Gene-rich X chromosomes implicate intragenomic conflict in the evolution of bizarre genetic systems
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, Research Support, U.S. Gov't, Non-P.H.S., práce podpořená grantem
PubMed
35653559
PubMed Central
PMC9191650
DOI
10.1073/pnas.2122580119
Knihovny.cz E-zdroje
- Klíčová slova
- genomic conflict, haplodiploidy, insects, sex chromosomes, sex determination,
- MeSH
- chromozom X * genetika MeSH
- diploidie MeSH
- genom * genetika MeSH
- haploidie MeSH
- molekulární evoluce MeSH
- procesy určující pohlaví * MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
Haplodiploidy and paternal genome elimination (HD/PGE) are common in invertebrates, having evolved at least two dozen times, all from male heterogamety (i.e., systems with X chromosomes). However, why X chromosomes are important for the evolution of HD/PGE remains debated. The Haploid Viability Hypothesis posits that X-linked genes promote the evolution of male haploidy by facilitating purging recessive deleterious mutations. The Intragenomic Conflict Hypothesis holds that conflict between genes drives genetic system turnover; under this model, X-linked genes could promote the evolution of male haploidy due to conflicts with autosomes over sex ratios and genetic transmission. We studied lineages where we can distinguish these hypotheses: species with germline PGE that retain an XX/X0 sex determination system (gPGE+X). Because evolving PGE in these cases involves changes in transmission without increases in male hemizygosity, a high degree of X linkage in these systems is predicted by the Intragenomic Conflict Hypothesis but not the Haploid Viability Hypothesis. To quantify the degree of X linkage, we sequenced and compared 7 gPGE+X species’ genomes with 11 related species with typical XX/XY or XX/X0 genetic systems, representing three transitions to gPGE. We find highly increased X linkage in both modern and ancestral genomes of gPGE+X species compared to non-gPGE relatives and recover a significant positive correlation between percent X linkage and the evolution of gPGE. These empirical results substantiate longstanding proposals for a role for intragenomic conflict in the evolution of genetic systems such as HD/PGE.
Department of Biology and Ecology Faculty of Science University of Ostrava Ostrava Czech Republic
Department of Biology San Francisco State University San Francisco CA 94132
Department of Molecular and Cell Biology University of California Merced CA 95343
Department of Thoracic Surgery Brigham and Women's Hospital Boston MA 02115
Iridian Genomes Inc Bethesda MD 20817
Quantitative and Systems Biology Graduate Group University of California Merced CA 95343
Zobrazit více v PubMed
Ashman T. L., et al. ; Tree of Sex Consortium, Tree of sSex: A database of sexual systems. Sci. Data 1, 140015 (2014). PubMed PMC
Brown S. W., Automatic frequency response in the evolution of male haploidy and other coccid chromosome systems. Genetics 49, 797–817 (1964). PubMed PMC
Hamilton W. D., Extraordinary sex ratios. A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. Science 156, 477–488 (1967). PubMed
Hartl D. L., Brown S. W., The origin of male haploid genetic systems and their expected sex ratio. Theor. Popul. Biol. 1, 165–190 (1970). PubMed
Bull J. J., An advantage for the evolution of male haploidy and systems with similar genetic transmission. Heredity 43, 361–381 (1979).
Normark B. B., Perspective: Maternal kin groups and the origins of asymmetric genetic systems-genomic imprinting, haplodiploidy, and parthenogenesis. Evolution 60, 631–642 (2006). PubMed
Gardner A., Ross L., Mating ecology explains patterns of genome elimination. Ecol. Lett. 17, 1602–1612 (2014). PubMed PMC
Blackmon H., Hardy N. B., Ross L., The evolutionary dynamics of haplodiploidy: Genome architecture and haploid viability. Evolution 69, 2971–2978 (2015). PubMed PMC
Goldstein D. B., Deleterious mutations and the evolution of male haploidy. Am. Soc. Nat. 144, 176–183 (1994).
Normark B. B., Haplodiploidy as an outcome of coevolution between male-killing cytoplasmic elements and their hosts. Evolution 58, 790–798 (2004). PubMed
Haig D., The evolution of unusual chromosomal systems in sciarid flies: Intragenomic conflict and the sex ratio. J. Evol. Biol. 6, 249–261 (1993).
Werren J. H., Beukeboom L. W., Sex determination, sex ratios, and genetic conflict. Annu. Rev. Ecol. Syst. 29, 233–261 (1998).
Normark B. B., Ross L., Genetic conflict, kin and the origins of novel genetic systems. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130364 (2014). PubMed PMC
Burt A., Trivers R., Genes in Conflict: The Biology of Selfish Genetic Elements (Harvard University Press, 2006).
Bachtrog D., The Y chromosome as a battleground for intragenomic conflict. Trends Genet. 36, 510–522 (2020). PubMed PMC
Mank J. E., Hosken D. J., Wedell N., Conflict on the sex chromosomes: Cause, effect, and complexity. Cold Spring Harb. Perspect. Biol. 6, a017715 (2014). PubMed PMC
Haig D., The evolution of unusual chromosomal systems in coccoids: Extraordinary sex ratios revisited. J. Evol. Biol. 6, 69–77 (1993).
Ross L., Pen I., Shuker D. M., Genomic conflict in scale insects: The causes and consequences of bizarre genetic systems. Biol. Rev. Camb. Philos. Soc. 85, 807–828 (2010). PubMed
Metz C. W., Chromosome Behavior, Inheritance and Sex Determination in Sciara (American Naturalist, 1938).
White M. J. D., Cytological Studies on Gall Midges (Cecidomyidae) (The University of Texas, 1950).
