Editorial: Comparative approach emphasises the biodiversity of vertebrate sensory systems

Shaun P Collin^1*Wayne Iwan Lee Davies^1,2*

• ¹La Trobe University School of Agriculture Biomedicine and Environment, Melbourne, Australia
• ²Umea universitet Institutionen for Molekylarbiologi, Umeå, Sweden

The aim of this Research Topic was to provide a current update on the breadth and depth of comparative sensory research to improve our understanding of the diversity of sensory systems in chordates and to complement an earlier collection of articles focussed on aquatic vertebrates (https://www.frontiersin.org/researchtopics/3996/biodiversity-of-sensory-systems-in-aquatic-vertebrates).The three articles that were accepted under this topic provided excellent examples of how light and sound are sampled by the eyes (phototransduction) and inner ear (mechanotransduction), respectively, and how the receptor arrays in each sensory modality are organised to optimise sensitivity within visual and auditory (three dimensional) space.In Wagner et al (https://www.frontiersin.org/journals/ecology-andevolution/articles/10.3389/fevo.2022.1044565/full ), the tubular eyes of deep-sea opisthoproctid spookfishes are revealed to contain image-forming, retinal diverticula, often combining both reflective and refractive optics, which appear to be more anatomically and optically complex than all other vertebrate eyes discovered to date. Together with eye and body movements, these ocular adaptations direct ventrolateral illumination into the dorsally-directed tubular eyes to extend each species' visual field, presumably to detect the approach of predators in the photon-limited mesopelagic zone of the open ocean. In this detailed investigation of six species of "barrel-eyed" spookfishes, the authors also present a credible case regarding the evolution of such complex eyes in which tubular eyes with image-forming diverticula could have evolved from conventional, laterally-positioned eyes via a series of intermediate steps (Nilsson and Pelger, 1994). This article exemplifies the intense selection pressures on the visual systems in animals that inhabit extreme environments in order to maximise sensitivity to both dim, downwelling sunlight and the bioluminescent emissions that frequent the mesopelagic zone (Locket, 1977).Along similar lines, Clark and Taylor (https://www.frontiersin.org/journals/ecology-andevolution/articles/10.3389/fevo.2023.1190549/full ) use multiple hidden Markov models (HMMs) to uncover the rich diversity of visual pigments (or opsins) from the UniProt Reference Proteomes database that is constructed from genome sequences and represents nearly 1,400 eukaryote species and 24 million sequences. The authors concentrated their eMorts on opsins or G-protein coupled receptors that have roles in phototropism, entrainment of circadian rhythms and vision. Their model retrieved over 2,000 opsins from 262 species, thereby establishing a consensus classification system and allowing for broader taxonomic comparisons. In recent years, there has been a large number of opsin types discovered, i.e. melanopsin, intrinsically photosensitive retinal ganglion cell opsins, pinopsin, neuropsin, teleost multi-tissue opsins, peropsins and gluopsins in addition to the more classical retinal photoreceptor opsins. Many of these have been named for the tissue or cell in which they were first found, while others have been classified according to their phylogenetic history or function and even after the signal transduction pathway through which they operate. The HMMs is a powerful tool that describes existing amino acid sequence alignments to which all other sequences can be subsequently scored and aligned in a consistent and reproducible way. Interestingly, the actinopterygian fishes have the highest fraction of opsins among the diMerent classes of chordates (6.9% of all 7tm_1 sequences), while the arthropodan insects had the highest percentage of opsins (11.4%) within the invertebrates, reflecting their high levels of species' and habitat' diversity. The need for a new nomenclature has also recently been recognised for chordate photoreceptor types based on their evolutionary history, where a naming system to refer to orthologous cell types across a diversity of species has been lacking (Baden et al., 2025). As has been done for other retinal cell classes, the classification is informed by functional, anatomical, developmental and molecular identities of the whole neuron, including the opsin gene that each photoreceptor type expresses.The last article in this series is also an evolutionary investigation but, in contrast to the previous articles, which concentrate on the diversity and evolution of maximising visual sensitivity in a range of light environments, this study provides insight into how sound is detected and localised in a representative of the earliest jawed vertebrates, i.e. the New Zealand carpet shark Cephaloscyllium isabellum (Elasmobranchii). Sauer et al. (https://www.frontiersin.org/journals/ecology-andevolution/articles/10.3389/fevo.2022.1034891/full ) reveal that the size of the maculae and the number of hair cells increases during development in the saccular, lagenar and utricular maculae (up to a three-fold) but not in the macular neglecta. However, the orientation of the hair cells remained consistent during ontogeny with all maculae exhibiting a bi-directional orientation pattern, where the hair cells were split into two groups with opposing (180° diMerence) orientations. Increases in hair cell number is thought to enhance auditory (and vestibular) sensitivity, while the orientation (polarity) of the hair cells provides insight into how this species localises sound. Although there are only a few ontogenetic studies of the auditory and vestibular systems in this group of cartilaginous fishes, it appears that the hair cell orientation patterns vary across the Chondrichthyes (in other sharks but also in rays, skates and chimaerids), especially within the macular neglecta, a (non-otolithic) organ which serves an important role in sound detection (Corwin, 1981). This level of diversity has been borne out in a more recent study on the macula neglecta, that found it to be relatively small, with low hair cell density in the Port Jackson shark Heterodontus portusjacksoni, consistent with this species' benthic lifestyle suggesting that this species relies more on substrate-borne vibrations and spatial stability than on acute directional hearing, aligning with its ecology in wave-exposed, rocky reef habitats (Robins et al., 2025).In summary, the research topic 'Biodiversity of Sensory Systems in Chordates' is a broad and growing theme of research focus. A comparative approach will also be necessary to investigate the sensory vulnerabilities of chordates in response to future anthropogenic pressure.