Ancestral male recombination in Drosophila albomicans produced geographically restricted neo-Y chromosome haplotypes varying in age and onset of decay

Autoři: Kevin H-C. Wei aff001;  Doris Bachtrog aff001
Působiště autorů: Department of Integrative Biology, University of California Berkeley, Berkeley, California, United States of America aff001
Vyšlo v časopise: Ancestral male recombination in Drosophila albomicans produced geographically restricted neo-Y chromosome haplotypes varying in age and onset of decay. PLoS Genet 15(11): e32767. doi:10.1371/journal.pgen.1008502
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008502


Male Drosophila typically have achiasmatic meiosis, and fusions between autosomes and the Y chromosome have repeatedly created non-recombining neo-Y chromosomes that degenerate. Intriguingly, Drosophila nasuta males recombine, but their close relative D. albomicans reverted back to achiasmy after evolving neo-sex chromosomes. Here we use genome-wide polymorphism data to reconstruct the complex evolutionary history of neo-sex chromosomes in D. albomicans and examine the effect of recombination and its cessation on the initiation of neo-Y decay. Population and phylogenomic analyses reveal three distinct neo-Y types that are geographically restricted. Due to ancestral recombination with the neo-X, overall nucleotide diversity on the neo-Y is similar to the neo-X but severely reduced within neo-Y types. Consistently, the neo-Y chromosomes fail to form a monophyletic clade in sliding window trees outside of the region proximal to the fusion. Based on tree topology changes, we inferred the recombination breakpoints that produced haplotypes specific to each neo-Y type. We show that recombination became suppressed at different time points for the different neo-Y haplotypes. Haplotype age correlates with onset of neo-Y decay, and older neo-Y haplotypes show more fixed gene disruption via frameshift indels and down-regulation of neo-Y alleles. Genes are downregulated independently on the different neo-Ys, but are depleted of testes-expressed genes across all haplotypes. This indicates that genes important for male function are initially shielded from degeneration. Our results offer a time course of the early progression of Y chromosome evolution, showing how the suppression of recombination, through the reversal to achiasmy in D. albomicans males, initiates the process of degeneration.

Klíčová slova:

Alleles – Centromeres – Drosophila melanogaster – Haplotypes – Phylogenetic analysis – RNA folding – Sex chromosomes – Y chromosomes


1. Bull JJ. Evolution of Sex Determining Mechanisms. Benjamin/Cummings Publishing Company, Advanced Book Program; 1983.

2. Charlesworth B. Model for evolution of Y chromosomes and dosage compensation. Proc Natl Acad Sci U S A. 1978;75: 5618–5622. doi: 10.1073/pnas.75.11.5618 281711

3. Charlesworth B. The evolution of sex chromosomes. Science. 1991;251: 1030–1033. doi: 10.1126/science.1998119 1998119

4. Bachtrog D. Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet. 2013;14: 113–124. doi: 10.1038/nrg3366 23329112

5. Lahn BT, Page DC. Four evolutionary strata on the human X chromosome. Science. 1999;286: 964–967. doi: 10.1126/science.286.5441.964 10542153

6. Sandstedt SA, Tucker PK. Evolutionary strata on the mouse X chromosome correspond to strata on the human X chromosome. Genome Res. 2004;14: 267–272. doi: 10.1101/gr.1796204 14762062

7. Zhou Q, Zhang J, Bachtrog D, An N, Huang Q, Jarvis ED, et al. Complex evolutionary trajectories of sex chromosomes across bird taxa. Science. 2014;346: 1246338. doi: 10.1126/science.1246338 25504727

8. Handley L-JL, Ceplitis H, Ellegren H. Evolutionary strata on the chicken Z chromosome: implications for sex chromosome evolution. Genetics. 2004;167: 367–376. doi: 10.1534/genetics.167.1.367 15166161

9. Roesti M, Moser D, Berner D. Recombination in the threespine stickleback genome—patterns and consequences. Mol Ecol. 2013;22: 3014–3027. doi: 10.1111/mec.12322 23601112

10. Charlesworth D. Plant Sex Chromosomes. Annu Rev Plant Biol. 2016;67: 397–420. doi: 10.1146/annurev-arplant-043015-111911 26653795

11. Pandey RS, Azad RK. Deciphering evolutionary strata on plant sex chromosomes and fungal mating-type chromosomes through compositional segmentation. Plant Mol Biol. 2016;90: 359–373. doi: 10.1007/s11103-015-0422-y 26694866

