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Novel predator-induced phenotypic plasticity by hemoglobin and physiological changes in the brain of Xenopus tropicalis

Organisms adapt to changes in their environment to survive. The emergence of predators is an example of environmental change, and organisms try to change their external phenotypic systems and physiological mechanisms to adapt to such changes. In general, prey exhibit different phenotypes to predator...

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Autores principales: Mori, Tsukasa, Machida, Kazumasa, Kudou, Yuki, Kimishima, Masaya, Sassa, Kaito, Goto-Inoue, Naoko, Minei, Ryuhei, Ogura, Atsushi, Kobayashi, Yui, Kamiya, Kentaro, Nakaya, Daiki, Yamamoto, Naoyuki, Kashiwagi, Akihiko, Kashiwagi, Keiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10279953/
https://www.ncbi.nlm.nih.gov/pubmed/37346489
http://dx.doi.org/10.3389/fphys.2023.1178869
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author Mori, Tsukasa
Machida, Kazumasa
Kudou, Yuki
Kimishima, Masaya
Sassa, Kaito
Goto-Inoue, Naoko
Minei, Ryuhei
Ogura, Atsushi
Kobayashi, Yui
Kamiya, Kentaro
Nakaya, Daiki
Yamamoto, Naoyuki
Kashiwagi, Akihiko
Kashiwagi, Keiko
author_facet Mori, Tsukasa
Machida, Kazumasa
Kudou, Yuki
Kimishima, Masaya
Sassa, Kaito
Goto-Inoue, Naoko
Minei, Ryuhei
Ogura, Atsushi
Kobayashi, Yui
Kamiya, Kentaro
Nakaya, Daiki
Yamamoto, Naoyuki
Kashiwagi, Akihiko
Kashiwagi, Keiko
author_sort Mori, Tsukasa
collection PubMed
description Organisms adapt to changes in their environment to survive. The emergence of predators is an example of environmental change, and organisms try to change their external phenotypic systems and physiological mechanisms to adapt to such changes. In general, prey exhibit different phenotypes to predators owing to historically long-term prey-predator interactions. However, when presented with a novel predator, the extent and rate of phenotypic plasticity in prey are largely unknown. Therefore, exploring the physiological adaptive response of organisms to novel predators is a crucial topic in physiology and evolutionary biology. Counterintuitively, Xenopus tropicalis tadpoles do not exhibit distinct external phenotypes when exposed to new predation threats. Accordingly, we examined the brains of X. tropicalis tadpoles to understand their response to novel predation pressure in the absence of apparent external morphological adaptations. Principal component analysis of fifteen external morphological parameters showed that each external morphological site varied nonlinearly with predator exposure time. However, the overall percentage change in principal components during the predation threat (24 h) was shown to significantly (p < 0.05) alter tadpole morphology compared with that during control or 5-day out treatment (5 days of exposure to predation followed by 5 days of no exposure). However, the adaptive strategy of the altered sites was unknown because the changes were not specific to a particular site but were rather nonlinear in various sites. Therefore, RNA-seq, metabolomic, Ingenuity Pathway Analysis, and Kyoto Encyclopedia of Genes and Genomes analyses were performed on the entire brain to investigate physiological changes in the brain, finding that glycolysis-driven ATP production was enhanced and ß-oxidation and the tricarboxylic acid cycle were downregulated in response to predation stress. Superoxide dismutase was upregulated after 6 h of exposure to new predation pressure, and radical production was reduced. Hemoglobin was also increased in the brain, forming oxyhemoglobin, which is known to scavenge hydroxyl radicals in the midbrain and hindbrain. These suggest that X. tropicalis tadpoles do not develop external morphological adaptations that are positively correlated with predation pressure, such as tail elongation, in response to novel predators; however, they improve their brain functionality when exposed to a novel predator.
