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.

Department of Biology and Ecology Faculty of Science University of Ostrava Ostrava Czech Republic

Department of Entomology and Nematology University of Florida Gainesville Florida USA

Institute of Ecology and Evolution University of Edinburgh Edinburgh UK

RIKEN Center for Interdisciplinary Theoretical and Mathematical Sciences RIKEN Wako Japan

School of Biology University of St Andrews St Andrews UK

Whitehead Institute for Biomedical Science and Howard Hughes Medical Institute Cambridge Massachusetts USA

Zobrazit více v PubMed

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

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

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

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

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

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

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

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

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

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.

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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 PMC

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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 PMC

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

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

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

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 PMC

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

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

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

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

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

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 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 PMC

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

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 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 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 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 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 PMC

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

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

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

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

Cingolani, P. et al. Using PubMed PMC

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

R Core Team.

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

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

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

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

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 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 PMC