Genetic control of startle behavior in medaka fish
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...
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| creator | Tsuboko, Satomi Kimura, Tetsuaki Shinya, Minori Suehiro, Yuji Okuyama, Teruhiro Shimada, Atsuko Takeda, Hiroyuki Naruse, Kiyoshi Kubo, Takeo Takeuchi, Hideaki |
| description | 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. |
| doi_str_mv | 10.1371/journal.pone.0112527 |
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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.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0112527</identifier><identifier>PMID: 25393539</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adaptiveness ; Animal behavior ; Animals ; Attenuation ; Behavior, Animal ; Biology and Life Sciences ; Crosses, Genetic ; Gene mapping ; Genetic control ; Genome ; Genomics ; Genotype ; Genotypes ; Inbreeding ; Linkage analysis ; Local population ; Movement ; Odds Ratio ; Oryzias - genetics ; Oryzias latipes ; Photic Stimulation ; Polymorphism, Genetic ; Population genetics ; Populations ; Progeny ; Properties (attributes) ; Quantitative Trait Loci ; Reflex, Startle - genetics ; Rodents ; Science ; Sensitivity ; Species extinction ; Startle response ; Strains (organisms) ; Vertebrates ; Visual stimuli</subject><ispartof>PloS one, 2014-11, Vol.9 (11), p.e112527-e112527</ispartof><rights>2014 Tsuboko et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2014 Tsuboko et al 2014 Tsuboko et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c592t-ca430e160890a555f53c4635c43da160407cadcda30c0ebbc1bcfdcd7985f2173</citedby><cites>FETCH-LOGICAL-c592t-ca430e160890a555f53c4635c43da160407cadcda30c0ebbc1bcfdcd7985f2173</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4231031/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4231031/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2100,2926,23865,27923,27924,53790,53792,79371,79372</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25393539$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Burgess, Harold A.</contributor><creatorcontrib>Tsuboko, Satomi</creatorcontrib><creatorcontrib>Kimura, Tetsuaki</creatorcontrib><creatorcontrib>Shinya, Minori</creatorcontrib><creatorcontrib>Suehiro, Yuji</creatorcontrib><creatorcontrib>Okuyama, Teruhiro</creatorcontrib><creatorcontrib>Shimada, Atsuko</creatorcontrib><creatorcontrib>Takeda, Hiroyuki</creatorcontrib><creatorcontrib>Naruse, Kiyoshi</creatorcontrib><creatorcontrib>Kubo, Takeo</creatorcontrib><creatorcontrib>Takeuchi, Hideaki</creatorcontrib><title>Genetic control of startle behavior in medaka fish</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>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.</description><subject>Adaptiveness</subject><subject>Animal behavior</subject><subject>Animals</subject><subject>Attenuation</subject><subject>Behavior, Animal</subject><subject>Biology and Life Sciences</subject><subject>Crosses, Genetic</subject><subject>Gene mapping</subject><subject>Genetic control</subject><subject>Genome</subject><subject>Genomics</subject><subject>Genotype</subject><subject>Genotypes</subject><subject>Inbreeding</subject><subject>Linkage analysis</subject><subject>Local population</subject><subject>Movement</subject><subject>Odds Ratio</subject><subject>Oryzias - genetics</subject><subject>Oryzias latipes</subject><subject>Photic Stimulation</subject><subject>Polymorphism, Genetic</subject><subject>Population genetics</subject><subject>Populations</subject><subject>Progeny</subject><subject>Properties (attributes)</subject><subject>Quantitative Trait Loci</subject><subject>Reflex, Startle - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tsuboko, Satomi</au><au>Kimura, Tetsuaki</au><au>Shinya, Minori</au><au>Suehiro, Yuji</au><au>Okuyama, Teruhiro</au><au>Shimada, Atsuko</au><au>Takeda, Hiroyuki</au><au>Naruse, Kiyoshi</au><au>Kubo, Takeo</au><au>Takeuchi, Hideaki</au><au>Burgess, Harold A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genetic control of startle behavior in medaka fish</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014-11-13</date><risdate>2014</risdate><volume>9</volume><issue>11</issue><spage>e112527</spage><epage>e112527</epage><pages>e112527-e112527</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25393539</pmid><doi>10.1371/journal.pone.0112527</doi><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS); EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adaptiveness Animal behavior Animals Attenuation Behavior, Animal Biology and Life Sciences Crosses, Genetic Gene mapping Genetic control Genome Genomics Genotype Genotypes Inbreeding Linkage analysis Local population Movement Odds Ratio Oryzias - genetics Oryzias latipes Photic Stimulation Polymorphism, Genetic Population genetics Populations Progeny Properties (attributes) Quantitative Trait Loci Reflex, Startle - genetics Rodents Science Sensitivity Species extinction Startle response Strains (organisms) Vertebrates Visual stimuli |
| title | Genetic control of startle behavior in medaka fish |
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