Nejvíce citovaný článek - PubMed ID 31028711
Sex Chromosome Turnover in Moths of the Diverse Superfamily Gelechioidea
Sex chromosomes can expand through fusion with autosomes, thereby acquiring unique evolutionary patterns. In butterflies and moths (Lepidoptera), these sex chromosome-autosome (SA) fusions occur relatively frequently, suggesting possible evolutionary advantages. Here, we investigated how SA fusion affects chromosome features and molecular evolution in leafroller moths (Lepidoptera: Tortricidae). Phylogenomic analysis showed that Tortricidae diverged ∼124 million years ago, accompanied by an SA fusion between the Merian elements M(20 + 17) and MZ. In contrast to partial autosomal fusions, the fused neo-Z Chromosome developed a hierarchical architecture, in which the three elements exhibit heterogeneous sequence features and evolutionary patterns. Specifically, the M17 part had a distinct base composition and chromatin domains. Unlike M20 and MZ, M17 was expressed at the same levels as autosomes in both sexes, compensating for the lost gene dosage in females. Concurrently, the SA fusion drove M17 as an evolutionary hotspot, accelerating the evolution of several genes related to ecological adaptation (e.g., ABCCs) and facilitating the divergence of closely related species, whereas the undercompensated M20 did not show such an effect. Thus, accelerated evolution under a novel pattern of dosage compensation may have favored the adaptive radiation of this group. This study demonstrates the association between a karyotype variant and adaptive evolution and explains the recurrent SA fusion in the Lepidoptera.
- MeSH
- chromozomy hmyzu genetika MeSH
- fylogeneze * MeSH
- fyziologická adaptace genetika MeSH
- molekulární evoluce * MeSH
- můry * genetika klasifikace MeSH
- pohlavní chromozomy * genetika MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Sex chromosomes play an outsized role in adaptation and speciation, and thus deserve particular attention in evolutionary genomics. In particular, fusions between sex chromosomes and autosomes can produce neo-sex chromosomes, which offer important insights into the evolutionary dynamics of sex chromosomes. Here, we investigate the evolutionary origin of the previously reported Danaus neo-sex chromosome within the tribe Danaini. We assembled and annotated genomes of Tirumala septentrionis (subtribe Danaina), Ideopsis similis (Amaurina), Idea leuconoe (Euploeina) and Lycorea halia (Itunina) and identified their Z-linked scaffolds. We found that the Danaus neo-sex chromosome resulting from the fusion between a Z chromosome and an autosome corresponding to the Melitaea cinxia chromosome (McChr) 21 arose in a common ancestor of Danaina, Amaurina and Euploina. We also identified two additional fusions as the W chromosome further fused with the synteny block McChr31 in I. similis and independent fusion occurred between ancestral Z chromosome and McChr12 in L. halia. We further tested a possible role of sexually antagonistic selection in sex chromosome turnover by analysing the genomic distribution of sex-biased genes in I. leuconoe and L. halia. The autosomes corresponding to McChr21 and McChr31 involved in the fusions are significantly enriched in female- and male-biased genes, respectively, which could have hypothetically facilitated fixation of the neo-sex chromosomes. This suggests a role of sexual antagonism in sex chromosome turnover in Lepidoptera. The neo-Z chromosomes of both I. leuconoe and L. halia appear fully compensated in somatic tissues, but the extent of dosage compensation for the ancestral Z varies across tissues and species.