12. Hill WG, Robertson A. The effect of linkage on limits to artificial selection. Genet Res. 1966;8: 269–294. 5980116

13. Charlesworth B, Charlesworth D. The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci. 2000;355: 1563–1572. doi: 10.1098/rstb.2000.0717 11127901

14. Rice WR. Evolution of the Y Sex Chromosome in Animals. Bioscience. 1996;46: 331–343.

15. Rice WR. Degeneration of a nonrecombining chromosome. Science. 1994;263: 230–232. doi: 10.1126/science.8284674 8284674

16. Charlesworth B. The evolution of chromosomal sex determination and dosage compensation. Curr Biol. 1996;6: 149–162. doi: 10.1016/s0960-9822(02)00448-7 8673462

17. Muller HJ. THE RELATION OF RECOMBINATION TO MUTATIONAL ADVANCE. Mutat Res. 1964;106: 2–9. doi: 10.1016/0027-5107(64)90047-8 14195748

18. White MJD. Animal Cytology and Evolution. Cambridge University Press; 1973.

19. Charlesworth B, Langley CH, Stephan W. The evolution of restricted recombination and the accumulation of repeated DNA sequences. Genetics. 1986;112: 947–962. 3957013

20. Charlesworth B, Sniegowski P, Stephan W. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature. 1994;371: 215–220. doi: 10.1038/371215a0 8078581

21. Hoskins RA, Smith CD, Carlson JW, Carvalho AB, Halpern A, Kaminker JS, et al. Heterochromatic sequences in a Drosophila whole-genome shotgun assembly. Genome Biol. 2002;3: research0085. doi: 10.1186/gb-2002-3-12-research0085 12537574

22. Jobling MA, Tyler-Smith C. The human Y chromosome: an evolutionary marker comes of age. Nat Rev Genet. 2003;4: 598–612. 12897772

23. Chang C-H, Larracuente AM. Heterochromatin-Enriched Assemblies Reveal the Sequence and Organization of the Drosophila melanogaster Y Chromosome. Genetics. 2019;211: 333–348. doi: 10.1534/genetics.118.301765 30420487

24. Beaudry FEG, Barrett SCH, Wright SI. Genomic Loss and Silencing on the Y Chromosomes of Rumex. Genome Biol Evol. 2017;9: 3345–3355. doi: 10.1093/gbe/evx254 29211839

25. Crowson D, Barrett SCH, Wright SI. Purifying and Positive Selection Influence Patterns of Gene Loss and Gene Expression in the Evolution of a Plant Sex Chromosome System. Mol Biol Evol. 2017;34: 1140–1154. doi: 10.1093/molbev/msx064 28158772

26. Liu Z, Moore PH, Ma H, Ackerman CM, Ragiba M, Yu Q, et al. A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature. 2004;427: 348–352. doi: 10.1038/nature02228 14737167

27. Marais GAB, Nicolas M, Bergero R, Chambrier P, Kejnovsky E, Monéger F, et al. Evidence for degeneration of the Y chromosome in the dioecious plant Silene latifolia. Curr Biol. 2008;18: 545–549. doi: 10.1016/j.cub.2008.03.023 18394889

28. Peichel CL, Ross JA, Matson CK, Dickson M, Grimwood J, Schmutz J, et al. The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome. Curr Biol. 2004;14: 1416–1424. doi: 10.1016/j.cub.2004.08.030 15324658

29. Vicoso B, Charlesworth B. Evolution on the X chromosome: unusual patterns and processes. Nat Rev Genet. 2006;7: 645–653. 16847464

30. Marin R, Cortez D, Lamanna F, Pradeepa MM, Leushkin E, Julien P, et al. Convergent origination of a -like dosage compensation mechanism in a reptile lineage. Genome Res. 2017;27: 1974–1987. doi: 10.1101/gr.223727.117 29133310

31. McQueen HA, McBride D, Miele G, Bird AP, Clinton M. Dosage compensation in birds. Curr Biol. 2001;11: 253–257. doi: 10.1016/s0960-9822(01)00070-7 11250153

32. Ellegren H, Hultin-Rosenberg L, Brunström B, Dencker L, Kultima K, Scholz B. Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes. BMC Biol. 2007;5: 40. doi: 10.1186/1741-7007-5-40 17883843

33. Schield DR, Card DC, Hales NR, Perry BW, Pasquesi GM, Blackmon H, et al. The origins and evolution of chromosomes, dosage compensation, and mechanisms underlying venom regulation in snakes. Genome Res. 2019;29: 590–601. doi: 10.1101/gr.240952.118 30898880

34. Sturtevant AH, Novitski E. The Homologies of the Chromosome Elements in the Genus Drosophila. Genetics. 1941;26: 517–541. 17247021

35. Muller JH. Bearings of the Drosophila work on systematics in New systematic J. Huxley, Ed. Clarendon Press, Oxford; 1940.

