Abstract

The ostariophysian fishes are the most species-rich clade in freshwaters. This diversification has been suggested to be associated with the fright reaction presented in most ostariophysians. However, the genetic forces that underlie fright reaction remains poorly understood. In the present study, through integrating behavioral, physiological, transcriptomic, and evolutionary genomic analyses, we found that the fright reaction has a broad impact on zebrafish at multiple levels, including changes in swimming behaviors, cortisol levels, and gene expression patterns. In total, 1,555 and 1,599 differentially expressed genes were identified in olfactory mucosae and brain of zebrafish, respectively, with a greater number upregulated after the fright reaction. Functional annotation showed that response to stress and signal transduction were strongly represented, which is directly associated with the fright reaction. These differentially expressed genes were shown to be evolved accelerated under the influence of positive selection, indicating that protein-coding evolution has played a major role in fright reaction. We found the basal vomeronasal type 2 receptors (v2r) gene, v2rl1, displayed significantly decrease expression after fright reaction, which suggests that v2rs may be important to detect the alarm substance and induce the fright reaction. Collectively, based on our transcriptome and evolutionary genomics analyses, we suggest that transcriptional plasticity of gene may play an important role in fright reaction in ostariophysian fishes.

Highlights

  • As the largest group of fishes in freshwater habitats, Ostariophysi consists of more than 10,000 currently recognized species around the world, which constitutes roughly 75% of all freshwater fish species, 30% of all known bony fish species, and one-sixth of all vertebrate species (Nelson, 2006; Van Der Laan et al, 2014)

  • We found that the swimming trajectory of zebrafish was evenly distributed in the rectangular tank when administered with deionized water (Figure 1A)

  • The zebrafish exposed with alarm substances spent an much less time in the upper part of the tank compared with the control group (P = 1.6 × 10−16, Figure 1C), but showed a significantly higher frequency of freezing bouts, relative to controls (P = 1.7 × 10−5, Figure 1D)

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Summary

Introduction

As the largest group of fishes in freshwater habitats, Ostariophysi consists of more than 10,000 currently recognized species around the world, which constitutes roughly 75% of all freshwater fish species, 30% of all known bony fish species, and one-sixth of all vertebrate species (Nelson, 2006; Van Der Laan et al, 2014). The superorder includes the enormous Mekong giant catfish (Pangasianodon gigas) 2.7 m in length and weighing 300 kg (Siluriformes), well-known electric eel (Electrophorus electricus) (Gymnotiformes), and the apex predators piranhas (Characiformes) Considering their ancient origin, enormous evolutionary and ecological diversity, as well as the nearly limitation of all members to freshwater, ostariophysan fishes have attracted a great deal of attention in evolutionary biology and biogeography since the definition of this group (Fink and Fink, 1981; Saitoh et al, 2003; Briggs, 2005; Nakatani et al, 2011; Chen et al, 2013; Arcila et al, 2017; Chakrabarty et al, 2017). What are the genes responsible for the fright reaction? How many genes change expression levels during the fright reaction?

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