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Hybridization promotes asexual reproduction in Caenorhabditis nematodes


Autoři: Piero Lamelza aff001;  Janet M. Young aff003;  Luke M. Noble aff004;  Lews Caro aff001;  Arielle Isakharov aff002;  Meenakshi Palanisamy aff002;  Matthew V. Rockman aff004;  Harmit S. Malik aff001;  Michael Ailion aff001
Působiště autorů: Molecular and Cellular Biology Graduate Program, University of Washington, Seattle, Washington, United States of America aff001;  Department of Biochemistry, University of Washington, Seattle, Washington, United States of America aff002;  Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America aff003;  Department of Biology and Center for Genomics & Systems Biology, New York University, New York, New York, United States of America aff004;  Howard Hughes Medical Institute, Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America aff005
Vyšlo v časopise: Hybridization promotes asexual reproduction in Caenorhabditis nematodes. PLoS Genet 15(12): e32767. doi:10.1371/journal.pgen.1008520
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008520

Souhrn

Although most unicellular organisms reproduce asexually, most multicellular eukaryotes are obligately sexual. This implies that there are strong barriers that prevent the origin or maintenance of asexuality arising from an obligately sexual ancestor. By studying rare asexual animal species we can gain a better understanding of the circumstances that facilitate their evolution from a sexual ancestor. Of the known asexual animal species, many originated by hybridization between two ancestral sexual species. The balance hypothesis predicts that genetic incompatibilities between the divergent genomes in hybrids can modify meiosis and facilitate asexual reproduction, but there are few instances where this has been shown. Here we report that hybridizing two sexual Caenorhabditis nematode species (C. nouraguensis females and C. becei males) alters the normal inheritance of the maternal and paternal genomes during the formation of hybrid zygotes. Most offspring of this interspecies cross die during embryogenesis, exhibiting inheritance of a diploid C. nouraguensis maternal genome and incomplete inheritance of C. becei paternal DNA. However, a small fraction of offspring develop into viable adults that can be either fertile or sterile. Fertile offspring are produced asexually by sperm-dependent parthenogenesis (also called gynogenesis or pseudogamy); these progeny inherit a diploid maternal genome but fail to inherit a paternal genome. Sterile offspring are hybrids that inherit both a diploid maternal genome and a haploid paternal genome. Whole-genome sequencing of individual viable worms shows that diploid maternal inheritance in both fertile and sterile offspring results from an altered meiosis in C. nouraguensis oocytes and the inheritance of two randomly selected homologous chromatids. We hypothesize that hybrid incompatibility between C. nouraguensis and C. becei modifies maternal and paternal genome inheritance and indirectly induces gynogenetic reproduction. This system can be used to dissect the molecular mechanisms by which hybrid incompatibilities can facilitate the emergence of asexual reproduction.

Klíčová slova:

Embryos – Genomic libraries – Homologous chromosomes – Meiosis – Oocytes – Sperm – Chromatids – Maternal inheritance


Zdroje

1. Felsenstein J. THE EVOLUTIONARY ADVANTAGE OF RECOMBINATION. Genetics. 1976;78: 737–756. S1090-0233(10)00296-0 [pii]\r doi: 10.1016/j.tvjl.2010.09.005

2. Gibson AK, Delph LF, Lively CM. The two-fold cost of sex: Experimental evidence from a natural system. Evol Lett. 2017;1: 6–15. doi: 10.1002/evl3.1 30233811

3. Maynard Smith J. What use is sex? J Theor Biol. 1971;30: 319–335. doi: 10.1016/0022-5193(71)90058-0 5548029

4. Dacks J, Roger AJ. The First Sexual Lineage and the Relevance of Facultative Sex. J Mol Evol. 1999;48: 779–83. doi: 10.1007/pl00013156 10229582

5. Kassir Y, Granot D, Simchen G. IME1, a Positive Regulator Gene of Meiosis in S. cerevisiae. Cell. 1988;52: 853–862. doi: 10.1016/0092-8674(88)90427-8 3280136

6. Bell G. The masterpiece of nature: the evolution and genetics of sexuality. University of California Press, Berkeley CA; 1982.

7. Burke NW, Bonduriansky R. Sexual Conflict, Facultative Asexuality, and the True Paradox of Sex. Trends in Ecology and Evolution. Elsevier Ltd; 2017. pp. 646–652. doi: 10.1016/j.tree.2017.06.002 28651895

8. Mirzaghaderi G, Hörandl E. The evolution of meiotic sex and its alternatives. Proc R Soc B Biol Sci. 2016;283: 20161221. doi: 10.1098/rspb.2016.1221 27605505

9. Beukeboom LW, Vrijenhoek RC. Evolutionary genetics and ecology of sperm-dependent parthenogenesis. J Evol Biol. 1998;11: 755–782. doi: 10.1007/s000360050117