36. Vicoso B, Bachtrog D. Numerous Transitions of Sex Chromosomes in Diptera. PLoS Biol. 2015;13: e1002078. doi: 10.1371/journal.pbio.1002078 25879221

37. Carvalho AB, Clark AG. Y Chromosome of D. pseudoobscura Is Not Homologous to the Ancestral Drosophila Y. Science. 2005;307: 108–110. doi: 10.1126/science.1101675 15528405

38. Mahajan S, Bachtrog D. Convergent evolution of Y chromosome gene content in flies. Nat Commun. 2017;8: 785. doi: 10.1038/s41467-017-00653-x 28978907

39. Bachtrog D, Charlesworth B. Reduced adaptation of a non-recombining neo-Y chromosome. Nature. 2002;416: 323–326. doi: 10.1038/416323a 11907578

40. Steinemann M, Steinemann S. Enigma of Y chromosome degeneration: Neo-Y and Neo-X chromosomes of Drosophila miranda a model for sex chromosome evolution. Genetica. 1998;102: 409. 9720292

41. Bachtrog D. Expression profile of a degenerating neo-y chromosome in Drosophila. Curr Biol. 2006;16: 1694–1699. doi: 10.1016/j.cub.2006.07.053 16950105

42. Bachtrog D, Hom E, Wong KM, Maside X, de Jong P. Genomic degradation of a young Y chromosome in Drosophila miranda. Genome Biol. 2008;9: R30. doi: 10.1186/gb-2008-9-2-r30 18269752

43. Mahajan S, Wei KH-C, Nalley MJ, Gibilisco L, Bachtrog D. De novo assembly of a young Drosophila Y chromosome using single-molecule sequencing and chromatin conformation capture. PLoS Biol. 2018;16: e2006348. doi: 10.1371/journal.pbio.2006348 30059545

44. Krivshenko JD. A CYTOGENETIC STUDY OF THE X CHROMOSOME OF Drosophila Busckii AND ITS RELATION TO PHYLOGENY. Proc Natl Acad Sci U S A. 1955;41: 1071–1079. doi: 10.1073/pnas.41.12.1071 16589798

45. Zhou Q, Bachtrog D. Ancestral Chromatin Configuration Constrains Chromatin Evolution on Differentiating Sex Chromosomes in Drosophila. PLoS Genet. 2015;11: e1005331. doi: 10.1371/journal.pgen.1005331 26114585

46. Kitagawa O, Wakahama K-I, Fuyama Y, Shimada Y, Takanashi E, Hatsumi M, et al. Genetic studies of the Drosophila nasuta subgroup, with notes on distribution and morphology. 遺伝學雑誌. 1982;57: 113–141.

47. Ohsako T, Aotsuka T, Kitagawa O. The origins of the Japanese mainland population of Drosophila albomicans. Jpn J Genet. 1994;69: 183–194. doi: 10.1266/jjg.69.183 8074888

48. Chang H-Y, Ayala FJ. ON THE ORIGIN OF INCIPIENT REPRODUCTIVE ISOLATION: THE CASE OF DROSOPHILA ALBOMICANS AND D. NASUTA. Evolution. 1989;43: 1610–1624. doi: 10.1111/j.1558-5646.1989.tb02612.x 28564329

49. Bachtrog D. The speciation history of the Drosophila nasuta complex. Genet Res. 2006;88: 13–26. doi: 10.1017/S0016672306008330 17014741

50. Cheng C-H, Chang C-H, Chang H-Y. Early-Stage Evolution of the Neo-Y Chromosome in Drosophila albomicans. Zool Stud. 2011;50: 338–349.

51. Kim Y-K, Phillips DR, Tao Y. Evidence for no sexual isolation between Drosophila albomicans and D. nasuta. Ecol Evol. 2013;3: 2061–2074. doi: 10.1002/ece3.619 23919152

52. Wakahama K-I, Shinohara T, Hatsumi M, Uchida S, Kitagawa O. Metaphase chromosome configuration of the immigrans species group of Drosophila. 遺伝學雑誌. 1983;58: 315–326.

