Predation threats for a 24-h period activated the extension of axons in the brains of Xenopus tadpoles

Tsukasa Mori,Naoyuki Yamamoto,Satoshi Hayakawa,Den Hatakeyama,Yoichiro Kitani,Akihiko Kashiwagi,Naoko Goto-Inoue,Keiko Kashiwagi,Kazumasa Machida

doi:10.1038/s41598-020-67975-7

Tsukasa Mori, Naoyuki Yamamoto + Show 7 more

Open Access

https://doi.org/10.1038/s41598-020-67975-7

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Abstract

The threat of predation is a driving force in the evolution of animals. We have previously reported that Xenopus laevis enhanced their tail muscles and increased their swimming speeds in the presence of Japanese larval salamander predators. Herein, we investigated the induced gene expression changes in the brains of tadpoles under the threat of predation using 3′-tag digital gene expression profiling. We found that many muscle genes were expressed after 24 h of exposure to predation. Ingenuity pathway analysis further showed that after 24 h of a predation threat, various signal transduction genes were stimulated, such as those affecting the actin cytoskeleton and CREB pathways, and that these might increase microtubule dynamics, axonogenesis, cognition, and memory. To verify the increase in microtubule dynamics, DiI was inserted through the tadpole nostrils. Extension of the axons was clearly observed from the nostril to the diencephalon and was significantly increased (P ≤ 0.0001) after 24 h of exposure to predation, compared with that of the control. The dynamic changes in the signal transductions appeared to bring about new connections in the neural networks, as suggested by the microtubule dynamics. These connections may result in improved memory and cognition abilities, and subsequently increase survivability.

Highlights

The threat of predation is a driving force in the evolution of animals
In this study we aimed to investigate two problems: first, which signal transduction pathways are altered in the X. laevis tadpole brains immediately after acute and chronic predation exposures, and in a post exposure period; and, second, if the adaptations in response to the predation threat occurred over short periods of time, as signal transduction pathways are known to be directly involved with such adaptations
Identification of genes expressed in the brain using 3′‐tag digital gene expression profil‐ ing

Summary

Introduction

The threat of predation is a driving force in the evolution of animals. We have previously reported that Xenopus laevis enhanced their tail muscles and increased their swimming speeds in the presence of Japanese larval salamander predators. One of their inducible changes is to increase both the height and length of their tails in the presence of a native predation threat, such as the dragonfly larvae[10,15,16] Japanese predators such as the larval salamander Hynobius lichenatus, have been found to elicit a predation threat response in X. laevis tadpoles, resulting in significant enhancements to their tail muscles and decreases in their relative ventral fin heights, leading to significantly higher than average swimming s peeds[17]. In this investigation, as the tadpoles were directly preyed upon by the predators, they may be responding to salamander kairomones, visual cues, or conspecific alarm cues released by the damaged tadpoles. Research into the survival adaptations in evolutionary scenarios against unfamiliar predators, using signal transduction analysis in the brain, has not previously been widely conducted

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