Living in darkness: Exploring adaptation of Proteus anguinus in 3 dimensions by X-ray imaging.

Ambystoma mexicanum Proteus anguinus X-ray microCT axolotl cave animal microtomography olm salamander subterranean adaptations

Journal

GigaScience
ISSN: 2047-217X
Titre abrégé: Gigascience
Pays: United States
ID NLM: 101596872

Informations de publication

Date de publication:
05 04 2022
Historique:
received: 27 08 2021
revised: 06 01 2022
accepted: 27 02 2022
entrez: 5 4 2022
pubmed: 6 4 2022
medline: 8 4 2022
Statut: ppublish

Résumé

Lightless caves can harbour a wide range of living organisms. Cave animals have evolved a set of morphological, physiological, and behavioural adaptations known as troglomorphisms, enabling their survival in the perpetual darkness, narrow temperature and humidity ranges, and nutrient scarcity of the subterranean environment. In this study, we focused on adaptations of skull shape and sensory systems in the blind cave salamander, Proteus anguinus, also known as olm or simply proteus-the largest cave tetrapod and the only European amphibian living exclusively in subterranean environments. This extraordinary amphibian compensates for the loss of sight by enhanced non-visual sensory systems including mechanoreceptors, electroreceptors, and chemoreceptors. We compared developmental stages of P. anguinus with Ambystoma mexicanum, also known as axolotl, to make an exemplary comparison between cave- and surface-dwelling paedomorphic salamanders. We used contrast-enhanced X-ray computed microtomography for the 3D segmentation of the soft tissues in the head of P. anguinus and A. mexicanum. Sensory organs were visualized to elucidate how the animal is adapted to living in complete darkness. X-ray microCT datasets were provided along with 3D models for larval, juvenile, and adult specimens, showing the cartilage of the chondrocranium and the position, shape, and size of the brain, eyes, and olfactory epithelium. P. anguinus still keeps some of its secrets. Our high-resolution X-ray microCT scans together with 3D models of the anatomical structures in the head may help to elucidate the nature and origin of the mechanisms behind its adaptations to the subterranean environment, which led to a series of troglomorphisms.

Sections du résumé

BACKGROUND
Lightless caves can harbour a wide range of living organisms. Cave animals have evolved a set of morphological, physiological, and behavioural adaptations known as troglomorphisms, enabling their survival in the perpetual darkness, narrow temperature and humidity ranges, and nutrient scarcity of the subterranean environment. In this study, we focused on adaptations of skull shape and sensory systems in the blind cave salamander, Proteus anguinus, also known as olm or simply proteus-the largest cave tetrapod and the only European amphibian living exclusively in subterranean environments. This extraordinary amphibian compensates for the loss of sight by enhanced non-visual sensory systems including mechanoreceptors, electroreceptors, and chemoreceptors. We compared developmental stages of P. anguinus with Ambystoma mexicanum, also known as axolotl, to make an exemplary comparison between cave- and surface-dwelling paedomorphic salamanders.
FINDINGS
We used contrast-enhanced X-ray computed microtomography for the 3D segmentation of the soft tissues in the head of P. anguinus and A. mexicanum. Sensory organs were visualized to elucidate how the animal is adapted to living in complete darkness. X-ray microCT datasets were provided along with 3D models for larval, juvenile, and adult specimens, showing the cartilage of the chondrocranium and the position, shape, and size of the brain, eyes, and olfactory epithelium.
CONCLUSIONS
P. anguinus still keeps some of its secrets. Our high-resolution X-ray microCT scans together with 3D models of the anatomical structures in the head may help to elucidate the nature and origin of the mechanisms behind its adaptations to the subterranean environment, which led to a series of troglomorphisms.

Identifiants

pubmed: 35380661
pii: 6562166
doi: 10.1093/gigascience/giac030
pmc: PMC8982192
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© The Author(s) 2022. Published by Oxford University Press GigaScience.

