Gene-rich germline-restricted chromosomes in black-winged fungus gnats evolved through hybridization

PLoS Biology, Journal Year: 2022, Volume and Issue: 20(2), P. e3001559 - e3001559

Published: Feb. 25, 2022

Germline-restricted DNA has evolved in diverse animal taxa and is found several vertebrate clades, nematodes, flies. In these lineages, either portions of chromosomes or entire are eliminated from somatic cells early development, restricting the genome to germline. Little known about why germline-restricted evolved, especially flies, which 3 families, Chironomidae, Cecidomyiidae, Sciaridae, carry (GRCs). We conducted a genomic analysis GRCs fungus gnat Bradysia ( Sciara ) coprophila (Diptera: Sciaridae), 2 large “L” chromosomes. sequenced assembled B . used differences sequence coverage k-mer frequency between germline tissues identify GRC compare it other genome. that large, gene rich, have many genes with divergent homologs on also exist population we sequenced. more similar another Dipteran family (Cecidomyiidae) than homologous Sciaridae. This unexpected finding suggests likely arose Sciaridae through hybridization related lineage. These results provide foundation answer questions evolution such as how this event resulted what features cause them be restricted

Language: Английский

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Evolutionary Perspectives on Germline-Restricted Chromosomes in Flies (Diptera)

Genome Biology and Evolution, Journal Year: 2021, Volume and Issue: 13(6)

Published: April 12, 2021

In some eukaryotes, germline soma differentiation involves elimination of parts the genome from somatic cells. The portions restricted to often contain genes that play a role in development and function germline. Lineages with germline-restricted DNA are taxonomically diverse, size varies substantially. Unfortunately, few these lineages have been studied detail. As result, we understand little about general evolutionary forces drive origin maintenance DNA. One taxonomic groups where has poorly flies (Diptera). three Dipteran families, Chironomidae, Cecidomyiidae, Sciaridae, entire chromosomes eliminated cells early embryonic development. Germline-restricted thought evolved independently families their size, number, transmission patterns vary between families. Although there is wealth cytological studies on flies, almost no genomic undertaken. very known how why they what encode. This review summarizes literature Diptera, discusses hypotheses for function, compares Diptera other eukaryotes. Finally, discuss represent promising system study propose future avenues research this topic.

Language: Английский

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Rapid gene content turnover on the germline-restricted chromosome in songbirds

Nature Communications, Journal Year: 2023, Volume and Issue: 14(1)

Published: July 29, 2023

The germline-restricted chromosome (GRC) of songbirds represents a taxonomically widespread example programmed DNA elimination. Despite its apparent indispensability, we still know very little about the GRC's genetic composition, function, and evolutionary significance. Here assemble GRC in two closely related species, common thrush nightingale. In total identify 192 genes across GRCs, with many them present multiple copies. Interestingly, appears to be under selective pressure, content differing dramatically between species appearing pseudogenized fragments. Only one gene, cpeb1, has complete coding region all examined individuals shows no copy number variation. acquisition this gene by corresponds earliest estimates origin, making it good candidate for functional indispensability songbirds.

Language: Английский

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The genetic architecture of recombination rates is polygenic and differs between the sexes in wild house sparrows (Passer domesticus)

Molecular Biology and Evolution, Journal Year: 2024, Volume and Issue: 41(9)

Published: Aug. 24, 2024

Abstract Meiotic recombination through chromosomal crossing-over is a fundamental feature of sex and an important driver genomic diversity. It ensures proper disjunction, allows increased selection responses, prevents mutation accumulation; however, it also mutagenic can break up favorable haplotypes. This cost–benefit dynamic likely to vary depending on mechanistic evolutionary contexts, indeed, rates show huge variation in nature. Identifying the genetic architecture this key understanding its causes consequences. Here, we investigate individual rate wild house sparrows (Passer domesticus). We integrate pedigree data identify autosomal crossover counts (ACCs) intrachromosomal allelic shuffling (r¯intra) 13,056 gametes transmitted from 2,653 individuals their offspring. Females had 1.37 times higher ACC, 1.55 r¯intra than males. ACC were heritable females males (ACC h2 = 0.23 0.11; 0.12 0.14), but cross-sex additive correlations low (rA 0.29 0.32 for r¯intra). Conditional bivariate analyses showed that all measures remained after accounting values opposite sex, indicating sex-specific evolve somewhat independently. Genome-wide models are polygenic driven by many small-effect loci, which act trans as global modifiers. Our findings have different potential birds, providing compelling mechanism evolution sexual dimorphism recombination.

Language: Английский

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Occasional paternal inheritance of the germline-restricted chromosome in songbirds

Proceedings of the National Academy of Sciences, Journal Year: 2022, Volume and Issue: 119(4)

Published: Jan. 20, 2022

Significance Most if not all songbirds possess a germline-restricted chromosome (GRC) which is believed to be exclusively maternally inherited. However, we show that, in the zebra finch, GRC can also paternally inherited and that potential for paternal inheritance may differ between families. We further genetic diversity of extremely reduced compared high mitochondrial DNA lineages, suggesting single haplotype has spread through Australian finch population relatively recently via occasional inheritance. Our study therefore suggests evolve selfish manner, could result intragenomic conflict.

