Faster adaptation but slower divergence of X chromosomes under paternal genome elimination

. 2025 Jun 11 ; 16 (1) : 5288. [epub] 20250611

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid40500283
Odkazy

PubMed 40500283
PubMed Central PMC12159173
DOI 10.1038/s41467-025-60114-8
PII: 10.1038/s41467-025-60114-8
Knihovny.cz E-zdroje

Differences in transmission and ploidy between sex chromosomes and autosomes drive divergent evolutionary trajectories, with sex chromosomes generally evolving faster. Because sex-linked genes are transmitted less frequently, they are under less efficient selection. Conversely, exposure of recessive mutations on haploid sex chromosomes creates more efficient selection. In most systems, these effects occur simultaneously and are confounded. The fly families Sciaridae (fungus gnats) and Cecidomyiidae (gall midges) have X0 sex determination, but males transmit only maternally inherited chromosomes. This phenomenon results in equal transmission of the X and autosomes, allowing the effect of haploid selection to be studied in isolation. We discover that, unlike well-studied systems, X chromosomes diverge more slowly than autosomes in these flies. Using population genomic and expression data, we show that despite the X evolving more adaptively, stronger purifying selection explains slower divergence. Our findings demonstrate the utility of non-Mendelian inheritance systems for understanding fundamental evolutionary processes.

Zobrazit více v PubMed

Bachtrog, D. et al. Sex determination: Why so many ways of doing it?. PubMed DOI PMC

Charlesworth, D., Charlesworth, B. & Marais, G. Steps in the evolution of heteromorphic sex chromosomes. PubMed DOI

Meisel, R. P. & Connallon, T. The faster-X effect: integrating theory and data. PubMed DOI PMC

Ohta, T. The nearly neutral theory of molecular evolution. DOI

Ávila, V. et al. Faster-X Effects in two drosophila lineages. PubMed DOI PMC

Kousathanas, A., Halligan, D. L. & Keightley, P. D. Faster-X adaptive protein evolution in house mice. PubMed DOI PMC

Jaquiéry, J. et al. Disentangling the causes for faster-X evolution in aphids. PubMed DOI PMC

Bechsgaard, J. et al. Evidence for faster X chromosome evolution in spiders. PubMed DOI PMC

Hayes, K., Barton, H. J. & Zeng, K. A study of faster-Z evolution in the great tit (Parus major). PubMed DOI PMC

Mongue, A. J., Hansen, M. E. & Walters, J. R. Support for faster and more adaptive Z chromosome evolution in two divergent lepidopteran lineages*. PubMed DOI PMC

Chase, M. A., Vilcot, M. & Mugal, C. F. Evidence that genetic drift not adaptation drives fast-Z and large-Z effects in Ficedula flycatchers. PubMed PMC

Mongue, A. J. & Baird, R. B. Genetic drift drives faster-Z evolution in the salmon louse Lepeophtheirus salmonis. PubMed

Charlesworth, B., Coyne, J. A. & Barton, N. H. The relative rates of evolution of sex chromosomes and autosomes. DOI

Thornton, K., Bachtrog, D. & Andolfatto, P. X chromosomes and autosomes evolve at similar rates in Drosophila: no evidence for faster-X protein evolution. PubMed DOI PMC

Rousselle, M., Faivre, N., Ballenghien, M., Galtier, N. & Nabholz, B. Hemizygosity enhances purifying selection: lack of fast-Z evolution in two satyrine butterflies. PubMed DOI PMC

Pinharanda, A. et al. Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast-Z effect in Heliconius. PubMed DOI PMC

Mank, J. E., Nam, K. & Ellegren, H. Faster-Z evolution Is predominantly due to genetic drift. PubMed DOI

Charlesworth, B., Campos, J. L. & Jackson, B. C. Faster-X evolution: Theory and evidence from Drosophila. PubMed DOI

Herbette, M. & Ross, L. Paternal genome elimination: patterns and mechanisms of drive and silencing. PubMed DOI

Hitchcock, T. J., Baird, R. B., Gardner, A. & Ross, L. Paternal genome elimination, monogenic reproduction, and the evolutionary genetics of atypical sex chromosome systems. Preprint at 10.1101/2024.10.23.619029 (2024).