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spelling pubmed-102799532023-06-21 Novel predator-induced phenotypic plasticity by hemoglobin and physiological changes in the brain of Xenopus tropicalis Mori, Tsukasa Machida, Kazumasa Kudou, Yuki Kimishima, Masaya Sassa, Kaito Goto-Inoue, Naoko Minei, Ryuhei Ogura, Atsushi Kobayashi, Yui Kamiya, Kentaro Nakaya, Daiki Yamamoto, Naoyuki Kashiwagi, Akihiko Kashiwagi, Keiko Front Physiol Physiology Organisms adapt to changes in their environment to survive. The emergence of predators is an example of environmental change, and organisms try to change their external phenotypic systems and physiological mechanisms to adapt to such changes. In general, prey exhibit different phenotypes to predators owing to historically long-term prey-predator interactions. However, when presented with a novel predator, the extent and rate of phenotypic plasticity in prey are largely unknown. Therefore, exploring the physiological adaptive response of organisms to novel predators is a crucial topic in physiology and evolutionary biology. Counterintuitively, Xenopus tropicalis tadpoles do not exhibit distinct external phenotypes when exposed to new predation threats. Accordingly, we examined the brains of X. tropicalis tadpoles to understand their response to novel predation pressure in the absence of apparent external morphological adaptations. Principal component analysis of fifteen external morphological parameters showed that each external morphological site varied nonlinearly with predator exposure time. However, the overall percentage change in principal components during the predation threat (24 h) was shown to significantly (p < 0.05) alter tadpole morphology compared with that during control or 5-day out treatment (5 days of exposure to predation followed by 5 days of no exposure). However, the adaptive strategy of the altered sites was unknown because the changes were not specific to a particular site but were rather nonlinear in various sites. Therefore, RNA-seq, metabolomic, Ingenuity Pathway Analysis, and Kyoto Encyclopedia of Genes and Genomes analyses were performed on the entire brain to investigate physiological changes in the brain, finding that glycolysis-driven ATP production was enhanced and ß-oxidation and the tricarboxylic acid cycle were downregulated in response to predation stress. Superoxide dismutase was upregulated after 6 h of exposure to new predation pressure, and radical production was reduced. Hemoglobin was also increased in the brain, forming oxyhemoglobin, which is known to scavenge hydroxyl radicals in the midbrain and hindbrain. These suggest that X. tropicalis tadpoles do not develop external morphological adaptations that are positively correlated with predation pressure, such as tail elongation, in response to novel predators; however, they improve their brain functionality when exposed to a novel predator. Frontiers Media S.A. 2023-06-06 /pmc/articles/PMC10279953/ /pubmed/37346489 http://dx.doi.org/10.3389/fphys.2023.1178869 Text en Copyright © 2023 Mori, Machida, Kudou, Kimishima, Sassa, Goto-Inoue, Minei, Ogura, Kobayashi, Kamiya, Nakaya, Yamamoto, Kashiwagi and Kashiwagi. https://creativecommons.org/licenses/by/4.0/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.
spellingShingle Physiology
Mori, Tsukasa
Machida, Kazumasa
Kudou, Yuki
Kimishima, Masaya
Sassa, Kaito
Goto-Inoue, Naoko
Minei, Ryuhei
Ogura, Atsushi
Kobayashi, Yui
Kamiya, Kentaro
Nakaya, Daiki
Yamamoto, Naoyuki
Kashiwagi, Akihiko
Kashiwagi, Keiko
Novel predator-induced phenotypic plasticity by hemoglobin and physiological changes in the brain of Xenopus tropicalis
title Novel predator-induced phenotypic plasticity by hemoglobin and physiological changes in the brain of Xenopus tropicalis
title_full Novel predator-induced phenotypic plasticity by hemoglobin and physiological changes in the brain of Xenopus tropicalis
title_fullStr Novel predator-induced phenotypic plasticity by hemoglobin and physiological changes in the brain of Xenopus tropicalis
title_full_unstemmed Novel predator-induced phenotypic plasticity by hemoglobin and physiological changes in the brain of Xenopus tropicalis
title_short Novel predator-induced phenotypic plasticity by hemoglobin and physiological changes in the brain of Xenopus tropicalis
title_sort novel predator-induced phenotypic plasticity by hemoglobin and physiological changes in the brain of xenopus tropicalis
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10279953/
https://www.ncbi.nlm.nih.gov/pubmed/37346489
http://dx.doi.org/10.3389/fphys.2023.1178869
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