- Klíčová slova
- butterflies, dosage compensation, fusions, sex chromosomes, sexual antagonism, sex‐biased genes,
- MeSH
- fylogeneze MeSH
- molekulární evoluce MeSH
- motýli * genetika MeSH
- pohlavní chromozomy * genetika MeSH
- syntenie MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
The Neotropical monophyletic catfish genus Harttia represents an excellent model to study karyotype and sex chromosome evolution in teleosts. Its species split into three phylogenetic clades distributed along the Brazilian territory and they differ widely in karyotype traits, including the presence of standard or multiple sex chromosome systems in some members. Here, we investigate the chromosomal rearrangements and associated synteny blocks involved in the origin of a multiple X1X2Y sex chromosome system present in three out of six sampled Amazonian-clade species. Using 5S and 18S ribosomal DNA fluorescence in situ hybridization and whole chromosome painting with probes corresponding to X1 and X2 chromosomes of X1X2Y system from H. punctata, we confirm previous assumptions that X1X2Y sex chromosome systems of H. punctata, H. duriventris and H. villasboas represent the same linkage groups which also form the putative XY sex chromosomes of H. rondoni. The shared homeology between X1X2Y sex chromosomes suggests they might have originated once in the common ancestor of these closely related species. A joint arrangement of mapped H. punctata X1 and X2 sex chromosomes in early diverging species of different Harttia clades suggests that the X1X2Y sex chromosome system may have formed through an X chromosome fission rather than previously proposed Y-autosome fusion.
- MeSH
- chromozom Y MeSH
- fylogeneze MeSH
- hybridizace in situ fluorescenční MeSH
- pohlavní chromozomy genetika MeSH
- sumci * genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Genes for major ribosomal RNAs (rDNA) are present in multiple copies mainly organized in tandem arrays. The number and position of rDNA loci can change dynamically and their repatterning is presumably driven by other repetitive sequences. We explored a peculiar rDNA organization in several representatives of Lepidoptera with either extremely large or numerous rDNA clusters. We combined molecular cytogenetics with analyses of second- and third-generation sequencing data to show that rDNA spreads as a transcription unit and reveal association between rDNA and various repeats. Furthermore, we performed comparative long read analyses among the species with derived rDNA distribution and moths with a single rDNA locus, which is considered ancestral. Our results suggest that satellite arrays, rather than mobile elements, facilitate homology-mediated spread of rDNA via either integration of extrachromosomal rDNA circles or ectopic recombination. The latter arguably better explains preferential spread of rDNA into terminal regions of lepidopteran chromosomes as efficiency of ectopic recombination depends on the proximity of homologous sequences to telomeres.
- Klíčová slova
- Lepidoptera, major ribosomal RNA genes, mobile elements, satellite,
- MeSH
- chromozomy MeSH
- můry * genetika MeSH
- repetitivní sekvence nukleových kyselin * MeSH
- ribozomální DNA genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- ribozomální DNA MeSH
Moths of the family Crambidae include a number of pests that cause economic losses to agricultural crops. Despite their economic importance, little is known about their genome architecture and chromosome evolution. Here, we characterized the chromosomes and repetitive DNA of the sugarcane borer Diatraea saccharalis using a combination of low-pass genome sequencing, bioinformatics, and cytogenetic methods, focusing on the sex chromosomes. Diploid chromosome numbers differed between the sexes, i.e., 2n = 33 in females and 2n = 34 in males. This difference was caused by the occurrence of a WZ1Z2 trivalent in female meiosis, indicating a multiple sex-chromosome system WZ1Z2/Z1Z1Z2Z2. A strong interstitial telomeric signal was observed on the W chromosome, indicating a fusion of the ancestral W chromosome with an autosome. Among repetitive DNAs, transposable elements (TEs) accounted for 39.18% (males) to 41.35% (females), while satDNAs accounted for only 0.214% (males) and 0.215% (females) of the genome. FISH mapping revealed different chromosomal organization of satDNAs, such as single localized clusters, spread repeats, and non-clustered repeats. Two TEs mapped by FISH were scattered. Although we found a slight enrichment of some satDNAs in the female genome, they were not differentially enriched on the W chromosome. However, we found enriched FISH signals for TEs on the W chromosome, suggesting their involvement in W chromosome degeneration and differentiation. These data shed light on karyotype and repetitive DNA dynamics due to multiple chromosome fusions in D. saccharalis, contribute to the understanding of genome structure in Lepidoptera and are important for future genomic studies.