Références

Annu Int Conf IEEE Eng Med Biol Soc. 2016 Aug;2016:3342-3345
pubmed: 28269019
Science. 2004 Dec 3;306(5702):1783-6
pubmed: 15486254
Science. 2007 Nov 2;318(5851):772-7
pubmed: 17975060
Sci Rep. 2017 Mar 27;7:45054
pubmed: 28345609
PeerJ. 2021 Jul 28;9:e11840
pubmed: 34395082
Sci Rep. 2019 Oct 17;9(1):14896
pubmed: 31624273
Bioscience. 2021 Dec 08;72(3):254-266
pubmed: 35241972
J Exp Biol. 2001 Jan;204(Pt 2):269-81
pubmed: 11136613
Nat Methods. 2012 Jul;9(7):671-5
pubmed: 22930834
Biol Bull. 1976 Dec;151(3):450-66
pubmed: 1016662
Am J Phys Anthropol. 2012 Mar;147(3):472-81
pubmed: 22281866
Behav Processes. 1998 May;43(2):107-13
pubmed: 24895999
Evol Dev. 2008 May-Jun;10(3):265-72
pubmed: 18460088
J Hum Evol. 2009 Jan;56(1):66-75
pubmed: 18986680
J Exp Biol. 2008 May;211(Pt 10):1668-80
pubmed: 18456894
BMC Physiol. 2009 Jun 22;9:11
pubmed: 19545439
Sci Rep. 2018 Sep 20;8(1):14145
pubmed: 30237460
Gigascience. 2017 Jun 1;6(6):1-11
pubmed: 28419369
PLoS Biol. 2020 Nov 17;18(11):e3000902
pubmed: 33201874
Ann N Y Acad Sci. 2022 Jan;1507(1):5-11
pubmed: 34480358
Pflugers Arch. 2000;439(3 Suppl):R165-7
pubmed: 10653179

Auteurs

Markéta Tesařová (M)

Central European Institute of Technology, Brno University of Technology, Purkyňova 123, Brno, 61200, Czech Republic.

Lucia Mancini (L)

Elettra-Sincrotrone Trieste S.C.p.A., S.S. 14 - km 163,5 in Area Science Park, Basovizza, Trieste, 34149, Italy.

Edgardo Mauri (E)

Speleovivarium Erwin Pichl, Adriatic Speleology Society, Via Guido Reni, 2/C, Trieste, 34123, Italy.

Gregor Aljančič (G)

Institute Tular Cave Laboratory, Oldhamska 8a, Kranj, 4000, Slovenia.

Magdalena Năpăruş-Aljančič (M)

Institute Tular Cave Laboratory, Oldhamska 8a, Kranj, 4000, Slovenia.
Research Centre of the Slovenian Academy of Sciences and Arts: Karst Research Institute, Titov trg 2, Postojna, 6230, Slovenia.

Rok Kostanjšek (R)

University of Ljubljana, Biotechnical Faculty, Department of Biology, Večna pot 111, Ljubljana, 1000, Slovenia.

Lilijana Bizjak Mali (L)

University of Ljubljana, Biotechnical Faculty, Department of Biology, Večna pot 111, Ljubljana, 1000, Slovenia.

Tomáš Zikmund (T)

Central European Institute of Technology, Brno University of Technology, Purkyňova 123, Brno, 61200, Czech Republic.

Markéta Kaucká (M)

Max Planck Institute for Evolutionary Biology, August-Thienemann-Str. 2, Plon, 24306, Germany.

Federica Papi (F)

Speleovivarium Erwin Pichl, Adriatic Speleology Society, Via Guido Reni, 2/C, Trieste, 34123, Italy.

Jana Goyens (J)

Laboratory of Functional Morphology, University of Antwerp, Universiteitsplein 1, Wilrijk, 2610, Belgium.

Anass Bouchnita (A)

Department of Information Technology, Uppsala University, Box 337, Uppsala, 755 01, Sweden.
Department of Integrative Biology, University of Texas at Austin, Austin, 78712, Texas, USA.

Andreas Hellander (A)

Department of Information Technology, Uppsala University, Box 337, Uppsala, 755 01, Sweden.

Igor Adameyko (I)

Medical University of Vienna, Center for Brain Research, Department of Neuroimmunology, Spitalgasse 4, 1090 Vienna, Austria.
Karolinska Institutet, Department of Physiology and Pharmacology, Solnavagen 9, 17165 Solna, Sweden.

Jozef Kaiser (J)

Central European Institute of Technology, Brno University of Technology, Purkyňova 123, Brno, 61200, Czech Republic.

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Classifications MeSH