53. Yu YC, Lin FJ, Chang HY. Stepwise chromosome evolution in Drosophila albomicans. Heredity. 1999;83 (Pt 1): 39–45.

54. Zhou Q, Bachtrog D. Chromosome-wide gene silencing initiates Y degeneration in Drosophila. Curr Biol. 2012;22: 522–525. doi: 10.1016/j.cub.2012.01.057 22365853

55. McAllister BF, Charlesworth B. Reduced sequence variability on the Neo-Y chromosome of Drosophila americana americana. Genetics. 1999;153: 221–233. 10471708

56. Satomura K, Tamura K. Ancient Male Recombination Shaped Genetic Diversity of Neo-Y Chromosome in Drosophila albomicans. Mol Biol Evol. 2016;33: 367–374. doi: 10.1093/molbev/msv221 26494844

57. Elgin SCR, Reuter G. Position-effect variegation, heterochromatin formation, and gene silencing in Drosophila. Cold Spring Harb Perspect Biol. 2013;5: a017780. doi: 10.1101/cshperspect.a017780 23906716

58. Alekseyenko AA, Ellison CE, Gorchakov AA, Zhou Q, Kaiser VB, Toda N, et al. Conservation and de novo acquisition of dosage compensation on newly evolved sex chromosomes in Drosophila. Genes Dev. 2013;27: 853–858. doi: 10.1101/gad.215426.113 23630075

59. Ellison CE, Bachtrog D. Dosage compensation via transposable element mediated rewiring of a regulatory network. Science. 2013;342: 846–850. doi: 10.1126/science.1239552 24233721

60. Tschiersch B, Hofmann A, Krauss V, Dorn R, Korge G, Reuter G. The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J. 1994;13: 3822–3831. 7915232

61. Ebert A, Lein S, Schotta G, Reuter G. Histone modification and the control of heterochromatic gene silencing in Drosophila. Chromosome Res. 2006;14: 377–392. 16821134

62. Lucchesi JC, Kuroda MI. Dosage compensation in Drosophila. Cold Spring Harb Perspect Biol. 2015;7. doi: 10.1101/cshperspect.a019398 25934013

63. McManus CJ, Coolon JD, Duff MO, Eipper-Mains J, Graveley BR, Wittkopp PJ. Regulatory divergence in Drosophila revealed by mRNA-seq. Genome Res. 2010;20: 816–825. doi: 10.1101/gr.102491.109 20354124

64. Zhang L, Sun T, Woldesellassie F, Xiao H, Tao Y. Sex Ratio Meiotic Drive as a Plausible Evolutionary Mechanism for Hybrid Male Sterility. PLoS Genet. 2015;11: e1005073. doi: 10.1371/journal.pgen.1005073 25822261

65. Harrison RG, Larson EL. Hybridization, introgression, and the nature of species boundaries. J Hered. 2014;105 Suppl 1: 795–809.

66. Turissini DA, Matute DR. Fine scale mapping of genomic introgressions within the Drosophila yakuba clade. PLoS Genet. 2017;13: e1006971. doi: 10.1371/journal.pgen.1006971 28873409

67. Yoshida K, Makino T, Kitano J. Accumulation of Deleterious Mutations on the Neo-Y Chromosome of Japan Sea Stickleback (Gasterosteus nipponicus). J Hered. 2017;108: 63–68. 27614083

68. Rens W, O’Brien PCM, Grützner F, Clarke O, Graphodatskaya D, Tsend-Ayush E, et al. The multiple sex chromosomes of platypus and echidna are not completely identical and several share homology with the avian Z. Genome Biol. 2007;8: R243. doi: 10.1186/gb-2007-8-11-r243 18021405

69. Mikkelsen TS, Wakefield MJ, Aken B, Amemiya CT, Chang JL, Duke S, et al. Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature. 2007;447: 167–177. doi: 10.1038/nature05805 17495919

70. Cortez D, Marin R, Toledo-Flores D, Froidevaux L, Liechti A, Waters PD, et al. Origins and functional evolution of Y chromosomes across mammals. Nature. 2014;508: 488–493. doi: 10.1038/nature13151 24759410

71. Helena Mangs A, Morris BJ. The Human Pseudoautosomal Region (PAR): Origin, Function and Future. Curr Genomics. 2007;8: 129–136. doi: 10.2174/138920207780368141 18660847

