Dynamic co-evolution of transposable elements and the piRNA pathway in African cichlid fishes
East African cichlid fishes have diversified in an explosive fashion, but the (epi)genetic basis of the phenotypic diversity of these fishes remains largely unknown. Although transposable elements (TEs) have been associated with phenotypic variation in cichlids, little is known about their transcrip...
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creator | Almeida, Miguel Vasconcelos Blumer, Moritz Yuan, Chengwei Ulrika Sierra, Pío Price, Jonathan L Quah, Fu Xiang Friman, Aleksandr Dallaire, Alexandra Vernaz, Grégoire Putman, Audrey L K Smith, Alan M Joyce, Domino A Butter, Falk Haase, Astrid D Durbin, Richard Santos, M Emília Miska, Eric A |
description | East African cichlid fishes have diversified in an explosive fashion, but the (epi)genetic basis of the phenotypic diversity of these fishes remains largely unknown. Although transposable elements (TEs) have been associated with phenotypic variation in cichlids, little is known about their transcriptional activity and epigenetic silencing. We set out to bridge this gap and to understand the interactions between TEs and their cichlid hosts.
Here, we describe dynamic patterns of TE expression in African cichlid gonads and during early development. Orthology inference revealed strong conservation of TE silencing factors in cichlids, and an expansion of piwil1 genes in Lake Malawi cichlids, likely driven by PiggyBac TEs. The expanded piwil1 copies have signatures of positive selection and retain amino acid residues essential for catalytic activity. Furthermore, the gonads of African cichlids express a Piwi-interacting RNA (piRNA) pathway that targets TEs. We define the genomic sites of piRNA production in African cichlids and find divergence in closely related species, in line with fast evolution of piRNA-producing loci.
Our findings suggest dynamic co-evolution of TEs and host silencing pathways in the African cichlid radiations. We propose that this co-evolution has contributed to cichlid genomic diversity. |
doi_str_mv | 10.1186/s13059-025-03475-z |
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Here, we describe dynamic patterns of TE expression in African cichlid gonads and during early development. Orthology inference revealed strong conservation of TE silencing factors in cichlids, and an expansion of piwil1 genes in Lake Malawi cichlids, likely driven by PiggyBac TEs. The expanded piwil1 copies have signatures of positive selection and retain amino acid residues essential for catalytic activity. Furthermore, the gonads of African cichlids express a Piwi-interacting RNA (piRNA) pathway that targets TEs. We define the genomic sites of piRNA production in African cichlids and find divergence in closely related species, in line with fast evolution of piRNA-producing loci.
Our findings suggest dynamic co-evolution of TEs and host silencing pathways in the African cichlid radiations. We propose that this co-evolution has contributed to cichlid genomic diversity.</description><identifier>ISSN: 1474-760X</identifier><identifier>ISSN: 1474-7596</identifier><identifier>EISSN: 1474-760X</identifier><identifier>DOI: 10.1186/s13059-025-03475-z</identifier><identifier>PMID: 39844208</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Animals ; Cichlidae ; Cichlids - genetics ; DNA Transposable Elements ; Epigenetic inheritance ; Evolution, Molecular ; Fishes ; Genes ; Genetic aspects ; Genetic research ; Gonads - metabolism ; Molecular evolution ; Natural history ; Phylogeny ; Physiological aspects ; Piwi-Interacting RNA ; RNA ; RNA processing ; RNA, Small Interfering - genetics ; RNA, Small Interfering - metabolism ; Transposons</subject><ispartof>Genome Biology, 2025-01, Vol.26 (1), p.14-37, Article 14</ispartof><rights>2025. The Author(s).</rights><rights>COPYRIGHT 2025 BioMed Central Ltd.</rights><rights>The Author(s) 2025 2025</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c441t-a8792ca6eb4a72382f4800a27c3258ac8ea4f6db33967d89c51be72e761a93993</cites><orcidid>0000-0002-4816-3111</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11753138/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11753138/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39844208$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Almeida, Miguel Vasconcelos</creatorcontrib><creatorcontrib>Blumer, Moritz</creatorcontrib><creatorcontrib>Yuan, Chengwei Ulrika</creatorcontrib><creatorcontrib>Sierra, Pío</creatorcontrib><creatorcontrib>Price, Jonathan L</creatorcontrib><creatorcontrib>Quah, Fu Xiang</creatorcontrib><creatorcontrib>Friman, Aleksandr</creatorcontrib><creatorcontrib>Dallaire, Alexandra</creatorcontrib><creatorcontrib>Vernaz, Grégoire</creatorcontrib><creatorcontrib>Putman, Audrey L K</creatorcontrib><creatorcontrib>Smith, Alan M</creatorcontrib><creatorcontrib>Joyce, Domino A</creatorcontrib><creatorcontrib>Butter, Falk</creatorcontrib><creatorcontrib>Haase, Astrid D</creatorcontrib><creatorcontrib>Durbin, Richard</creatorcontrib><creatorcontrib>Santos, M Emília</creatorcontrib><creatorcontrib>Miska, Eric A</creatorcontrib><title>Dynamic co-evolution of transposable elements and the piRNA pathway in African cichlid fishes</title><title>Genome Biology</title><addtitle>Genome Biol</addtitle><description>East African cichlid fishes have diversified in an explosive fashion, but the (epi)genetic basis of the phenotypic diversity of these fishes remains largely unknown. Although transposable elements (TEs) have been associated with phenotypic variation in cichlids, little is known about their transcriptional activity and epigenetic silencing. We set out to bridge this gap and to understand the interactions between TEs and their cichlid hosts.
