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Bidirectional sex change and plasticity of gonadal phases in the goby Lubricogobius exiguus
Of the ca. 500 known hermaphroditic fish species, bidirectional sex change and simultaneous hermaphroditism are currently known in 69 and 57 species, respectively. Both bidirectional sex change and simultaneous hermaphroditism are predicted to evolve when mating opportunities are limited, such as in...
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Published in: | Journal of fish biology 2023-05, Vol.102 (5), p.1079-1087 |
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creator | Oyama, Takumi Sonoyama, Takayuki Kasai, Miku Sakai, Yoichi Sunobe, Tomoki |
description | Of the ca. 500 known hermaphroditic fish species, bidirectional sex change and simultaneous hermaphroditism are currently known in 69 and 57 species, respectively. Both bidirectional sex change and simultaneous hermaphroditism are predicted to evolve when mating opportunities are limited, such as in cases of low‐density distribution and low mobility of individuals. However, the plasticity of sex is adaptive in obtaining mating opportunities, especially when there is mate loss. Pair‐rearing experiments and histological observations of gonads of the goby Lubricogobius exiguus, which has low‐density distributions and low mobility, showed bidirectional sex change. The male‐role individuals in pairs had gonads in which only the testis was functional (male‐phase), whereas the female‐role individuals had two types of gonads: only the ovary was functional (female‐phase) or both testis and ovary were functional (simultaneously hermaphroditic phase, SH‐phase). In addition, single‐rearing experiments showed SH‐phase gonads in all individuals, and some cyclic spawning but no self‐fertilization occurred. These results revealed that L. exiguus has an unusual sexual pattern among hermaphroditic fishes because they undergo bidirectional sex change and some maintain SH‐phase gonads. These findings indicate that the low‐density distribution and low mobility of L. exiguus in their natural habitat may have influenced the evolution of this unique sexual pattern. |
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Both bidirectional sex change and simultaneous hermaphroditism are predicted to evolve when mating opportunities are limited, such as in cases of low‐density distribution and low mobility of individuals. However, the plasticity of sex is adaptive in obtaining mating opportunities, especially when there is mate loss. Pair‐rearing experiments and histological observations of gonads of the goby Lubricogobius exiguus, which has low‐density distributions and low mobility, showed bidirectional sex change. The male‐role individuals in pairs had gonads in which only the testis was functional (male‐phase), whereas the female‐role individuals had two types of gonads: only the ovary was functional (female‐phase) or both testis and ovary were functional (simultaneously hermaphroditic phase, SH‐phase). In addition, single‐rearing experiments showed SH‐phase gonads in all individuals, and some cyclic spawning but no self‐fertilization occurred. These results revealed that L. exiguus has an unusual sexual pattern among hermaphroditic fishes because they undergo bidirectional sex change and some maintain SH‐phase gonads. These findings indicate that the low‐density distribution and low mobility of L. exiguus in their natural habitat may have influenced the evolution of this unique sexual pattern.</description><identifier>ISSN: 0022-1112</identifier><identifier>EISSN: 1095-8649</identifier><identifier>DOI: 10.1111/jfb.15363</identifier><identifier>PMID: 36856167</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Animals ; bidirectional sex change ; Biological fertilization ; Density ; Density distribution ; Disorders of Sex Development ; Distribution ; Female ; Females ; Fertilization ; Fish ; Fishes ; Gonads ; Hermaphroditic Organisms ; Hermaphroditism ; low‐density distribution ; Lubricogobius exiguus ; Male ; Males ; Marine fishes ; Mating ; Mobility ; Ovaries ; Ovary ; Plastic properties ; Plasticity ; Reproductive behaviour ; Self-fertilization ; Sex ; Sex Determination Processes ; sexual plasticity ; simultaneous hermaphrodite ; Spawning ; Testes ; Testis</subject><ispartof>Journal of fish biology, 2023-05, Vol.102 (5), p.1079-1087</ispartof><rights>2023 Fisheries Society of the British Isles.