Adaptive shift of active electroreception in weakly electric fish for troglobitic life

The adaptive-shift hypothesis for the evolution of cave-dwelling species posits that ancestor species in surface habitats had exaptations for subterranean life that were exploited when individuals invaded caves. Weakly electric Gymnotiform fishes, nocturnal South American teleost fishes, have featur...

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Main Authors: Daphne Soares, Kathryn Gallman, Maria Elina Bichuette, Eric S. Fortune
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-09-01
Series:Frontiers in Ecology and Evolution
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fevo.2023.1180506/full
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author Daphne Soares
Kathryn Gallman
Maria Elina Bichuette
Eric S. Fortune
author_facet Daphne Soares
Kathryn Gallman
Maria Elina Bichuette
Eric S. Fortune
author_sort Daphne Soares
collection DOAJ
description The adaptive-shift hypothesis for the evolution of cave-dwelling species posits that ancestor species in surface habitats had exaptations for subterranean life that were exploited when individuals invaded caves. Weakly electric Gymnotiform fishes, nocturnal South American teleost fishes, have features that appear to be likely exaptations for troglobitic life. These fishes have active electrosensory systems in which fish generate weak electric fields that are detected by specialized electroreceptors. Gymnotiform fishes use their electric fields for navigation, prey capture (scene analysis), and social communication. Although active electrosensory systems appear to be exaptations for troglobitic life, as fish use these systems to “see in the dark”, producing electric fields is energetically costly. Cave habitats, which often are low in resources, may not be able to support such high energetic demands. Eigenmannia vicentespelaea, a species of weakly electric fish that is endemic to the São Vicente II cave in central Brazil, surprisingly generates stronger electric fields than their surface relatives. The increase in strength of electric fields may result simply from differences in size between cave and surface populations, but may also be due to lack of predation pressure in the cave or increases in “sensory volumes” and acuity that improve prey localization and capture. Eigenmannia vicentespelaea exhibits the classical phenotypes of any troglobitic fish: these fish have small to nonexistent eyes and loss of pigmentation. The closest living surface relative, Eigenmannia trilineata, inhabits streams nearby and has eyes and pigmentation. The electrosensory and locomotor behavior of both species of fish were measured in their natural habitats using a grid recording system. Surface Eigenmannia exhibited dramatic circadian changes in social behavior, such as hiding under rocks during the day and foraging in groups at night, while cave Eigenmannia displayed territorial behavior with no apparent circadian modulations. The territorial behavior involved electrical and movement-based interactions that may be a form of boundary patrolling. Electrosocial behavior and scene analysis are mechanistically interlinked because both stem from active sensing tactics.
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spelling doaj.art-d8c1da5b6e314308acefbf20578d54202023-09-01T10:02:38ZengFrontiers Media S.A.Frontiers in Ecology and Evolution2296-701X2023-09-011110.3389/fevo.2023.11805061180506Adaptive shift of active electroreception in weakly electric fish for troglobitic lifeDaphne Soares0Kathryn Gallman1Maria Elina Bichuette2Eric S. Fortune3Biological Sciences, New Jersey Institute of Technology, Newark, NJ, United StatesBiological Sciences, New Jersey Institute of Technology, Newark, NJ, United StatesDepartamento de Ecologia e Biologia Evolutiva, Universidade Federal de São Carlos, São Carlos, BrazilBiological Sciences, New Jersey Institute of Technology, Newark, NJ, United StatesThe adaptive-shift hypothesis for the evolution of cave-dwelling species posits that ancestor species in surface habitats had exaptations for subterranean life that were exploited when individuals invaded caves. Weakly electric Gymnotiform fishes, nocturnal South American teleost fishes, have features that appear to be likely exaptations for troglobitic life. These fishes have active electrosensory systems in which fish generate weak electric fields that are detected by specialized electroreceptors. Gymnotiform fishes use their electric fields for navigation, prey capture (scene analysis), and social communication. Although active electrosensory systems appear to be exaptations for troglobitic life, as fish use these systems to “see in the dark”, producing electric fields is energetically costly. Cave habitats, which often are low in resources, may not be able to support such high energetic demands. Eigenmannia vicentespelaea, a species of weakly electric fish that is endemic to the São Vicente II cave in central Brazil, surprisingly generates stronger electric fields than their surface relatives. The increase in strength of electric fields may result simply from differences in size between cave and surface populations, but may also be due to lack of predation pressure in the cave or increases in “sensory volumes” and acuity that improve prey localization and capture. Eigenmannia vicentespelaea exhibits the classical phenotypes of any troglobitic fish: these fish have small to nonexistent eyes and loss of pigmentation. The closest living surface relative, Eigenmannia trilineata, inhabits streams nearby and has eyes and pigmentation. The electrosensory and locomotor behavior of both species of fish were measured in their natural habitats using a grid recording system. Surface Eigenmannia exhibited dramatic circadian changes in social behavior, such as hiding under rocks during the day and foraging in groups at night, while cave Eigenmannia displayed territorial behavior with no apparent circadian modulations. The territorial behavior involved electrical and movement-based interactions that may be a form of boundary patrolling. Electrosocial behavior and scene analysis are mechanistically interlinked because both stem from active sensing tactics.https://www.frontiersin.org/articles/10.3389/fevo.2023.1180506/fullcaveweakly electric fishevolutionEODterritorytroglomorphism
spellingShingle Daphne Soares
Kathryn Gallman
Maria Elina Bichuette
Eric S. Fortune
Adaptive shift of active electroreception in weakly electric fish for troglobitic life
Frontiers in Ecology and Evolution
cave
weakly electric fish
evolution
EOD
territory
troglomorphism
title Adaptive shift of active electroreception in weakly electric fish for troglobitic life
title_full Adaptive shift of active electroreception in weakly electric fish for troglobitic life
title_fullStr Adaptive shift of active electroreception in weakly electric fish for troglobitic life
title_full_unstemmed Adaptive shift of active electroreception in weakly electric fish for troglobitic life
title_short Adaptive shift of active electroreception in weakly electric fish for troglobitic life
title_sort adaptive shift of active electroreception in weakly electric fish for troglobitic life
topic cave
weakly electric fish
evolution
EOD
territory
troglomorphism
url https://www.frontiersin.org/articles/10.3389/fevo.2023.1180506/full
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AT mariaelinabichuette adaptiveshiftofactiveelectroreceptioninweaklyelectricfishfortroglobiticlife
AT ericsfortune adaptiveshiftofactiveelectroreceptioninweaklyelectricfishfortroglobiticlife