Orthopteran Neo-Sex Chromosomes Reveal Dynamics of Recombination Suppression and Evolution of Supergenes.

IF 4.5 1区 生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY Molecular Ecology Pub Date : 2024-10-30 DOI:10.1111/mec.17567
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
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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.

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直翅目新性腺染色体揭示了重组抑制和超级基因进化的动态。
一个多世纪以来,性染色体的早期进化一直模糊不清。摩拉宾蚱蜢的 Vandiemenella viatica 物种群非常适合研究性染色体分化和 Y 染色体退化的早期阶段。这是因为新XY性染色体是通过X-常染色体与不同的常染色体融合而独立进化多次的。在这里,我们生成了代表具有和不具有新性染色体核型的两个染色体种族(P24XY 和 P24X0)的新染色体组,以及具有不同新 XY 染色体系统的第三个染色体种族(P25XY)的序列数据。有趣的是,这两个新 XY 染色体种族是由不同的 X 自体融合(分别涉及 chr1 和 chrB)形成的,而且我们发现这两个新 Y 染色体都部分停止了与新 X 染色体的重组。我们发现,新 XY 染色体通过 SNPs 和结构突变的积累而发生了分化,许多新 Y 连锁基因在重组停止后发生了退化。然而,新-Y 染色体的非重组区域除了与精子发生、生育和繁殖相关的基因外,还含有对性别决定至关重要的未退化基因,如性致死基因和转化基因,这说明了它们作为男性化超级基因的整合作用。与预期相反,与其他基因组区域相比,新Y染色体上转座元件(TE)的密度(略低)。这项研究揭示了年轻性染色体的独特动态,即重组抑制的进化和(某些)新性染色体基因的明显衰变,并提供了一个令人信服的案例,说明染色体融合和融合后突变过程如何促进超级基因的进化。
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来源期刊
Molecular Ecology
Molecular Ecology 生物-进化生物学
CiteScore
8.40
自引率
10.20%
发文量
472
审稿时长
1 months
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
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