Skip to main content

EDITORIAL article

Front. Ecol. Evol., 04 January 2024
Sec. Behavioral and Evolutionary Ecology
This article is part of the Research Topic Adaptations to Subterranean Environments View all 14 articles

Editorial: Adaptations to subterranean environments

  • 1Department of Life, Health and Environmental Sciences (MeSVA), University of L’Aquila, L’Aquila, Italy
  • 2Department of Biological Sciences, The University of Alabama in Huntsville, Huntsville, AL, United States
  • 3Division of Molecular Biology, Institut Ruđer Bošković, Zagreb, Croatia

Editorial on the Research Topic
Adaptations to subterranean environments

The subterranean realm is a fascinating world that still holds many secrets and wonders (Culver and Pipan, 2019; Ficetola et al., 2019). Species that have successfully colonized caves and other subterranean environments have often had to deal with novel and unique conditions that promoted the appearance (or disappearance) of specific traits (Howarth and Moldovan, 2018; Soares and Niemiller, 2020). Several morphological, behavioral, and physiological traits are considered adaptive; however, an exhaustive list of adaptive traits documented in subterranean species remains to be assembled. Recent studies continue to uncover evidence for the evolution of traits in subterranean environments that were previously unrecognized (e.g. Hesselberg; Lunghi and Bilandžija), especially thanks to new methods that expand our research possibilities (Bierbach et al., 2018; Mammola et al., 2021). Historically, the morphological phenotype was used as an exclusive criterion for recognizing obligate cave species (Christiansen, 1962). Among them, the loss or reduction of eyes, depigmentation, and elongation of appendages have been recognized as defining traits for living in complete darkness (Bilandžija et al., 2012; Gonzalez et al., 2017). Selection pressures imposed by subterranean environments are often so strong that even conspecific individuals can exhibit divergent phenotypes depending on their habitats (Jeffery, 2020; Lunghi and Zhao, 2020), as two studies on fish (Enriquez et al.) and newts (Guillaume) published in this Research Topic also show. Other less conspicuous traits should also be included within the array of adaptations to cave life. For example, behavioral adjustments may be the first changes individuals need to make in a novel subterranean environment (Lunghi et al., 2023). All behaviors based on visual inputs must be replaced by new ones that rely on other sensory stimuli, such as chemical or mechanical cues (Plath et al., 2004; Yoshizawa et al., 2012). Consequently, the nervous system, for example, should undergo specific modifications of its structure and function to adapt to the new conditions. Further, many cave species have modulated their metabolism to better withstand long periods of starvation in generally food-deprived subterranean environments (Hervant, 2012; Lipovšek et al., 2019). This Research Topic on Adaptations to Subterranean Environments aimed to assemble some of the latest studies on adaptive traits in obligate and facultative cave species and to highlight new research perspectives (Culver and Pipan, 2015; Culver et al.). Thirteen papers are included in this Research Topic, including five reviews on specific topics, such as biomimetics (Hesselberg), chemoreception (Berning and Gross), and electroception (Soares et al.). Eight original research articles address various aspects of adaptation to subterranean life, including the genetic mechanisms that enable the establishment of the specific trait in the population (Arcila et al.; Bondareva et al.). Various model species were used for these studies, including less-studied species such as mammals (Luna et al.) and microorganisms (Frumkin et al.). On the other hand, more conventional model species of subterranean invertebrates were used to properly understand the phylogeography of congeneric species (Kováč et al.) and to test whether widely accepted theories such as Island and Rensch’s rules can also apply to subterranean species (Herczeg et al.). The array of different studies in this Research Topic not only provide a general overview of subterranean adaptations and demonstrate the growing interest and scope of research on this topic, but also provide new insights into which and how specific adaptive traits evolve in species that have colonized the subterranean realm.

Author contributions

EL: Writing – original draft, Writing – review & editing. MN: Writing – review & editing. HB: Writing – review & editing.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

References

Bierbach D., Lukas J., Bergmann A., Elsner K., Höhne L., Weber C., et al. (2018). Insights into the social behavior of surface and cave-dwelling fish (Poecilia mexicana) in light and darkness through the use of a biomimetic robot. Front. Robotics AI 5, 3. doi: 10.3389/frobt.2018.00003

CrossRef Full Text | Google Scholar

Bilandžija H., Ćetković H., Jeffery W. R. (2012). Evolution of albinism in cave planthoppers by a convergent defect in the first step of melanin biosynthesis. Evol. Dev. 14 (2), 196–203. doi: 10.1111/j.1525-142X.2012.00535.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Christiansen K. (1962). Proposition pour la classification des animaux cavernicoles. Spelunca 2, 76–78.

