Scents in Sync: Evolution of chemical communication in turtles

Many animals use olfactory signals to communicate with members of their own species. These chemical signals, often referred to as pheromones, are involved in several important activities of an individual such as locating mating partners and avoiding aggressive competitors. Effective transmission of the information from the sender (i.e. the individual that sends the chemical signal) to the receiver(s) is a crucial step for successful transmission of the signal. To reach the intended receiver, chemical signals should be designed to maximize transmission in a given environment. Therefore pheromone chemical composition should vary among different habitats and climatic conditions.

Terrestrial and aquatic habitats are completely different in terms of physical and chemical properties. This may have a profound effect on the chemical composition of pheromones. For instance, certain compounds may transmit better in water while others are more suitable as airborne molecules. Therefore, chemical signal composition may vary according to the habitat or environment in which they are used. Moreover, more closely related species could be more similar in terms of chemical composition due to the effect of a shared recent common ancestor.

Pond in SW Spain – Typical habitat of freshwater turtles like Mauremys leprosa Pond in SW Spain – Typical habitat of freshwater turtles like Mauremys leprosa

Pond in SW Spain – Typical habitat of freshwater turtles like Mauremys leprosa

The main aim of the project is to understand how environmental factors shape the composition of chemical signals in an ancient group of vertebrates - turtles. These vertebrates occupy highly diverse habitats such as ponds, rivers and streams as well as terrestrial environments such as deserts or temperate or humid forests. Given their wide range of environments, this group offers an excellent opportunity to examine how chemosensory systems are shaped by the environment and phylogeny. Turtles have a well-developed sense of smell, and they also secrete pheromones from several sources, including specialized glands. One of the main organs involved in chemical communication are mental glands (MGs). MGs are paired epidermal structures located on the gular region of the head. They produce secretions that may be involved in mate choice. These glands are present in some species of turtles but are absent in many others. Therefore the first part of the project aims to reconstruct the evolutionary history of mental glands across the turtle phylogeny. We have examined a large number of specimens (i.e. more than 600) from museum and live collections for the presence or absence of mental glands. Together with previous literature, our data comprise a comprehensive database on turtle mental gland occurrence. Mental gland occurrence will be mapped across the turtle phylogeny to reconstruct the evolutionary history of this trait. In some selected species the anatomy of mental glands will be studied by means of histological techniques (i.e. light and electron microscopy).

Mauremys leprosa in the field Mauremys leprosa in the field

Mauremys leprosa in the field

Detail of Mental Glands in M. leprosa Detail of Mental Glands in M. leprosa

Detail of mental glands in M. leprosa

Mental gland in Siebenrockiella crassicollis Mental gland in Siebenrockiella crassicollis

Mental gland in Siebenrockiella crassicollis

In the next phase of the study, we will select a representative subset of species for which mental glands will be sampled to characterize their composition. We plan to identify the lipids and proteins secreted in mental glands using sensitive methods such as gas chromatography/mass spectrometry, mass spectra proteomics as well as transcriptomics. Climatic, geophysical and habitat data will be gathered for the sampled species. We will test the hypothesis whether different habitats (i.e. aquatic or terrestrial), and climatic conditions (i.e. dry or humid) shape mental gland chemistry within a phylogenetic framework. This will allow us to test whether pheromones evolved in sync to environmental conditions.

Histology of the gland of M. leprosa

Histology of the gland of M. leprosa

Traditionally it was thought that humans have a very poor sense of smell, and therefore our knowledge of the chemical signals that abound in nature are something of a mystery to us. Other animals, including most other vertebrates, are much more proficient in detecting and using chemical cues in the environment. This project will shed light on the evolution of chemical communication in turtles, providing a fascinating glimpse into the chemosensory world of an extremely old group of vertebrates.

Testudo hermanni

Testudo hermanni

This project is funded through the National Science Centre of Poland, grant 2017/25/B/NZ8/01498, “Environmental factors and the evolution of chemical communication in turtles - a phylogenetic perspective” (Czynniki środowiskowe a ewolucja komunikacji chemicznej u żółwi - perspektywa filogenetyczna)

Principal investigator: Dr. Alejandro Ibáñez Ricoma (Institute of Zoology and Biomedical Research, Jagiellonian University, Kraków, Poland)

Collaborators involved in the project: Dr. hab. Maciej Pabijan (Institute of Zoology and Biomedical Research, Jagiellonian University, Kraków, Poland), Prof. Dr. Uwe Fritz (Museum of Zoology, Dresden, Germany) Dr. Albert Martinez-Silvestre (Catalonian Reptiles & Amphibians Rescue Center, Barcelona, Spain) Dr. Peter Praschag (Turtle Island, Graz, Austria), Emilia Rydzy (Jagiellonian University)

Chrysemys from turtle Island

Chrysemys from Turtle Island

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