Vicoso, B. & Charlesworth, B. Effective population size and the faster-x effect: an extended model. PubMed DOI

Charlesworth, B. Patterns of age-specific means and genetic variances of mortality rates predicted by the mutation-accumulation theory of ageing. PubMed DOI

Pool, J. E. & Nielsen, R. Population size changes reshape genomic patterns of diversity. PubMed DOI PMC

Vicoso, B. & Charlesworth, B. Evolution on the X chromosome: unusual patterns and processes. PubMed DOI

Vicoso, B. & Charlesworth, B. Recombination rates may affect the ratio of X to autosomal noncoding polymorphism in African populations of Drosophila melanogaster. PubMed DOI PMC

Hutter, S., Li, H., Beisswanger, S., De Lorenzo, D. & Stephan, W. Distinctly different sex ratios in African and European populations of Drosophila melanogaster inferred from chromosomewide single nucleotide polymorphism data. PubMed DOI PMC

Garrigan, D., Kingan, S. B., Geneva, A. J., Vedanayagam, J. P. & Presgraves, D. C. Genome diversity and divergence in Drosophila mauritiana: multiple signatures of faster X evolution. PubMed DOI PMC

Kirkpatrick, M., Guerrero, R. F. & Scarpino, S. V. Patterns of neutral genetic variation on recombining sex chromosomes. PubMed DOI PMC

Sayres, M. A. W. Genetic diversity on the sex chromosomes. PubMed DOI PMC

Lasne, C., Sgrò, C. M. & Connallon, T. The relative contributions of the X chromosome and autosomes to local adaptation. PubMed DOI PMC

Baird, R. B., Mongue, A. J. & Ross, L. Why put all your eggs in one basket? Evolutionary perspectives on the origins of monogenic reproduction. PubMed DOI PMC

Benatti, T. R. et al. A neo-sex chromosome that drives postzygotic sex determination in the Hessian Fly ( PubMed DOI PMC

Baird, R. B. et al. Recent evolution of a maternally acting sex-determining supergene in a fly with single-sex broods. PubMed DOI PMC

Charlesworth, B. & Jensen, J. D. Effects of selection at linked sites on patterns of genetic variability. PubMed DOI PMC

Amabis, J. M., Reinach, F. C. & Andrews, N. Spermatogenesis in PubMed DOI

White, M. J. D.

Parker, D. J., Jaron, K. S., Dumas, Z., Robinson-Rechavi, M. & Schwander, T. X chromosomes show relaxed selection and complete somatic dosage compensation across Timema stick insect species. PubMed DOI PMC

Stoletzki, N. & Eyre-Walker, A. Estimation of the neutrality index. PubMed DOI

Charlesworth, J. & Eyre-Walker, A. The McDonald–Kreitman test and slightly deleterious mutations. PubMed DOI

Messer, P. W. & Petrov, D. A. Frequent adaptation and the McDonald–Kreitman test. PubMed DOI PMC

Rice, W. R. Sex chromosomes and the evolution of sexual dimorphism. PubMed DOI

Klein, K., Kokko, H. & Ten Brink, H. Disentangling verbal arguments: intralocus sexual conflict in haplodiploids. PubMed DOI

Wright, A. E., Moghadam, H. K. & Mank, J. E. Trade-off between selection for dosage compensation and masculinization on the avian Z chromosome. PubMed DOI PMC

Allen, S. L., Bonduriansky, R. & Chenoweth, S. F. The genomic distribution of sex-biased genes in Drosophila serrata: X chromosome demasculinization, feminization, and hyperexpression in both sexes. PubMed DOI PMC

Albritton, S. E. et al. Sex-biased gene expression and evolution of the x chromosome in nematodes. PubMed DOI PMC

Mongue, A. J. & Walters, J. R. The Z chromosome is enriched for sperm proteins in two divergent species of Lepidoptera. PubMed DOI

Grath, S. & Parsch, J. Sex-biased gene expression. PubMed DOI

Vicoso, B. & Bachtrog, D. Numerous Transitions of Sex Chromosomes in Diptera. PubMed DOI PMC

Harrison, P. W. et al. Sexual selection drives evolution and rapid turnover of male gene expression. PubMed DOI PMC

Gallach, M., Domingues, S. & Betrán, E. Gene duplication and the genome distribution of sex-biased genes. PubMed PMC

Wright, A. E. et al. Male-biased gene expression resolves sexual conflict through the evolution of sex-specific genetic architecture. PubMed DOI PMC

Bain, S. A. et al. Sex-specific expression and DNA methylation in a species with extreme sexual dimorphism and paternal genome elimination. PubMed DOI

Hitchcock, T. J., Gardner, A. & Ross, L. Sexual antagonism in haplodiploids. PubMed DOI

Yang, L., Zhang, Z. & He, S. Both male-biased and female-biased genes evolve faster in fish genomes. PubMed DOI PMC

Kopp, A., Duncan, I. & Carroll, S. B. Genetic control and evolution of sexually dimorphic characters in Drosophila. PubMed DOI

Krylov, D. M., Wolf, Y. I., Rogozin, I. B. & Koonin, E. V. Gene loss, protein sequence divergence, gene dispensability, expression level, and interactivity are correlated in eukaryotic evolution. PubMed DOI PMC

Drummond, D. A., Bloom, J. D., Adami, C., Wilke, C. O. & Arnold, F. H. Why highly expressed proteins evolve slowly. PubMed DOI PMC

