The Formation and Position of Middle Ear Ossicles During Development in Cetacea

Abstract

The order Cetacea (dolphins, whales, and porpoises) evolved from terrestrial artiodactyls (even‐toed ungulates) around 50 million years ago. This transition from land to water occurred over an evolutionarily short period of less than 10 million years and is considered one of the best examples of macroevolutionary change among vertebrates. Among the sensory systems, the ear has developed a number of unique adaptations to adapt to water borne sounds. We hypothesize that a record of these evolutionary changes is preserved in the prenatal ontogeny. In particular, previous studies on fossils have identified a rotation of the middle ear ossicles with regard to the median plane, as well as a deflection of the axis of the cochlea. It is not clear whether these two movements are related to each other. The purpose of this study is to investigate middle ear development within odontocetes (toothed whales) using two species of dolphin (Stenella attenuata and stenella longirostris). Using Amira and Avizo 3‐D software we investigate the malleus, incus, and stapes over a range of embryological stages and their relationship to inner ear structures, such as the cochlea and semicircular canals. These data are then compared to what is known for adult Stenella.Data is collected on histological sections and CTs of heads of embryologic and fetal specimens. These specimens have either been stained using phosphotungstic acid and microCT scanned (stored in 70% ethanol) or sliced at 7μm and stained using hematoxylin and eosin. We photograph histologic specimens (every other slice) in the region containing the middle and inner ear structures. Avizo and Amira software version 2019.1 are used to reconstruct the middle ear ossicles, cochlea, and semicircular canals of Stenella from micro CT scans and histological specimens. After reconstruction we use the 3‐D images to evaluate changes in the formation and position of the middle ear ossicles through development.The outline of middle ear and cochlear development in these dolphins is similar to that of land mammals. For example, the otic capsule shows the formation of the cochlea, and ossicle formation passes through mesenchymal and cartilaginous stages. The malleus is attached to Meckel’s cartilage and the stapes is associated with the otic capsule. Additionally, there are general similarities in ossicular shape in the later fetal stages, however in earlier embryonic stages the manubrium of the malleus and the crura of the incus are not as apparent as they are in land mammals, possibly foreshadowing the specific adaptations of cetaceans. Changes within the position of the ossicles in relation to one another as well as the cochlea and semicircular canals occur in order for the middle ear to develop into its adult state. In adult odontocetes, the malleus is fused to the tympanic plate through its anterior process, the process gracilius, creating a folded tympanic membrane. These findings support our hypothesis that many of the middle ear adaptations for odontocetes can be visualized in utero. Preliminary evidence suggests that changes in ossicular position replicate cetacean evolution. This research continues to shed light on how and when these unique changes occur to allow cetacean specialization to underwater hearing.