</rights><rights>Journal of Fish Biology © 2023 The Fisheries Society of the British Isles</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4543-ea00e07f14bf147db543b80278e50e5efb372f06ad6f4e40cfbfb033644b1beb3</citedby><cites>FETCH-LOGICAL-c4543-ea00e07f14bf147db543b80278e50e5efb372f06ad6f4e40cfbfb033644b1beb3</cites><orcidid>0000-0003-2854-3202 ; 0000-0001-7137-3726 ; 0000-0002-9602-1601</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36856167$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Oyama, Takumi</creatorcontrib><creatorcontrib>Sonoyama, Takayuki</creatorcontrib><creatorcontrib>Kasai, Miku</creatorcontrib><creatorcontrib>Sakai, Yoichi</creatorcontrib><creatorcontrib>Sunobe, Tomoki</creatorcontrib><title>Bidirectional sex change and plasticity of gonadal phases in the goby Lubricogobius exiguus</title><title>Journal of fish biology</title><addtitle>J Fish Biol</addtitle><description>Of the ca. 500 known hermaphroditic fish species, bidirectional sex change and simultaneous hermaphroditism are currently known in 69 and 57 species, respectively. Both bidirectional sex change and simultaneous hermaphroditism are predicted to evolve when mating opportunities are limited, such as in cases of low‐density distribution and low mobility of individuals. However, the plasticity of sex is adaptive in obtaining mating opportunities, especially when there is mate loss. Pair‐rearing experiments and histological observations of gonads of the goby Lubricogobius exiguus, which has low‐density distributions and low mobility, showed bidirectional sex change. The male‐role individuals in pairs had gonads in which only the testis was functional (male‐phase), whereas the female‐role individuals had two types of gonads: only the ovary was functional (female‐phase) or both testis and ovary were functional (simultaneously hermaphroditic phase, SH‐phase). In addition, single‐rearing experiments showed SH‐phase gonads in all individuals, and some cyclic spawning but no self‐fertilization occurred. These results revealed that L. exiguus has an unusual sexual pattern among hermaphroditic fishes because they undergo bidirectional sex change and some maintain SH‐phase gonads. These findings indicate that the low‐density distribution and low mobility of L. exiguus in their natural habitat may have influenced the evolution of this unique sexual pattern.</description><subject>Animals</subject><subject>bidirectional sex change</subject><subject>Biological fertilization</subject><subject>Density</subject><subject>Density distribution</subject><subject>Disorders of Sex Development</subject><subject>Distribution</subject><subject>Female</subject><subject>Females</subject><subject>Fertilization</subject><subject>Fish</subject><subject>Fishes</subject><subject>Gonads</subject><subject>Hermaphroditic Organisms</subject><subject>Hermaphroditism</subject><subject>low‐density distribution</subject><subject>Lubricogobius exiguus</subject><subject>Male</subject><subject>Males</subject><subject>Marine fishes</subject><subject>Mating</subject><subject>Mobility</subject><subject>Ovaries</subject><subject>Ovary</subject><subject>Plastic properties</subject><subject>Plasticity</subject><subject>Reproductive behaviour</subject><subject>Self-fertilization</subject><subject>Sex</subject><subject>Sex Determination Processes</subject><subject>sexual plasticity</subject><subject>simultaneous hermaphrodite</subject><subject>Spawning</subject><subject>Testes</subject><subject>Testis</subject><issn>0022-1112</issn><issn>1095-8649</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNp10M9LwzAUB_AgipvTg_-ABLzoodtL0187uuH8wcCLnjyUpH3ZMrp2Ni2u_71vbnoQDISEx4cvvC9jlwKGgs5oZfRQhDKSR6wvYBx6SRSMj1kfwPc9An6PnTm3AoCxHMtT1pNREkYiivvsfWJzW2PW2KpUBXe45dlSlQvkqsz5plCusZltOl4ZviCSE9oslUPHbcmbJdJUd3ze6tpmFf1t6zhu7aJt3Tk7MapweHF4B-xtdv86ffTmLw9P07u5lwVhID1UAAixEYGmG-eahjoBP04wBAzRaBn7BiKVRybAADKjjQYpoyDQQqOWA3azz93U1UeLrknX1mVYFKrEqnUpJQl_109C9PoPXVVtTZuTIiRDH2IgdbtXWV05V6NJN7Vdq7pLBaS7xlNqPP1unOzVIbHVa8x_5U_FBEZ78GkL7P5PSp9nk33kFx1nikw</recordid><startdate>202305</startdate><enddate>202305</enddate><creator>Oyama, Takumi</creator><creator>Sonoyama, Takayuki</creator><creator>Kasai, Miku</creator><creator>Sakai, Yoichi</creator><creator>Sunobe, Tomoki</creator><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7SN</scope><scope>7TN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-2854-3202</orcidid><orcidid>https://orcid.org/0000-0001-7137-3726</orcidid><orcidid>https://orcid.org/0000-0002-9602-1601</orcidid></search><sort><creationdate>202305</creationdate><title>Bidirectional sex change and plasticity of gonadal phases in the goby Lubricogobius exiguus</title><author>Oyama, Takumi ; Sonoyama, Takayuki ; Kasai, Miku ; Sakai, Yoichi ; Sunobe, Tomoki</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4543-ea00e07f14bf147db543b80278e50e5efb372f06ad6f4e40cfbfb033644b1beb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Animals</topic><topic>bidirectional sex change</topic><topic>Biological fertilization</topic><topic>Density</topic><topic>Density distribution</topic><topic>Disorders of Sex Development</topic><topic>Distribution</topic><topic>Female</topic><topic>Females</topic><topic>Fertilization</topic><topic>Fish</topic><topic>Fishes</topic><topic>Gonads</topic><topic>Hermaphroditic Organisms</topic><topic>Hermaphroditism</topic><topic>low‐density distribution</topic><topic>Lubricogobius exiguus</topic><topic>Male</topic><topic>Males</topic><topic>Marine fishes</topic><topic>Mating</topic><topic>Mobility</topic><topic>Ovaries</topic><topic>Ovary</topic><topic>Plastic properties</topic><topic>Plasticity</topic><topic>Reproductive behaviour</topic><topic>Self-fertilization</topic><topic>Sex</topic><topic>Sex Determination Processes</topic><topic>sexual plasticity</topic><topic>simultaneous hermaphrodite</topic><topic>Spawning</topic><topic>Testes</topic><topic>Testis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Oyama, Takumi</creatorcontrib><creatorcontrib>Sonoyama, Takayuki</creatorcontrib><creatorcontrib>Kasai, Miku</creatorcontrib><creatorcontrib>Sakai, Yoichi</creatorcontrib><creatorcontrib>Sunobe, Tomoki</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Ecology Abstracts</collection><collection>Oceanic Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of fish biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Oyama, Takumi</au><au>Sonoyama, Takayuki</au><au>Kasai, Miku</au><au>Sakai, Yoichi</au><au>Sunobe, Tomoki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Bidirectional sex change and plasticity of gonadal phases in the goby Lubricogobius exiguus</atitle><jtitle>Journal of fish biology</jtitle><addtitle>J Fish Biol</addtitle><date>2023-05</date><risdate>2023</risdate><volume>102</volume><issue>5</issue><spage>1079</spage><epage>1087</epage><pages>1079-1087</pages><issn>0022-1112</issn><eissn>1095-8649</eissn><abstract>Of the ca. 500 known hermaphroditic fish species, bidirectional sex change and simultaneous hermaphroditism are currently known in 69 and 57 species, respectively. Both bidirectional sex change and simultaneous hermaphroditism are predicted to evolve when mating opportunities are limited, such as in cases of low‐density distribution and low mobility of individuals. However, the plasticity of sex is adaptive in obtaining mating opportunities, especially when there is mate loss. Pair‐rearing experiments and histological observations of gonads of the goby Lubricogobius exiguus, which has low‐density distributions and low mobility, showed bidirectional sex change. The male‐role individuals in pairs had gonads in which only the testis was functional (male‐phase), whereas the female‐role individuals had two types of gonads: only the ovary was functional (female‐phase) or both testis and ovary were functional (simultaneously hermaphroditic phase, SH‐phase). In addition, single‐rearing experiments showed SH‐phase gonads in all individuals, and some cyclic spawning but no self‐fertilization occurred. These results revealed that L. exiguus has an unusual sexual pattern among hermaphroditic fishes because they undergo bidirectional sex change and some maintain SH‐phase gonads. These findings indicate that the low‐density distribution and low mobility of L. exiguus in their natural habitat may have influenced the evolution of this unique sexual pattern.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>36856167</pmid><doi>10.1111/jfb.15363</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0003-2854-3202</orcidid><orcidid>https://orcid.org/0000-0001-7137-3726</orcidid><orcidid>https://orcid.org/0000-0002-9602-1601</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals bidirectional sex change Biological fertilization Density Density distribution Disorders of Sex Development Distribution Female Females Fertilization Fish Fishes Gonads Hermaphroditic Organisms Hermaphroditism low‐density distribution Lubricogobius exiguus Male Males Marine fishes Mating Mobility Ovaries Ovary Plastic properties Plasticity Reproductive behaviour Self-fertilization Sex Sex Determination Processes sexual plasticity simultaneous hermaphrodite Spawning Testes Testis |
title | Bidirectional sex change and plasticity of gonadal phases in the goby Lubricogobius exiguus |
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