72. Lemaitre C, Braga MDV, Gautier C, Sagot M-F, Tannier E, Marais GAB. Footprints of inversions at present and past pseudoautosomal boundaries in human sex chromosomes. Genome Biol Evol. 2009;1: 56–66. doi: 10.1093/gbe/evp006 20333177

73. Marais G, Galtier N. Sex chromosomes: how X-Y recombination stops. Curr Biol. 2003;13: R641–3. doi: 10.1016/s0960-9822(03)00570-0 12932341

74. Kaiser VB, Zhou Q, Bachtrog D. Nonrandom gene loss from the Drosophila miranda neo-Y chromosome. Genome Biol Evol. 2011;3: 1329–1337. doi: 10.1093/gbe/evr103 21987387

75. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25: 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168

76. Mai D, Nalley MJ, Bachtrog D. Patterns of genomic differentiation in the Drosophila nasuta species complex. Mol Biol Evol. 2019. doi: 10.1093/molbev/msz215 31556453

77. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20: 1297–1303. doi: 10.1101/gr.107524.110 20644199

78. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 2011;43: 491–498. doi: 10.1038/ng.806 21478889

79. Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics. 2011;27: 2987–2993. doi: 10.1093/bioinformatics/btr509 21903627

80. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics. 2012;13: 134. doi: 10.1186/1471-2105-13-134 22708584

81. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30: 1312–1313. doi: 10.1093/bioinformatics/btu033 24451623

82. Bouckaert RR. DensiTree: making sense of sets of phylogenetic trees. Bioinformatics. 2010;26: 1372–1373. doi: 10.1093/bioinformatics/btq110 20228129

83. Revell LJ. phytools: an R package for phylogenetic comparative biology (and other things): phytools: R package. Methods Ecol Evol. 2012;3: 217–223.

84. Paradis E, Claude J, Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics. 2004;20: 289–290. doi: 10.1093/bioinformatics/btg412 14734327

85. Pertea M, Pertea GM, Antonescu CM, Chang T-C, Mendell JT, Salzberg SL. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 2015;33: 290–295. doi: 10.1038/nbt.3122 25690850

86. Zhang Z, Li J, Zhao X-Q, Wang J, Wong GK-S, Yu J. KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinformatics. 2006;4: 259–263. doi: 10.1016/S1672-0229(07)60007-2 17531802

87. Wang D-P, Wan H-L, Zhang S, Yu J. Gamma-MYN: a new algorithm for estimating Ka and Ks with consideration of variable substitution rates. Biol Direct. 2009;4: 20. doi: 10.1186/1745-6150-4-20 19531225

88. Liao Y, Smyth GK, Shi W. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res. 2013;41: e108. doi: 10.1093/nar/gkt214 23558742

89. Huang W, Li L, Myers JR, Marth GT. ART: a next-generation sequencing read simulator. Bioinformatics. 2012;28: 593–594. doi: 10.1093/bioinformatics/btr708 22199392

90. Brind’Amour J, Liu S, Hudson M, Chen C, Karimi MM, Lorincz MC. An ultra-low-input native ChIP-seq protocol for genome-wide profiling of rare cell populations. Nat Commun. 2015;6: 6033. doi: 10.1038/ncomms7033 25607992

91. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26: 841–842. doi: 10.1093/bioinformatics/btq033 20110278

92. Gibilisco L, Zhou Q, Mahajan S, Bachtrog D. Alternative Splicing within and between Drosophila Species, Sexes, Tissues, and Developmental Stages. PLoS Genet. 2016;12: e1006464. doi: 10.1371/journal.pgen.1006464 27935948

93. Yanai I, Benjamin H, Shmoish M, Chalifa-Caspi V, Shklar M, Ophir R, et al. Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification. Bioinformatics. 2005;21: 650–659. doi: 10.1093/bioinformatics/bti042 15388519

Genetika Reprodukční medicína

Článek vyšel v časopise

PLOS Genetics

2019 Číslo 11

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Zvyšte si kvalifikaci online z pohodlí domova

Kurz originály vs. generika
nový kurz

Klinická farmakokinetika betablokátorů

Současné možnosti terapie osteoartrózy
Autoři: MUDr. Jakub Holešovský

Preferovaná úlevová léčba Asthma Bronchiale
Autoři: PharmDr. Petr Sedlák

Inhibitory karboanhydrázy v léčbě glaukomu
Autoři: MUDr. Petr Výborný, CSc., FEBO

Všechny kurzy
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.


Nemáte účet?  Registrujte se