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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...
Autores principales: | , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2023
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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. |
format | Online Article Text |
id | pubmed-10279953 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
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
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title_full | Novel predator-induced phenotypic plasticity by hemoglobin and physiological changes in the brain of Xenopus tropicalis
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title_fullStr | Novel predator-induced phenotypic plasticity by hemoglobin and physiological changes in the brain of Xenopus tropicalis
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title_full_unstemmed | Novel predator-induced phenotypic plasticity by hemoglobin and physiological changes in the brain of Xenopus tropicalis
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title_short | Novel predator-induced phenotypic plasticity by hemoglobin and physiological changes in the brain of Xenopus tropicalis
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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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