Language: Английский

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Mendelian nightmares: the germline-restricted chromosome of songbirds

Chromosome Research, Journal Year: 2022, Volume and Issue: 30(2-3), P. 255 - 272

Published: April 13, 2022

Abstract Germline-restricted chromosomes (GRCs) are accessory that occur only in germ cells. They eliminated from somatic cells through programmed DNA elimination during embryo development. GRCs have been observed several unrelated animal taxa and show peculiar modes of non-Mendelian inheritance within-individual elimination. Recent cytogenetic phylogenomic evidence suggests a GRC is present across the species-rich songbirds, but absent non-passerine birds, implying over half all 10,500 bird species extensive germline/soma genome differences. Here, we review recent insights gained genomic, transcriptomic, approaches with regard to genetic content, phylogenetic distribution, songbird GRC. While many questions remain unsolved terms inheritance, elimination, function, discuss plausible scenarios future directions for understanding this widespread form

Language: Английский

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Asymmetric Inheritance: The Diversity and Evolution of Non-Mendelian Reproductive Strategies

Annual Review of Ecology Evolution and Systematics, Journal Year: 2022, Volume and Issue: 53(1), P. 1 - 23

Published: July 29, 2022

The ability to reproduce is the key trait that distinguishes living organisms from inorganic matter, and strategies used achieve successful reproduction are almost as diverse themselves. In animals, most widespread form of involves separate male female sexes: Each sex produces haploid gametes via meiosis, two fuse a new diploid organism. some cases, both parents contribute equally nuclear cytoplasmic genomes their offspring. However, such fully symmetric represents extreme end continuum toward complete asymmetry, where offspring inherit only one parents. Asymmetries also occur with respect fate maternally paternally inherited which affected by non-Mendelian inheritance. this review, we describe diversity animal reproductive systems along different axes symmetry–asymmetry suggest evolutionary routes may have led increased levels asymmetry.

Language: Английский

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Heat shock factor 5 establishes the male germ-line meiotic sex chromosome inactivation through regulation of Smarca4

Heliyon, Journal Year: 2023, Volume and Issue: 9(5), P. e15194 - e15194

Published: April 22, 2023

Meiotic sex chromosome inactivation is an essential event in male germ cell development, which directed by DNA damage response signaling independent of Xist RNA to silence the transcription activity chromosomes. However, specific mechanism establishment and maintenance meiotic silencing still unclear. Here we identify HSF5 as a testicular protein expression was at onset meiosis pachytene stage round sperm. When function lost, remodeling fail, followed activation CHK2 checkpoint leads apoptosis. Furthermore, found that SMARCA4 linking MSCI uncover additional factors with remodeling. Together, our results demonstrate requirement for spermatogenesis suggest role mammalian HSF5-SMARCA4 programmed events take place during meiosis.

Language: Английский

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Micro Germline-Restricted Chromosome in Blue Tits: Evidence for Meiotic Functions

Molecular Biology and Evolution, Journal Year: 2023, Volume and Issue: 40(5)

Published: April 28, 2023

Abstract The germline-restricted chromosome (GRC) is likely present in all songbird species but differs widely size and gene content. This extra has been described as either a microchromosome with only limited basic content or macrochromosome enriched functions related to female gonad embryo development. Here, we assembled, annotated, characterized the first micro-GRC blue tit (Cyanistes caeruleus) using high-fidelity long-read sequencing data. Although some genes on GRC show signals of pseudogenization, others potentially have important functions, currently past. We highlight paralog BMP15, which among highest expressed both tits zebra finches (Taeniopygia guttata) known play role oocyte follicular maturation other vertebrates. are further for synaptonemal complex. found similar functional enrichment when analyzing published data from two nightingale (Luscinia spp.). hypothesize that these maintaining standard maternal inheritance recombining paternal GRCs during potential episodes biparental inheritance.

Language: Английский

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The genetic architecture of recombination rates is polygenic and differs between the sexes in wild house sparrows (Passer domesticus)

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: Jan. 27, 2023

Abstract Meiotic recombination through chromosomal crossing-over is a fundamental feature of sex and an important driver genomic diversity. It ensures proper disjunction, allows increased selection responses, prevents mutation accumulation; however, it also mutagenic can break up favourable haplotypes. This cost/benefit dynamic likely to vary depending on mechanistic evolutionary contexts, indeed, rates show huge variation in nature. Identifying the genetic architecture this key understanding its causes consequences. Here, we investigate individual rate wild house sparrows ( Passer domesticus ). We integrate pedigree data identify autosomal crossover counts (ACC) intra-chromosomal allelic shuffling r̅ intra ) 13,056 gametes. Females had 1.37 times higher ACC, 1.55 than males. ACC were heritable females males (ACC h 2 = 0.23 0.11; 0.12 0.14), but cross-sex additive correlations low (r A 0.29 0.32 for Conditional bivariate analyses showed that all measures remained after accounting values opposite sex, indicating sex-specific evolve somewhat independently. Genome-wide models are polygenic driven by many small-effect loci, which act trans as global modifiers. Our findings have different potential birds, providing compelling mechanism evolution sexual dimorphism recombination.

Language: Английский

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