Here, we describe dynamic patterns of TE expression in African cichlid gonads and during early development. Orthology inference revealed strong conservation of TE silencing factors in cichlids, and an expansion of piwil1 genes in Lake Malawi cichlids, likely driven by PiggyBac TEs. The expanded piwil1 copies have signatures of positive selection and retain amino acid residues essential for catalytic activity. Furthermore, the gonads of African cichlids express a Piwi-interacting RNA (piRNA) pathway that targets TEs. We define the genomic sites of piRNA production in African cichlids and find divergence in closely related species, in line with fast evolution of piRNA-producing loci.
Our findings suggest dynamic co-evolution of TEs and host silencing pathways in the African cichlid radiations. We propose that this co-evolution has contributed to cichlid genomic diversity.</description><subject>Animals</subject><subject>Cichlidae</subject><subject>Cichlids - genetics</subject><subject>DNA Transposable Elements</subject><subject>Epigenetic inheritance</subject><subject>Evolution, Molecular</subject><subject>Fishes</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genetic research</subject><subject>Gonads - metabolism</subject><subject>Molecular evolution</subject><subject>Natural history</subject><subject>Phylogeny</subject><subject>Physiological aspects</subject><subject>Piwi-Interacting RNA</subject><subject>RNA</subject><subject>RNA processing</subject><subject>RNA, Small Interfering - genetics</subject><subject>RNA, Small Interfering - metabolism</subject><subject>Transposons</subject><issn>1474-760X</issn><issn>1474-7596</issn><issn>1474-760X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2025</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>KPI</sourceid><sourceid>DOA</sourceid><recordid>eNpVkktvEzEUhUcIREvhD7BAXsJiit-PFYrKK6IChEBig6w7HjtxNbGH8aSQ_nrcplSNvLB1fe53feTTNM8JPiVEy9eFMCxMi6loMeNKtFcPmmPCFW-VxD8f3jsfNU9KucCYGE7l4-aIGc05xfq4-fV2l2ATHXK59Zd52M4xJ5QDmidIZcwFusEjP_iNT3NBkHo0rz0a47fPCzTCvP4DOxQTWoQpOkjIRbceYo9CLGtfnjaPAgzFP7vdT5of7999P_vYnn_5sDxbnLeOczK3oJWhDqTvOCjKNA1cYwxUOUaFBqc98CD7jjEjVa-NE6TzinolCRhmDDtplntun-HCjlPcwLSzGaK9KeRpZWGaoxu8lcQ4SrVjyikuvDZB6E7LOtxIEzqorDd71rjtNr531fcEwwH08CbFtV3lS0uIEowwXQkvbwlT_r31ZbabWJwfBkg-b4tlRGglmRGqSk_30hXUt8UUckW6unpfPyUnH2KtLzTlQktOrp2-Omiomtn_nVewLcV--ro81NK91k25lMmHOxME2-sE2X2CbE2QvUmQvapNL-7bv2v5Hxn2D-uWwZQ</recordid><startdate>20250122</startdate><enddate>20250122</enddate><creator>Almeida, Miguel Vasconcelos</creator><creator>Blumer, Moritz</creator><creator>Yuan, Chengwei Ulrika</creator><creator>Sierra, Pío</creator><creator>Price, Jonathan L</creator><creator>Quah, Fu Xiang</creator><creator>Friman, Aleksandr</creator><creator>Dallaire, Alexandra</creator><creator>Vernaz, Grégoire</creator><creator>Putman, Audrey L K</creator><creator>Smith, Alan M</creator><creator>Joyce, Domino A</creator><creator>Butter, Falk</creator><creator>Haase, Astrid D</creator><creator>Durbin, Richard</creator><creator>Santos, M Emília</creator><creator>Miska, Eric A</creator><general>BioMed Central Ltd</general><general>BioMed Central</general><general>BMC</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>KPI</scope><scope>IAO</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-4816-3111</orcidid></search><sort><creationdate>20250122</creationdate><title>Dynamic co-evolution of transposable elements and the piRNA pathway in African cichlid fishes</title><author>Almeida, Miguel Vasconcelos ; 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Although transposable elements (TEs) have been associated with phenotypic variation in cichlids, little is known about their transcriptional activity and epigenetic silencing. We set out to bridge this gap and to understand the interactions between TEs and their cichlid hosts.
Here, we describe dynamic patterns of TE expression in African cichlid gonads and during early development. Orthology inference revealed strong conservation of TE silencing factors in cichlids, and an expansion of piwil1 genes in Lake Malawi cichlids, likely driven by PiggyBac TEs. The expanded piwil1 copies have signatures of positive selection and retain amino acid residues essential for catalytic activity. Furthermore, the gonads of African cichlids express a Piwi-interacting RNA (piRNA) pathway that targets TEs. We define the genomic sites of piRNA production in African cichlids and find divergence in closely related species, in line with fast evolution of piRNA-producing loci.
Our findings suggest dynamic co-evolution of TEs and host silencing pathways in the African cichlid radiations. We propose that this co-evolution has contributed to cichlid genomic diversity.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>39844208</pmid><doi>10.1186/s13059-025-03475-z</doi><tpages>37</tpages><orcidid>https://orcid.org/0000-0002-4816-3111</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Cichlidae Cichlids - genetics DNA Transposable Elements Epigenetic inheritance Evolution, Molecular Fishes Genes Genetic aspects Genetic research Gonads - metabolism Molecular evolution Natural history Phylogeny Physiological aspects Piwi-Interacting RNA RNA RNA processing RNA, Small Interfering - genetics RNA, Small Interfering - metabolism Transposons |
title | Dynamic co-evolution of transposable elements and the piRNA pathway in African cichlid fishes |
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