- Klíčová slova
- Chromosome fusion, FISH, Holocentric chromosome, Multiple sex chromosomes, W chromatin, satDNA,
- MeSH
- karyotyp MeSH
- molekulární evoluce MeSH
- můry * genetika MeSH
- pohlavní chromozomy genetika MeSH
- Saccharum * genetika MeSH
- transpozibilní elementy DNA MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- transpozibilní elementy DNA MeSH
Despite decades of cytogenetic and genomic research of dynamic sex chromosome evolution in teleost fishes, multiple sex chromosomes have been largely neglected. In this review, we compiled available data on teleost multiple sex chromosomes, identified major trends in their evolution and suggest further trajectories in their investigation. In a compiled dataset of 440 verified records of fish sex chromosomes, we counted 75 multiple sex chromosome systems with 60 estimated independent origins. We showed that male-heterogametic systems created by Y-autosome fusion predominate and that multiple sex chromosomes are over-represented in the order Perciformes. We documented a striking difference in patterns of differentiation of sex chromosomes between male and female heterogamety and hypothesize that faster W sex chromosome differentiation may constrain sex chromosome turnover in female-heterogametic systems. We also found no significant association between the mechanism of multiple sex chromosome formation and percentage of uni-armed chromosomes in teleost karyotypes. Last but not least, we hypothesized that interaction between fish populations, which differ in their sex chromosomes, can drive the evolution of multiple sex chromosomes in fishes. This underlines the importance of broader inter-population sampling in studies of fish sex chromosomes. This article is part of the theme issue 'Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)'.
- Klíčová slova
- chromosome rearrangements, fish, repetitive DNA accumulation, sex chromosome differentiation, sex chromosome turnover,
- MeSH
- biologická evoluce * MeSH
- cytogenetika MeSH
- pohlavní chromozomy genetika MeSH
- ryby genetika MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
Sex chromatin is a conspicuous body that occurs in polyploid nuclei of most lepidopteran females and consists of numerous copies of the W sex chromosome. It is also a cytogenetic tool used to rapidly assess the W chromosome presence in Lepidoptera. However, certain chromosomal features could disrupt the formation of sex chromatin and lead to the false conclusion that the W chromosome is absent in the respective species. Here we tested the sex chromatin presence in 50 species of Geometridae. In eight selected species with either missing, atypical, or normal sex chromatin patterns, we performed a detailed karyotype analysis by means of comparative genomic hybridization (CGH) and fluorescence in situ hybridization (FISH). The results showed a high diversity of W chromosomes and clarified the reasons for atypical sex chromatin, including the absence or poor differentiation of W, rearrangements leading to the neo-W emergence, possible association with the nucleolus, and the existence of multiple W chromosomes. In two species, we detected intraspecific variability in the sex chromatin status and sex chromosome constitution. We show that the sex chromatin is not a sufficient marker of the W chromosome presence, but it may be an excellent tool to pinpoint species with atypical sex chromosomes.
- Klíčová slova
- Geometridae, Lepidoptera, W chromosome, comparative genomic hybridization, intraspecific chromosomal variability, neo-sex chromosomes, sex chromatin, sex chromosome evolution,
- MeSH
- druhová specificita MeSH
- hybridizace in situ fluorescenční MeSH
- karyotyp MeSH
- můry genetika MeSH
- pohlavní chromozomy genetika MeSH
- sexchromatin metabolismus MeSH
- srovnávací genomová hybridizace MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Fluorescence in situ hybridization (FISH) allows identification of particular chromosomes and their rearrangements. Using FISH with signal enhancement via antibody amplification and enzymatically catalysed reporter deposition, we evaluated applicability of universal cytogenetic markers, namely 18S and 5S rDNA genes, U1 and U2 snRNA genes, and histone H3 genes, in the study of the karyotype evolution in moths and butterflies. Major rDNA underwent rather erratic evolution, which does not always reflect chromosomal changes. In contrast, the hybridization pattern of histone H3 genes was well conserved, reflecting the stable organisation of lepidopteran genomes. Unlike 5S rDNA and U1 and U2 snRNA genes which we failed to detect, except for 5S rDNA in a few representatives of early diverging lepidopteran lineages. To explain the negative FISH results, we used quantitative PCR and Southern hybridization to estimate the copy number and organization of the studied genes in selected species. The results suggested that their detection was hampered by long spacers between the genes and/or their scattered distribution. Our results question homology of 5S rDNA and U1 and U2 snRNA loci in comparative studies. We recommend the use of histone H3 in studies of karyotype evolution.
