10.10.2024

Enhanced hearing as key innovation at a time of mass extinction

A new study in the field of Evolitionary Biology: Common ancestor of all modern reptiles already had a tympanic ear

An international team from Brazil, the USA, and Germany shows that the last common ancestor of all living reptiles had an enhanced sense of hearing due to an eardrum similar to that of modern animals. This might have helped them to survive in a period of mass extinction.

Background
The origin of hearing with an eardrum (tympanic membrane) in land vertebrates (tetrapods) is one of the most iconic examples of an evolutionary innovation directly linked to the transition from water to land in vertebrates 400 to 360 million years ago, a landmark event that reshaped the terrestrial biotas of the Earth. In the new terrestrial environment, animals faced several challenges, including the problem of hearing, because sound waves travel differently in air and water. Although the first, amphibian-like land vertebrates were able to hear, the evolution of a tympanic ear largely improved the hearing of animals on land.

The debate on the origin of tympanic hearing began in the 19th century, and up until now, it had remained unknown whether the first reptiles of the lineage, that today comprise a diversity of more than 20,000 species of crocodiles, lizards, snakes, and turtles, already had an increased hearing capacity.

Integrative approach
The investigation was headed by Dr. Mario Bronzati from the University of Tübingen in collaboration with laboratories in São Paulo, Brazil, in Stony Brook and Downers Grove, USA, as well as at the Senckenberg Centre for Human Evolution and Palaeoenvironment at the University of Tübingen. The authors approached the question of the origin of tympanic hearing in reptiles from the perspective of modern integrative biology, combining data from paleontology and developmental biology. The study provides developmental data from lizard and crocodile embryos, going beyond previous studies that used only chick embryos as biological models for reptiles as birds descended from dinosaurs and are easy to breed. Birds, however, are highly specialized and only provide limited clues about the origin of reptiles. The authors also discovered new details from the fossil record by studying a wide range of species of the oldest members of the reptilian group.

The tympanic hearing
Tympanic hearing is defined as hearing in the presence of a tympanic membrane that vibrates when it is reached by sound waves. The information from the vibration of the eardrum is transmitted to the brain, which interprets the mechanical impulse as sound.

Tympanic hearing is common in animals. In fact, it is the way we humans hear the sounds around us. However, despite the similarities in function and components of the hearing system, previous studies have shown that tympanic hearing actually evolved independently in mammals, amphibians, and reptiles. So, although the structures of our middle ear are very similar to those of a bird, biologists have shown that they actually evolved independently in these two groups. For example, there are differences in the genes that make up the eardrum in mammals and reptiles, and paleontologists studying the fossil record recognize that there are no ear openings (otic apertures) in the last common ancestors of mammals and reptiles, which lived more than 300 million years ago. The openings evolved independently in both lineages much later.

Fossils and embryos
In the new study, supported by the São Paulo Research Foundation and Alexander von Humboldt-Stiftung, Bronzati and his colleagues investigated the origin and evolution of tympanic hearing in modern reptiles and their rich fossil record. By analyzing the fossils of some of the oldest reptiles of the world, they observed modifications in the structure of the bones in the otic (ear) region of the skull of these animals. These changes created an ear opening and an area for the attachment of the eardrum, revealing that the ancestor of all reptiles already possessed tympanic hearing, with the presence of a tympanic membrane. 

The team also studied the embryonic development of the ear by investigating embryos from the lizard Tropidurus and the crocodilian Caiman. “Molecular analyses revealed many structural similarities in the formation of the tympanic ear when animals are still inside the egg. For instance, in reptiles the tympanic membrane forms in a part of the embryo’s head that is different from the position in mammals,” the senior author of the study, Prof. Dr. Tiana Kohlsdorf from the Departament of Biology of the University of São Paulo at Ribeirão Preto, Brazil, summarizes.

Hearing as key innovation
“This is the first study that reveals in detail the origin of tympanic hearing in reptiles. Our results suggest that the ancestor of all reptiles already had a tympanic membrane, similar to that we see in reptiles today. We also show that the closest relatives of reptiles did not have a tympanic membrane,” Bronzati says. These animals all went extinct at the Permian-Triassic boundary, about 250 million years ago. At the same time, modern reptile lineages were diversifying, which suggests that the evolution of tympanic hearing – to detect their small prey and to avoid predators – was a key factor in the evolutionary success of reptiles. 

“The combination of data from two distinct areas of biology, paleontology, and developmental biology, was crucial to test our hypothesis as they provided independent information about the evolution of the tympanic hearing in reptiles,” co-author PD Dr. Ingmar Werneburg from the Senckenberg Centre in Tübingen concluded. With this approach, the authors were able to answer a long-standing question in evolutionary biology, that the tympanic ear evolved at the origin of the lineage including the living reptiles.

Dr. Mario Bronzati, Prof. Dr. Tiana Kohlsdorf, PD Dr. Ingmar Werneburg/Department of Geosciences

Publication
Mario Bronzati, Felipe M. Vieceli, Vitória Botezelli, Pedro L. Godoy, Felipe C. Montefeltro, Jann P. M. Nassif, Juliana Luzete, Douglas Ribeiro, C. Y. Irene Yan, Ingmar Werneburg, Tiana Kohlsdorf (2024). Deep time origin of tympanic hearing in crown reptiles. Current Biology, https://doi.org/10.1016/j.cub.2024.09.041 

Kontakt 
Dr. Mario Bronzati
University of Tübingen
Humboldt-fellow at the Department of Geosciences
mariobronzatispam prevention@gmail.com,  mariobronzatispam prevention@alumni.usp.br  

Prof. Dr. Tiana Kohlsdorf
University of São Paulo, Brazil
Departamento de Biologia
tianaspam prevention@usp.br

PD Dr. Ingmar Werneburg
University of Tübingen
Senckenberg Centre for Human Evolution and Palaeoenvironment
Department of Geosciences
ingmar.werneburgspam prevention@senckenberg.de