arcade of bones Department of GeologicalSciences and Vertebrate Pale- ontology Laboratory, University of Texas, Austin, TX 7871 2, USA. extending from the mandibular symphysis to the fenestra vestibuli (FV) of the inner ear (Fig. 1). The craniomandibular joint (CMJ) was formed by the quadrate and articular, which served the dual functions of hearing and feeding. Over a 100-mil- lion-year span of premammalian history, the middle ear ossicles were gradually re- duced, reflecting specialization for increas- ingly high-frequency hearing (3), while the dentary correspondingly enlarged to undertake a greater role in feeding ((4). Hearing and feeding were structurally linked in premammalian history, but in mammals (5) these functions became de- coupled as the auditory chain detached from the mandible and repositioned be- hind it. The dentary remains as the only bone in the mammalian lower jaw, artic- ulating with the squamosal to form a new CMJ. Anatomical relations of the ear os- sicles to one another and auditory func- tion were little affected in this transforma- tion (3). Separation of the ossicles from the mandible is common to all adult mam- mals and was widely regarded as the de- finitive mammalian character under Lin- nean taxonomy (6). In modem didelphid (marsupial) develop- ment (7), as in mamma&generally ( 1, 2, 5), the auditory chain differentiates and begins growth attached to the mandible, forming an arcade of cartilages from the FV to the man- dibular symphysis (Fig. 2A). Three cartilages are present at birth. The stapes extends from the FV to the incus (quadrate), which is braced against the ventral edge of the otic capsule and articulates with the rear extremity of Meckel's cartilage. In the second develop- mental week, Meckel's cartilage cleaves to form the malleus (articular). The two pieces A 'lamrnalia Malleus ~uc~nbdontia ~~nddontia I Ectotyrnph,., C Fig. 1. (A) Coevolution of the mammalian mandible and middle ear (right view of auditory chain of Didelphis; the stapes is rotated and offset from lateralview) and the brain (illustrated by dorsal views of endocasts), plotted betweenthe incus and fenestra vestibuli. Abbreviations: CMJ, cranioman- on a phylogeny of selected mammals and their closest extinct relatives (5, dibular joint; FV, fenestra vestibuli of the inner ear. Crosses signify extinct 19). (B) Dorsal view of the brain of Didelphis (opossum). (C) Right lateral species. SCIENCE VOL. 273 2 AUGUST 1996