Olfaction across the water–air interface in anuran amphibians

Abstract

Extant anuran amphibians originate from an evolutionary intersection eventually leading to fully terrestrial tetrapods. In many ways, they have to deal with exposure to both terrestrial and aquatic environments: (i) phylogenetically, as derivatives of the first tetrapod group that conquered the terrestrial environment in evolution; (ii) ontogenetically, with a development that includes aquatic and terrestrial stages connected via metamorphic remodeling; and (iii) individually, with common changes in habitat during the life cycle. Our knowledge about the structural organization and function of the amphibian olfactory system and its relevance still lags behind findings on mammals. It is a formidable challenge to reveal underlying general principles of circuity-related, cellular, and molecular properties that are beneficial for an optimized sense of smell in water and air. Recent findings in structural organization coupled with behavioral observations could help to understand the importance of the sense of smell in this evolutionarily important animal group. We describe the structure of the peripheral olfactory organ, the olfactory bulb, and higher olfactory centers on a tissue, cellular, and molecular levels. Differences and similarities between the olfactory systems of anurans and other vertebrates are reviewed. Special emphasis lies on adaptations that are connected to the distinct demands of olfaction in water and air environment. These particular adaptations are discussed in light of evolutionary trends, ontogenetic development, and ecological demands.

Principles of odor coding in vertebrates and artificial chemosensory systems

“…Whereas early diverging vertebrates such as fishes have a single OS (single OE and OB), in the vertebrate lineage there is a strong tendency toward segregation of the OS into different subsystems. Most amphibians and reptiles have developed a dual OS composed of a main and an accessory OS that can be distinguished by anatomy and their cellular and molecular components (31)(32)(33). Whereas the main system is made up of the main OE and the main OB, the accessory system consists of the epithelium of the vomeronasal organ (VNO) and the accessory OB (19,25,34,35).…”

Distinct interhemispheric connectivity at the level of the olfactory bulb emerges during Xenopus laevis metamorphosis

“…Tadpoles of most anuran amphibians share a similarly structured olfactory periphery, consisting of the main olfactory epithelium in the principal nasal cavity (PC), a vomeronasal organ (VNO), as well as some minor additional epithelial surfaces (Jungblut et al, 2021; Weiss et al, 2021). This is well documented for all major groups of anurans: Archaeobatrachians (Benzekri and Reiss, 2012), Mesobatrachians (Manzini and Schild, 2010) and Neobatrachians (Jermakowicz et al, 2004; Jungblut et al, 2011, 2017; Nowack and Vences, 2016; Quinzio and Reiss, 2018).…”

“…During metamorphosis, the olfactory periphery transforms into a tripartite chamber system, consisting of the main olfactory epithelium in the PC, a middle cavity (MC) lined with non-sensory epithelium in most species, and the VNO (Helling, 1938; Reiss and Eisthen, 2008). While the larval system (PC and VNO) is specialized for the detection of waterborne odors, the sensory epithelium in the adult PC is associated with sensing volatile odors (for reviews, see Reiss and Eisthen, 2008; Weiss et al, 2021).…”

“…Newly generated ORNs in the PC are projecting their axons towards the dorsal part of the main olfactory bulb (dMOB) during metamorphosis (Hofmann and Meyer, 1991; Reiss and Burd, 1997a; Gaudin and Gascuel, 2005). Since it is solely innervated by ORNs residing in the adult ‘air-nose’, the dMOB is putatively associated with the processing of volatile odorants (Föske, 1934; Reiss and Eisthen, 2008; Weiss et al, 2021).…”

Editorial for the special issue "Olfactory Coding and Circuitries"

“…Their article gives an extensive overview of the anatomy and the olfactory receptors of the peripheral olfactory subsystems of larval and adult anuran amphibians. The challenge of the anuran olfactory system to function in water and on land is addressed in the contribution of Weiss et al (2021). These authors also provide a detailed overview of the anuran olfactory structures on a tissue, cellular and molecular level and review the differences and similarities between the olfactory systems of anurans and other vertebrates.…”