Dallai R., Fanciulli P. P., Frati F., Aberrant spermatogenesis and the peculiar mechanism of sex determination in Symphypleonan Collembola (Insecta). J. Hered. 91, 351–358 (2000). PubMed
de Souza Amorim D., et al. , Vertical stratification of insect abundance and species richness in an Amazonian tropical forest. Sci. Rep. 12, 1734 (2022). PubMed PMC
Hebert P. D. N., et al. , Counting animal species with DNA barcodes: Canadian insects. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371, 20150333 (2016). PubMed PMC
Ševčík J., Hippa H., Burdíková N., Just a fragment of undescribed diversity: Twenty new oriental and palearctic species of Sciaroidea (Diptera), including DNA sequence data and two new fossil genera. Insects 13, 19 (2021). PubMed PMC
Metz C. W., Chromosome behavior, inheritance and sex determination in Sciara. Am. Nat. 72, 485–520 (1938).
Jaron K. S., Hodson C. N., Ellers J., Baird S. J. E., Ross L., Genomic evidence of paternal genome elimination in globular springtails. bioRxiv [Preprint] (2021) 2021.11.12.468426 (Accessed 3 April 2022). PubMed PMC
Gallun R. L., Hatchett J. H., Genetic evidence of elimination of chromosomes in the Hessian fly. Ann. Entomol. Soc. Am. 62, 1095–1101 (1969).
Stuart J. J., Hatchett J. H., Cytogenetics of the Hessian fly: I. Mitotic karyotype analysis and polytene chromosome correlations. J. Hered. 79, 184–189 (1988). PubMed
Stuart J. J., Hatchett J. H., Cytogenetics of the Hessian fly: II. Inheritance and behavior of somatic and germ-line-limited chromosomes. J. Hered. 79, 190–199 (1988). PubMed
Goday C., Esteban M. R., Chromosome elimination in Sciarid flies. BioEssays 23, 242–250 (2001). PubMed
Muller H., “Bearings of the ‘Drosophila’ work on systematics” in The New Systematics, Huxley J., Ed. (Clarendon Press, 1940), pp. 185–268.
Sved J. A., et al. , Extraordinary conservation of entire chromosomes in insects over long evolutionary periods. Evolution 70, 229–234 (2016). PubMed
Vicoso B., Bachtrog D., Numerous transitions of sex chromosomes in Diptera. PLoS Biol. 13, e1002078 (2015). PubMed PMC
Richards S., Stuart J. J., BCM-HGSC Hessian Fly Genome Project. Baylor Coll. Med. Hum. Genome Seq. Cent. https://www.hgsc.bcm.edu/arthropods/hessian-fly-genome-project. (Accessed 21 June 2018).
Aggarwal R., et al. , A BAC-based physical map of the Hessian fly genome anchored to polytene chromosomes. BMC Genomics 10, 293 (2009). PubMed PMC
Ives A. R., T. Garland, Jr, “Phylogenetic regression for binary dependent variables” in Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology, Garamszegi L. Z., Ed. 2014), pp. 231–261.
Ives A. R., T. Garland, Jr, Phylogenetic logistic regression for binary dependent variables. Syst. Biol. 59, 9–26 (2010). PubMed
Meisel R. P., Delclos P. J., Wexler J. R., The X chromosome of the German cockroach, Blattella germanica, is homologous to a fly X chromosome despite 400 million years divergence. BMC Biol. 17, 100 (2019). PubMed PMC
Schaeffer S. W., et al. , Polytene chromosomal maps of 11 Drosophila species: The order of genomic scaffolds inferred from genetic and physical maps. Genetics 179, 1601–1655 (2008). PubMed PMC
Vicoso B., Bachtrog D., Reversal of an ancient sex chromosome to an autosome in Drosophila. Nature 499, 332–335 (2013). PubMed PMC
Keller Valsecchi C. I., Marois E., Basilicata M. F., Georgiev P., Akhtar A., Distinct mechanisms mediate X chromosome dosage compensation in Anopheles and Drosophila. Life Sci. Alliance 4, e202000996 (2021). PubMed PMC
Zdobnov E. M., et al. , Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster. Science 298, 149–159 (2002). PubMed
Li D., et al. , MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods 102, 3–11 (2016). PubMed
Bankevich A., et al. , SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012). PubMed PMC
Laetsch D. R., Blaxter M. L., BlobTools: Interrogation of genome assemblies [version 1; peer review: 2 approved with reservations]. F1000 Res. 6, 1287 (2017).
Hoff K. J., Lomsadze A., Borodovsky M., Stanke M., Whole-genome annotation with BRAKER. Methods Mol. Biol. 1962, 65–95 (2019). PubMed PMC
Simão F. A., Waterhouse R. M., Ioannidis P., Kriventseva E. V., Zdobnov E. M., BUSCO: Assessing Genome Assembly and Annotation Completeness with Single-Copy Orthologs (Bioinforma, 2015). PubMed
Marygold S. J., Crosby M. A., Goodman J. L., FlyBase Consortium, Using FlyBase, a database of Drosophila genes and genomes. Methods Mol. Biol. 1478, 1–31 (2016). PubMed PMC
Hadfield J. D., Nakagawa S., General quantitative genetic methods for comparative biology: Phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J. Evol. Biol. 23, 494–508 (2010). PubMed
si Tung Ho L., Ané C., A linear-time algorithm for Gaussian and non-Gaussian trait evolution models. Syst. Biol. 63, 397–408 (2014). PubMed
Ševčík J., et al. , Molecular phylogeny of the megadiverse insect infraorder Bibionomorpha sensu lato (Diptera). PeerJ 4, e2563 (2016). PubMed PMC
Genomic evidence of paternal genome elimination in the globular springtail Allacma fusca