Google Scholar

Culver D. C., Pipan T. (2015). Shifting paradigms of the evolution of cave life. Acta Carsologica 44, 415.

Google Scholar

Culver D. C., Pipan T. (2019). The biology of caves and other subterranean habitats (New York: Oxford University Press).

Google Scholar

Ficetola G. F., Canedoli C., Stoch F. (2019). The Racovitzan impediment and the hidden biodiversity of unexplored environments. Conserv. Biol. 33, 214–216. doi: 10.1111/cobi.13179

PubMed Abstract | CrossRef Full Text | Google Scholar

Gonzalez B. C., Worsaae K., Fontaneto D., Martínez A. (2017). Anophthalmia and elongation of body appendages in cave scale worms (Annelida: Aphroditiformia). Zoologica Scripta 47 (1), 106–121. doi: 10.1111/zsc.12258

CrossRef Full Text | Google Scholar

Hervant F. (2012). “Starvation in subterranean species versus surface-dwelling species: crustaceans, fish, and salamanders,” in Comparative physiology of fasting, starvation, and food limitation. Ed. McCue M. D. (Berlin: Springer), 91–102.

Google Scholar

Howarth F. G., Moldovan O. T. (2018). “The ecological classification of cave animals and their adaptations,” in Cave Ecology. Eds. Moldovan O. T., Kováč L., Halse S. (Berlin: Springer), 41–67.

Google Scholar

Jeffery W. R. (2020). Astyanax surface and cave fish morphs. EvoDevo 11, 14. doi: 10.1186/s13227-020-00159-6

PubMed Abstract | CrossRef Full Text | Google Scholar

Lipovšek S., Leitinger G., Janžekovič F., Kozel P., Dariš B., Perc M., et al. (2019). Towards understanding partial adaptation to the subterranean habitat in the European cave spider, Meta menardi: An ecocytological approach. Sci. Rep. 9, 9121. doi: 10.1038/s41598-019-45291-z

PubMed Abstract | CrossRef Full Text | Google Scholar

Lunghi E., Mammola S., Martínez A., Hesselberg T. (2023). Behavioural adjustments enable the colonization of subterranean environments. Zoological J. Linn. Soc. zlad133. doi: 10.1093/zoolinnean/zlad133

CrossRef Full Text | Google Scholar

Lunghi E., Zhao Y. (2020). Do Chinese cavefish show intraspecific variability in morphological traits? Ecol. Evol. 10 (14), 7723–7730. doi: 10.1002/ece3.6495

PubMed Abstract | CrossRef Full Text | Google Scholar

Mammola S., Lunghi E., Bilandzija H., Cardoso P., Grimm V., Schmidt S. I., et al. (2021). Collecting eco-evolutionary data in the dark: Impediments to subterranean research and how to overcome them. Ecol. Evol. 11 (11), 5911–5926. doi: 10.1002/ece3.7556

PubMed Abstract | CrossRef Full Text | Google Scholar

Plath M., Parzefall J., Körner K. E., Schlupp I. (2004). Sexual selection in darkness? Female mating preferences in surface- and cave-dwelling Atlantic mollies, Poecilia mexicana (Poeciliidae, Teleostei). Behav. Ecol. Sociobiology 55 (6), 596–601. doi: 10.1007/s00265-003-0750-9

CrossRef Full Text | Google Scholar

Soares D., Niemiller M. L. (2020). Extreme adaptation in caves. Anatomical Rec. 303, 15–23. doi: 10.1002/ar.24044

CrossRef Full Text | Google Scholar

Yoshizawa M., Yamamoto Y., O’Quin K. E., Jeffery W. R. (2012). Evolution of an adaptive behavior and its sensory receptors promotes eye regression in blind cavefish. BMC Biol. 10, 108. doi: 10.1186/1741-7007-10-108

PubMed Abstract | CrossRef Full Text | Google Scholar

Keywords: cave biology, biospeleology, troglophile, troglobite, stygobiont, underground, groundwater

Citation: Lunghi E, Niemiller ML and Bilandžija H (2024) Editorial: Adaptations to subterranean environments. Front. Ecol. Evol. 11:1354954. doi: 10.3389/fevo.2023.1354954

Received: 13 December 2023; Accepted: 21 December 2023;
Published: 04 January 2024.

Edited and Reviewed by:

Jordi Figuerola, Spanish National Research Council (CSIC), Spain

Copyright © 2024 Lunghi, Niemiller and Bilandžija. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Enrico Lunghi, ZW5yaWNvLmx1bmdoaUB1bml2YXEuaXQ=

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.