Suvratha Jayaprasad, Valentina Peona, Simon J Ellerstrand, Roberto Rossini, Ignas Bunikis, Olga V Pettersson, Remi-André Olsen, Carl-Johan Rubin, Elisabet Einarsdottir, Franziska Bonath, Tessa M Bradford, Steven J B Cooper, Bengt Hansson, Alexander Suh, Takeshi Kawakami, Holger Schielzeth, Octavio M Palacios-Gimenez
{"title":"Orthopteran Neo-Sex Chromosomes Reveal Dynamics of Recombination Suppression and Evolution of Supergenes.","authors":"Suvratha Jayaprasad, Valentina Peona, Simon J Ellerstrand, Roberto Rossini, Ignas Bunikis, Olga V Pettersson, Remi-André Olsen, Carl-Johan Rubin, Elisabet Einarsdottir, Franziska Bonath, Tessa M Bradford, Steven J B Cooper, Bengt Hansson, Alexander Suh, Takeshi Kawakami, Holger Schielzeth, Octavio M Palacios-Gimenez","doi":"10.1111/mec.17567","DOIUrl":null,"url":null,"abstract":"<p><p>The early evolution of sex chromosomes has remained obscure for more than a century. The Vandiemenella viatica species group of morabine grasshoppers is highly suited for studying the early stages of sex chromosome divergence and degeneration of the Y chromosome. This stems from the fact that neo-XY sex chromosomes have independently evolved multiple times by X-autosome fusions with different autosomes. Here, we generated new chromosome-level assemblies for two chromosomal races representing karyotypes with and without neo-sex chromosomes (P24XY and P24X0), and sequence data of a third chromosomal race with a different neo-XY chromosome system (P25XY). Interestingly, these two neo-XY chromosomal races are formed by different X-autosome fusions (involving chr1 and chrB, respectively), and we found that both neo-Y chromosomes have partly ceased to recombine with their neo-X counterpart. We show that the neo-XY chromosomes have diverged through accumulation of SNPs and structural mutations, and that many neo-Y-linked genes have degenerated since recombination ceased. However, the non-recombining regions of neo-Y chromosomes host non-degenerated genes crucial for sex determination, such as sex-lethal and transformer, alongside genes associated with spermatogenesis, fertility, and reproduction, illustrating their integrative role as a masculinizing supergene. Contrary to expectations, the neo-Y chromosomes showed (slightly) lower density of transposable elements (TEs) compared to other genomic regions. The study reveals the unique dynamics of young sex chromosomes, with evolution of recombination suppression and pronounced decay of (some) neo-sex chromosome genes, and provides a compelling case illustrating how chromosomal fusions and post-fusion mutational processes contribute to the evolution of supergenes.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":null,"pages":null},"PeriodicalIF":4.5000,"publicationDate":"2024-10-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Molecular Ecology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1111/mec.17567","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
The early evolution of sex chromosomes has remained obscure for more than a century. The Vandiemenella viatica species group of morabine grasshoppers is highly suited for studying the early stages of sex chromosome divergence and degeneration of the Y chromosome. This stems from the fact that neo-XY sex chromosomes have independently evolved multiple times by X-autosome fusions with different autosomes. Here, we generated new chromosome-level assemblies for two chromosomal races representing karyotypes with and without neo-sex chromosomes (P24XY and P24X0), and sequence data of a third chromosomal race with a different neo-XY chromosome system (P25XY). Interestingly, these two neo-XY chromosomal races are formed by different X-autosome fusions (involving chr1 and chrB, respectively), and we found that both neo-Y chromosomes have partly ceased to recombine with their neo-X counterpart. We show that the neo-XY chromosomes have diverged through accumulation of SNPs and structural mutations, and that many neo-Y-linked genes have degenerated since recombination ceased. However, the non-recombining regions of neo-Y chromosomes host non-degenerated genes crucial for sex determination, such as sex-lethal and transformer, alongside genes associated with spermatogenesis, fertility, and reproduction, illustrating their integrative role as a masculinizing supergene. Contrary to expectations, the neo-Y chromosomes showed (slightly) lower density of transposable elements (TEs) compared to other genomic regions. The study reveals the unique dynamics of young sex chromosomes, with evolution of recombination suppression and pronounced decay of (some) neo-sex chromosome genes, and provides a compelling case illustrating how chromosomal fusions and post-fusion mutational processes contribute to the evolution of supergenes.
期刊介绍:
Molecular Ecology publishes papers that utilize molecular genetic techniques to address consequential questions in ecology, evolution, behaviour and conservation. Studies may employ neutral markers for inference about ecological and evolutionary processes or examine ecologically important genes and their products directly. We discourage papers that are primarily descriptive and are relevant only to the taxon being studied. Papers reporting on molecular marker development, molecular diagnostics, barcoding, or DNA taxonomy, or technical methods should be re-directed to our sister journal, Molecular Ecology Resources. Likewise, papers with a strongly applied focus should be submitted to Evolutionary Applications. Research areas of interest to Molecular Ecology include:
* population structure and phylogeography
* reproductive strategies
* relatedness and kin selection
* sex allocation
* population genetic theory
* analytical methods development
* conservation genetics
* speciation genetics
* microbial biodiversity
* evolutionary dynamics of QTLs
* ecological interactions
* molecular adaptation and environmental genomics
* impact of genetically modified organisms