- MeSH
- cytogenetické vyšetření metody MeSH
- genom MeSH
- hybridizace in situ fluorescenční MeSH
- mapování chromozomů MeSH
- molekulární evoluce * MeSH
- motýli genetika MeSH
- můry genetika MeSH
- ribozomální DNA genetika MeSH
- RNA malá jaderná genetika MeSH
- RNA ribozomální 18S genetika MeSH
- RNA ribozomální 5S genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- ribozomální DNA MeSH
- RNA malá jaderná MeSH
- RNA ribozomální 18S MeSH
- RNA ribozomální 5S MeSH
- U2 small nuclear RNA MeSH Prohlížeč
Nesidiocoris tenuis (Reuter) is an efficient predatory biological control agent used throughout the Mediterranean Basin in tomato crops but regarded as a pest in northern European countries. From the family Miridae, it is an economically important insect yet very little is known in terms of genetic information and no genomic or transcriptomic studies have been published. Here, we use a linked-read sequencing strategy on a single female N. tenuis. From this, we assembled the 355 Mbp genome and delivered an ab initio, homology-based and evidence-based annotation. Along the way, the bacterial "contamination" was removed from the assembly. In addition, bacterial lateral gene transfer (LGT) candidates were detected in the N. tenuis genome. The complete gene set is composed of 24 688 genes; the associated proteins were compared to other hemipterans (Cimex lectularis, Halyomorpha halys and Acyrthosiphon pisum). We visualized the genome using various cytogenetic techniques, such as karyotyping, CGH and GISH, indicating a karyotype of 2n = 32. Additional analyses include the localization of 18S rDNA and unique satellite probes as well as pooled sequencing to assess nucleotide diversity and neutrality of the commercial population. This is one of the first mirid genomes to be released and the first of a mirid biological control agent.
- Klíčová slova
- Hemiptera, biocontrol, linked-read,
- MeSH
- Bacteria genetika MeSH
- biologická ochrana MeSH
- genom hmyzu MeSH
- Heteroptera genetika mikrobiologie MeSH
- přenos genů horizontální MeSH
- symbióza MeSH
- zvířata MeSH
- Check Tag
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- biologická ochrana MeSH
Sex-chromosome systems tend to be highly conserved and knowledge about their evolution typically comes from macroevolutionary inference. Rapidly evolving complex sex-chromosome systems represent a rare opportunity to study the mechanisms of sex-chromosome evolution at unprecedented resolution. Three cryptic species of wood-white butterflies-Leptidea juvernica, L. sinapis and L. reali-have each a unique set of multiple sex-chromosomes with 3-4 W and 3-4 Z chromosomes. Using a transcriptome-based microarray for comparative genomic hybridisation (CGH) and a library of bacterial artificial chromosome (BAC) clones, both developed in L. juvernica, we identified Z-linked Leptidea orthologs of Bombyx mori genes and mapped them by fluorescence in situ hybridisation (FISH) with BAC probes on multiple Z chromosomes. In all three species, we determined synteny blocks of autosomal origin and reconstructed the evolution of multiple sex-chromosomes. In addition, we identified W homologues of Z-linked orthologs and characterised their molecular differentiation. Our results suggest that the multiple sex-chromosome system evolved in a common ancestor as a result of dynamic genome reshuffling through repeated rearrangements between the sex chromosomes and autosomes, including translocations, fusions and fissions. Thus, the initial formation of neo-sex chromosomes could not have played a role in reproductive isolation between these Leptidea species. However, the subsequent species-specific fissions of several neo-sex chromosomes could have contributed to their reproductive isolation. Then, significantly increased numbers of Z-linked genes and independent neo-W chromosome degeneration could accelerate the accumulation of genetic incompatibilities between populations and promote their divergence resulting in speciation.
- MeSH
- molekulární evoluce * MeSH
- motýli * genetika MeSH
- pohlavní chromozomy * MeSH
- syntenie * MeSH
- zvířata MeSH
- Check Tag
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH