Dual processing of sulfated steroids in the olfactory system of an anuran amphibian

Abstract

Chemical communication is widespread in amphibians, but if compared to later diverging tetrapods the available functional data is limited. The existing information on the vomeronasal system of anurans is particularly sparse. Amphibians represent a transitional stage in the evolution of the olfactory system. Most species have anatomically separated main and vomeronasal systems, but recent studies have shown that in anurans their molecular separation is still underway. Sulfated steroids function as migratory pheromones in lamprey and have recently been identified as natural vomeronasal stimuli in rodents. Here we identified sulfated steroids as the first known class of vomeronasal stimuli in the amphibian Xenopus laevis. We show that sulfated steroids are detected and concurrently processed by the two distinct olfactory subsystems of larval Xenopus laevis, the main olfactory system and the vomeronasal system. Our data revealed a similar but partially different processing of steroid-induced responses in the two systems. Differences of detection thresholds suggest that the two information channels are not just redundant, but rather signal different information. Furthermore, we found that larval and adult animals excrete multiple sulfated compounds with physical properties consistent with sulfated steroids. Breeding tadpole and frog water including these compounds activated a large subset of sensory neurons that also responded to synthetic steroids, showing that sulfated steroids are likely to convey intraspecific information. Our findings indicate that sulfated steroids are conserved vomeronasal stimuli functioning in phylogenetically distant classes of tetrapods living in aquatic and terrestrial habitats.

Evolution of <i>V1R</i> pheromone receptor genes in vertebrates: diversity and commonality

“…Isogai et al (2011) extensively explored possible ligands for V1Rs by applying two-color in situ hybridization assays using probes against egr-1 (a marker for neuronal activation) and one specific receptor gene on VNO sections of individual mice that were exposed to variable stimuli. In this study, some V1Rs were shown to detect and discriminate distinct structural classes of sulfated steroids, which may act as sensitive reporters of the endocrine state in a broad range of vertebrates, including lamprey (Sorensen et al, 2005), goby (Murphy et al, 2001), cichlids (Cole and Stacey, 2006), tilapia (Keller-Costa et al, 2014) and amphibians (Sansone et al, 2015).…”

Quantitative comparative analysis of the nasal chemosensory organs of anurans during larval development and metamorphosis highlights the relative importance of chemosensory subsystems in the group

“…An interesting study was recently published by Sansone et al (). The authors found that sulfated steroids are detected by olfactory and vomeronasal neurons in tadpoles of X. laevis .…”

Volatile compound secretion coincides with modifications of the olfactory organ in mantellid frogs

“…The olfactory detection and neuronal processing of such multicomponent pheromones is a highly complex phenomenon, often simultaneously involving MOO and VNO. This interconnectivity of the two chemosensory systems is well studied in mammals (for review see Wyatt, ) and likely to occur in amphibians (Sansone et al ., ). Thirdly, neuronal activity of olfactory sensory cells is often dosage‐dependent.…”