12
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Ultrastructural evidence of a mechanosensory function of scale organs (sensilla) in sea snakes (Hydrophiinae)

      research-article

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          The evolution of epidermal scales was a major innovation in lepidosaurs, providing a barrier to dehydration and physical stress, while functioning as a sensitive interface for detecting mechanical stimuli in the environment. In snakes, mechanoreception involves tiny scale organs (sensilla) that are concentrated on the surface of the head. The fully marine sea snakes (Hydrophiinae) are closely related to terrestrial hydrophiine snakes but have substantially more protruding (dome-shaped) scale organs that often cover a larger portion of the scale surface. Various divergent selection pressures in the marine environment could account for this morphological variation relating to detection of mechanical stimuli from direct contact with stimuli and/or indirect contact via water motion (i.e. ‘hydrodynamic reception’), or co-option for alternate sensory or non-sensory functions. We addressed these hypotheses using immunohistochemistry, and light and electron microscopy, to describe the cells and nerve connections underlying scale organs in two sea snakes, Aipysurus laevis and Hydrophis stokesii. Our results show ultrastructural features in the cephalic scale organs of both marine species that closely resemble the mechanosensitive Meissner-like corpuscles that underlie terrestrial snake scale organs. We conclude that the scale organs of marine hydrophiines have retained a mechanosensory function, but future studies are needed to examine whether they are sensitive to hydrodynamic stimuli.

          Related collections

          Most cited references61

          • Record: found
          • Abstract: found
          • Article: not found

          The gentle touch receptors of mammalian skin.

          The skin is our largest sensory organ, transmitting pain, temperature, itch, and touch information to the central nervous system. Touch sensations are conveyed by distinct combinations of mechanosensory end organs and the low-threshold mechanoreceptors (LTMRs) that innervate them. Here we explore the various structures underlying the diverse functions of cutaneous LTMR end organs. Beyond anchoring of LTMRs to the surrounding dermis and epidermis, recent evidence suggests that the non-neuronal components of end organs play an active role in signaling to LTMRs and may physically gate force-sensitive channels in these receptors. Combined with LTMR intrinsic properties, the balance of these factors comprises the response properties of mechanosensory neurons and, thus, the neural encoding of touch.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Molecular Basis of Infrared Detection by Snakes

            Snakes possess a unique sensory system for detecting infrared radiation, enabling them to generate a ‘thermal image’ of predators or prey. Infrared signals are initially received by the pit organ, a highly specialized facial structure that is innervated by nerve fibers of the somatosensory system. How this organ detects and transduces infrared signals into nerve impulses is not known. Here we use an unbiased transcriptional profiling approach to identify TRPA1 channels as infrared receptors on sensory nerve fibers that innervate the pit organ. TRPA1 orthologues from pit bearing snakes (vipers, pythons, and boas) are the most heat sensitive vertebrate ion channels thus far identified, consistent with their role as primary transducers of infrared stimuli. Thus, snakes detect infrared signals through a mechanism involving radiant heating of the pit organ, rather than photochemical transduction. These findings illustrate the broad evolutionary tuning of TRP channels as thermosensors in the vertebrate nervous system.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Molecular phylogeny and divergence dates for Australasian elapids and sea snakes (hydrophiinae): evidence from seven genes for rapid evolutionary radiations.

              One of the most prolific radiations of venomous snakes, the Australo-Melanesian Hydrophiinae includes approximately 100 species of Australasian terrestrial elapids plus all approximately 60 species of viviparous sea snakes. Here, we estimate hydrophiine relationships based on a large data set comprising 5800 bp drawn from seven genes (mitochondrial: ND4, cytb, 12S, 16S; nuclear: rag1, cmos, myh). These data were analysed using parsimony, likelihood and Bayesian methods to better resolve hydrophiine phylogeny and provide a timescale for the terrestrial and marine radiations. Among oviparous forms, Cacophis, Furina and Demansia are basal to other Australian elapids (core oxyuranines). The Melanesian Toxicocalamus and Aspidomorphus group with Demansia, indicating multiple dispersal events between New Guinea and Australia. Oxyuranus and Pseudonaja form a robust clade. The small burrowing taxa form two separate clades, one consisting of Vermicella and Neelaps calanotus, and the other including Simoselaps, Brachyurophis and Neelaps bimaculatus. The viviparous terrestrial elapids form three separate groups: Acanthophis, the Rhinoplocephalus group and the Notechis-Hemiaspis group. True sea snakes (Hydrophiini) are robustly united with the Notechis-Hemiaspis group. Many of the retrieved groupings are consistent with previous molecular and morphological analyses, but the polyphyly of the viviparous and burrowing groups, and of Neelaps, are novel results. Bayesian relaxed clock analyses indicate very recent divergences: the approximately 160 species of the core Australian radiation (including sea snakes) arose within the last 10 Myr, with most inter-generic splits dating to between 10 and 6 Ma. The Hydrophis sea snake lineage is an exceptionally rapid radiation, with > 40 species evolving within the last 5 Myr.
                Bookmark

                Author and article information

                Journal
                R Soc Open Sci
                R Soc Open Sci
                RSOS
                royopensci
                Royal Society Open Science
                The Royal Society
                2054-5703
                April 2019
                10 April 2019
                10 April 2019
                : 6
                : 4
                : 182022
                Affiliations
                [1 ]School of Biological Sciences, The University of Adelaide , Adelaide, South Australia 5005, Australia
                [2 ]Adelaide Microscopy, the Centre for Advanced Microscopy and Microanalysis , Adelaide, South Australia 5005, Australia
                [3 ]College of Life and Environmental Science, University of Exeter , Exeter EX4 4QD, UK
                Author notes
                Author for correspondence: Jenna M. Crowe-Riddell e-mail: jmcroweriddell@ 123456gmail.com

                Electronic supplementary material is available online at https://dx.doi.org/10.6084/m9.figshare.c.4447781.

                Author information
                http://orcid.org/0000-0003-2794-2914
                http://orcid.org/0000-0003-3001-983X
                http://orcid.org/0000-0002-9581-268X
                Article
                rsos182022
                10.1098/rsos.182022
                6502359
                31183131
                888c326a-3419-4209-bdd0-12b1127e8904
                © 2019 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 29 November 2018
                : 15 March 2019
                Funding
                Funded by: Australian Governmnet Research Training Program Scholarship;
                Funded by: The Hermon Slade Foundation, http://dx.doi.org/10.13039/501100001109;
                Award ID: 0001039517
                Funded by: ARC Future Fellowship;
                Award ID: FT130101965
                Categories
                1001
                133
                70
                Biology (Whole Organism)
                Research Article
                Custom metadata
                April, 2019

                sea snake,scale organs,cutaneous,mechanoreceptor,skin,sensilla
                sea snake, scale organs, cutaneous, mechanoreceptor, skin, sensilla

                Comments

                Comment on this article