Genetic control of startle behavior in medaka fish.

Satomi Tsuboko,Hideaki Takeuchi,Teruhiro Okuyama,Kiyoshi Naruse,Yuji Suehiro,Minori Shinya,Takeo Kubo,Hiroyuki Takeda,Atsuko Shimada,Tetsuaki Kimura,Harold A Burgess

doi:10.1371/journal.pone.0112527

Abstract

Genetic polymorphisms are thought to generate intraspecific behavioral diversities, both within and among populations. The mechanisms underlying genetic control of behavioral properties, however, remain unclear in wild-type vertebrates, including humans. To explore this issue, we used diverse inbred strains of medaka fish (Oryzias latipes) established from the same and different local populations. Medaka exhibit a startle response to a visual stimulus (extinction of illumination) by rapidly bending their bodies (C-start) 20-ms after the stimulus presentation. We measured the rates of the response to repeated stimuli (1-s interval, 40 times) among four inbred strains, HNI-I, HNI-II, HO5, and Hd-rR-II1, and quantified two properties of the startle response: sensitivity (response rate to the first stimulus) and attenuation of the response probability with repeated stimulus presentation. Among the four strains, the greatest differences in these properties were detected between HNI-II and Hd-rR-II1. HNI-II exhibited high sensitivity (approximately 80%) and no attenuation, while Hd-rR-II1 exhibited low sensitivity (approximately 50%) and almost complete attenuation after only five stimulus presentations. Our findings suggested behavioral diversity of the startle response within a local population as well as among different populations. Linkage analysis with F2 progeny between HNI-II and Hd-rR-II1 detected quantitative trait loci (QTL) highly related to attenuation, but not to sensitivity, with a maximum logarithm of odds score of 11.82 on linkage group 16. The three genotypes (homozygous for HNI-II and Hd-rR-II1 alleles, and heterozygous) at the marker nearest the QTL correlated with attenuation. Our findings are the first to suggest that a single genomic region might be sufficient to generate individual differences in startle behavior between wild-type strains. Further identification of genetic polymorphisms that define the behavioral trait will contribute to our understanding of the neural mechanisms underlying behavioral diversity, allowing us to investigate the adaptive significance of intraspecific behavioral polymorphisms of the startle response.

Highlights

Many animals, including humans [1], exhibit intraspecific behavioral diversities [2,3,4,5,6], which are generated by learning and development, and by genetic factors [2,3]
We found that extinction of illumination robustly elicited a startle response in medaka fish
The findings of the present study demonstrated a significant difference in the startle response pattern among medaka inbred strains

Summary

Introduction

Many animals, including humans [1], exhibit intraspecific behavioral diversities [2,3,4,5,6], which are generated by learning and development, and by genetic factors [2,3]. Why individual differences are maintained in natural populations and how genetic polymorphisms generate behavioral diversities, remain unresolved. To explore this issue, we used medaka fish (Oryzias latipes). The availability of a dense genetic linkage map [15,16,17,18] and large-scale genomic data [19,20,21,22] allows us to identify the quantitative trait loci (QTL) for complex traits and to compare genetic polymorphisms in candidate genomic regions among medaka inbred strains. Medaka are considered an ideal animal model for the search of genetic factors that underlie complex traits [15]

Methods

Results

Conclusion