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...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-06-01
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| Series: | Frontiers in Physiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fphys.2023.1178869/full |
| _version_ | 1797810535779008512 |
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| author | Tsukasa Mori Kazumasa Machida Yuki Kudou Masaya Kimishima Kaito Sassa Naoko Goto-Inoue Ryuhei Minei Atsushi Ogura Yui Kobayashi Kentaro Kamiya Daiki Nakaya Naoyuki Yamamoto Akihiko Kashiwagi Keiko Kashiwagi |
| author_facet | Tsukasa Mori Kazumasa Machida Yuki Kudou Masaya Kimishima Kaito Sassa Naoko Goto-Inoue Ryuhei Minei Atsushi Ogura Yui Kobayashi Kentaro Kamiya Daiki Nakaya Naoyuki Yamamoto Akihiko Kashiwagi Keiko Kashiwagi |
| author_sort | Tsukasa Mori |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-03-13T07:10:20Z |
| format | Article |
| id | doaj.art-f868d3575bee464fbe1342747430fd76 |
| institution | Directory Open Access Journal |
| issn | 1664-042X |
| language | English |
| last_indexed | 2024-03-13T07:10:20Z |
| publishDate | 2023-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-f868d3575bee464fbe1342747430fd762023-06-06T04:49:53ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2023-06-011410.3389/fphys.2023.11788691178869Novel predator-induced phenotypic plasticity by hemoglobin and physiological changes in the brain of Xenopus tropicalisTsukasa Mori0Kazumasa Machida1Yuki Kudou2Masaya Kimishima3Kaito Sassa4Naoko Goto-Inoue5Ryuhei Minei6Atsushi Ogura7Yui Kobayashi8Kentaro Kamiya9Daiki Nakaya10Naoyuki Yamamoto11Akihiko Kashiwagi12Keiko Kashiwagi13Nihon University College of Bioresource Sciences, Fujisawa, JapanNihon University College of Bioresource Sciences, Fujisawa, JapanNihon University College of Bioresource Sciences, Fujisawa, JapanNihon University College of Bioresource Sciences, Fujisawa, JapanNihon University College of Bioresource Sciences, Fujisawa, JapanNihon University College of Bioresource Sciences, Fujisawa, JapanDepartment of Computer Bioscience, Nagahama Institute of Bio-Science and Technology, Nagahama, JapanDepartment of Computer Bioscience, Nagahama Institute of Bio-Science and Technology, Nagahama, JapanMilk. Inc, Tokyo, JapanMilk. Inc, Tokyo, JapanMilk. Inc, Tokyo, JapanDepartment of Animal Sciences, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, JapanHiroshima University Amphibian Research Center, Hiroshima, JapanHiroshima University Amphibian Research Center, Hiroshima, JapanOrganisms 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.https://www.frontiersin.org/articles/10.3389/fphys.2023.1178869/fullphenotypic plasticityXenopus tadpolesnovel predatorsthreat responsehemoglobin |
| spellingShingle | Tsukasa Mori Kazumasa Machida Yuki Kudou Masaya Kimishima Kaito Sassa Naoko Goto-Inoue Ryuhei Minei Atsushi Ogura Yui Kobayashi Kentaro Kamiya Daiki Nakaya Naoyuki Yamamoto Akihiko Kashiwagi Keiko Kashiwagi Novel predator-induced phenotypic plasticity by hemoglobin and physiological changes in the brain of Xenopus tropicalis Frontiers in Physiology phenotypic plasticity Xenopus tadpoles novel predators threat response hemoglobin |
| 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 | phenotypic plasticity Xenopus tadpoles novel predators threat response hemoglobin |
| url | https://www.frontiersin.org/articles/10.3389/fphys.2023.1178869/full |
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