Bédard, C., Cisneros, A. F., Jordan, D. & Landry, C. R. Correlation between protein abundance and sequence conservation: what do recent experiments say?. PubMed DOI

Jaquiéry, J. et al. Accelerated evolution of sex chromosomes in aphids, an X0 system. PubMed DOI

Hitchcock, T. J. Effective population size of X chromosomes and haplodiploids under cyclical parthenogenesis. Preprint at 10.1101/2024.04.05.586733 (2024).

da Cunha, P. R., Granadino, B., Perondini, A. L. & Sánchez, L. Dosage compensation in sciarids is achieved by hypertranscription of the single X chromosome in males. PubMed DOI PMC

Urban, J. M. et al. High contiguity de novo genome assembly and DNA modification analyses for the fungus fly, PubMed DOI PMC

Charlesworth, B. Model for evolution of Y chromosomes and dosage compensation. PubMed DOI PMC

Anderson, N. et al. Gene-rich X chromosomes implicate intragenomic conflict in the evolution of bizarre genetic systems. PubMed DOI PMC

Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. PubMed

Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. PubMed DOI PMC

Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. PubMed DOI PMC

Laetsch, D. R. & Blaxter, M. L. BlobTools: Interrogation of genome assemblies. DOI

Seppey, M., Manni, M. & Zdobnov, E. M. in

Minh, B. Q. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. PubMed DOI PMC

Rambaut, A. FigTree v1.3.1. (2010).

Girgis, H. Z. Red: an intelligent, rapid, accurate tool for detecting repeats de-novo on the genomic scale. PubMed DOI PMC

Stanke, M., Diekhans, M., Baertsch, R. & Haussler, D. Using native and syntenically mapped cDNA alignments to improve de novo gene finding. PubMed DOI

Lomsadze, A., Burns, P. D. & Borodovsky, M. Integration of mapped RNA-Seq reads into automatic training of eukaryotic gene finding algorithm. PubMed PMC

Hoff, K. J., Lange, S., Lomsadze, A., Borodovsky, M. & Stanke, M. BRAKER1: unsupervised RNA-Seq-based genome annotation with GeneMark-ET and AUGUSTUS. PubMed DOI PMC

Hoff, K. J., Lomsadze, A., Borodovsky, M. & Stanke, M. Whole-genome annotation with BRAKER. PubMed PMC

Brůna, T., Hoff, K. J., Lomsadze, A., Stanke, M. & Borodovsky, M. BRAKER2: automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database. PubMed DOI PMC

Kriventseva, E. V. et al. OrthoDB v10: sampling the diversity of animal, plant, fungal, protist, bacterial and viral genomes for evolutionary and functional annotations of orthologs. PubMed DOI PMC

Gabriel, L. et al. BRAKER3: Fully automated genome annotation using RNA-seq and protein evidence with GeneMark-ETP, AUGUSTUS, and TSEBRA. PubMed PMC

Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. PubMed DOI PMC

Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at 10.48550/arXiv.1303.3997 (2013).

Li, H. et al. The sequence alignment/map format and SAMtools. PubMed DOI PMC

Li, H. Minimap2: pairwise alignment for nucleotide sequences. PubMed DOI PMC

Korneliussen, T. S., Albrechtsen, A. & Nielsen, R. ANGSD: analysis of next generation sequencing data. PubMed DOI PMC

McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. PubMed DOI PMC

DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. PubMed DOI PMC

Van der Auwera, G. A. & O’Connor, B. D.

Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. PubMed DOI PMC

Cingolani, P. et al. Using PubMed PMC

Mackintosh, A. et al. The genome sequence of the scarce swallowtail, PubMed DOI PMC

R Core Team.

Emms, D. M. & Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics. PubMed DOI PMC

Navarro-Escalante, L., Zhao, C., Shukle, R. & Stuart, J. BSA-Seq discovery and functional analysis of candidate hessian fly (Mayetiola destructor) avirulence genes. PubMed DOI PMC

Metz, C. W. Genetic evidence of a selective segregation of chromosomes in Sciara (Diptera). PubMed DOI PMC

Gerbi, S. A. Non-random chromosome segregation and chromosome eliminations in the fly Bradysia (Sciara). PubMed DOI PMC

Bray, N., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal RNA-Seq quantification with kallisto. PubMed DOI

Kryuchkova-Mostacci, N. & Robinson-Rechavi, M. A benchmark of gene expression tissue-specificity metrics. PubMed PMC

Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. PubMed DOI PMC

Mongue, A. J., Hansen, M. E., Gu, L., Sorenson, C. E. & Walters, J. R. Nonfertilizing sperm in Lepidoptera show little evidence for recurrent positive selection. PubMed DOI PMC

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...