Comparative Anatomy and Evolutionary Morphology of the Larynx: An Important Key to Determine the Origin of Echolocation in Bats

Abstract

Echolocation is achieved through the production of high-frequency sounds and reception of their echoes, enabling bats to navigate in dark environments such as night time or in caves. Echolocation is widely recognized, alongside the ability of flight, as one of the crucial factors in the evolutionary success of bats. While it was previously believed that echolocation originated once in bat history (known as the single origin hypothesis), recent studies support multiple origins of this remarkable navigational ability (known as the independent origin hypothesis), by documenting distinct call types and complex phylogenetic relationships. Previous investigations have focused on studying the auditory bulla, brain, or thorax in relation to echolocation behaviours. Limited attention has been given to the larynx despite its pivotal role in generating high-frequency vocalizations. Laryngeal echolocation necessitates specific morphological adaptations to withstand the intense pressure associated with ultrasonic call production. However, the complete anatomical description of the larynx remains insufficient, and a comprehensive study exploring its involvement in echolocation is lacking. The primary research objective of this thesis is to determine whether echolocation arose from a single common ancestor of bats or if it independently emerged at multiple points along the phylogeny. By examining the morphological variations of the larynx, this project aims to advance our understanding of bat laryngeal anatomy and provide an evolutionary framework for these potential morphotypes. High-resolution visualization of the laryngeal components from diverse bat species was achieved through the application of non-destructive X-ray microtomography on iodine-stained specimens. The different bat clades exhibit significant variations in laryngeal morphology, with three primary morphotypes being evident. Non-laryngeal echolocating Pteropodidae, possess laryngeal anatomy similar to other small mammalian species. Among laryngeal echolocating bats, the remaining two morphotypes are characteristic of the Rhinolophoidea and Yangochiroptera suborders. Further analyses reveal a strong correlation between laryngeal echolocation strategies and distinct morphological specializations within the larynx. Examples of these anatomical adaptations include convergent evolution of tracheal chambers in nasal emitters and the significant shape modification of the cricoid cartilage in high-duty-cycle constant frequency specialists. Ancestral state reconstructions of the different laryngeal cartilages illustrate shared morphological traits between Pteropodidae and other non-echolocating mammals. Despite differential specializations observed among major bat suborders, the ancestor of all bats might have possessed similar laryngeal shape that extant laryngeally echolocating bats. Therefore, our research project supports a single acquisition of laryngeal echolocation early in the ancestor of the crown group of bats, then a loss of the ability to laryngeally echolocate in Pteropodidae.

Date of Award	26 Nov 2024
Original language	English
Awarding Institution	City University of Hong Kong
Supervisor	Alan G. McElligott (Supervisor) & Priscilla F. GERBER (Co-supervisor)