10. Coyne JA, Orr HA. Speciation. Sunderland, MA: Sinauer Associates; 2004.

11. Dobzhansky T. On the sterility of the interracial hybrids in Drosophila pseudoobscura. Proc Natl Acad Natl Acad Sci. 1933;19: 397–403. doi: 10.1073/pnas.19.4.397 16577530

12. Gibeaux R, Acker R, Kitaoka M, Georgiou G, van Kruijsbergen I, Ford B, et al. Paternal chromosome loss and metabolic crisis contribute to hybrid inviability in Xenopus. Nature. 2018;553: 337–341. doi: 10.1038/nature25188 29320479

13. Sanei M, Pickering R, Kumke K, Nasuda S, Houben A. Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids. Proc Natl Acad Sci. 2011;108: E498–E505. doi: 10.1073/pnas.1103190108 21746892

14. Ferree PM, Barbash DA. Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biol. 2009;7: e1000234. doi: 10.1371/journal.pbio.1000234 19859525

15. Vrijenhoek RC. Genetic and ecological constraints on the origins and establishment of unisexual vertebrates. Evol Ecol Unisexual Vertebr. 1989; 24–31.

16. Avise JC. Clonality: The Genetics, Ecology, and Evolution of Sexual Abstinence in Vertebrate Animals. Oxford University Press; 2009. doi: 10.1093/acprof:oso/9780195369670.001.0001

17. Lehtonen J, Schmidt DJ, Heubel K, Kokko H. Evolutionary and ecological implications of sexual parasitism. Trends Ecol Evol. 2013;28: 297–306. doi: 10.1016/j.tree.2012.12.006 23399316

18. Newton AA, Schnittker RR, Yu Z, Munday SS, Baumann DP, Neaves WB, et al. Widespread failure to complete meiosis does not impair fecundity in parthenogenetic whiptail lizards. Development. 2016;143: 4486–4494. doi: 10.1242/dev.141283 27802173

19. Ting JJ, Woodruff GC, Leung G, Shin N-R, Cutter AD, Haag ES. Intense sperm-mediated sexual conflict promotes reproductive isolation in Caenorhabditis nematodes. PLoS Biol. 2014;12: e1001915. doi: 10.1371/journal.pbio.1001915 25072732

20. Sadler PL, Shakes DC. Anucleate Caenorhabditis elegans sperm can crawl, fertilize oocytes and direct anterior-posterior polarization of the 1-cell embryo. Development. 2000;127: 355–366. 10603352

21. Cutter AD, Dey A, Murray RL. Evolution of the Caenorhabditis elegans genome. Mol Biol Evol. 2009;26: 1199–1234. doi: 10.1093/molbev/msp048 19289596

22. Roelens B, Schvarzstein M, Villeneuve AM. Manipulation of karyotype in Caenorhabditis elegans reveals multiple inputs driving pairwise chromosome synapsis during meiosis. Genetics. 2015;201: 1363–1379. doi: 10.1534/genetics.115.182279 26500263

23. Fierst JL, Willis JH, Thomas CG, Wang W, Reynolds RM, Ahearne TE, et al. Reproductive Mode and the Evolution of Genome Size and Structure in Caenorhabditis Nematodes. PLoS Genet. 2015;11: e1005323. doi: 10.1371/journal.pgen.1005323 26114425

24. Meneely PM, Farago AF, Kauffman TM. Crossover distribution and high interference for both the X chromosome and an autosome during oogenesis and spermatogenesis in Caenorhabditis elegans. Genetics. 2002;162: 1169–1177. 12454064

25. Madl JE, Herman RK. POLYPLOIDS AND SEX DETERMINATION IN CAENORHABDITIS ELEGANS. Genetics. 1979;93: 393–402. 295035

26. Rockman M V., Kruglyak L. Recombinational landscape and population genomics of Caenorhabditis elegans. PLoS Genet. 2009;5: e1000419. doi: 10.1371/journal.pgen.1000419 19283065

27. Ross JA, Koboldt DC, Staisch JE, Chamberlin HM, Gupta BP, Miller RD, et al. Caenorhabditis briggsae recombinant inbred line genotypes reveal inter-strain incompatibility and the evolution of recombination. PLoS Genet. 2011;7: e1002174. doi: 10.1371/journal.pgen.1002174 21779179

28. Oegema K, Hyman AA. Cell division. WormBook, ed C elegans Res Community, Wormb. doi: 10.1895/wormbook.1.72.1

29. Itono M, Okabayashi N, Morishima K, Fujimoto T, Yoshikawa H, Yamaha E, et al. Cytological Mechanisms of Gynogenesis and Sperm Incorporation in Unreduced Diploid Eggs of the Clonal Loach, Misgurnus anguillicaudatus (Teleostei: Cobitidae). J Exp Zool. 2007;307A: 35–50. doi: 10.1002/jez.a

30. Grosmaire M, Launay C, Siegwald M, Brugière T, Estrada-Virrueta L, Berger D, et al. Males as somatic investment in a parthenogenetic nematode. Science. 2019;363: 1210–1213. doi: 10.1126/science.aau0099 30872523

31. Fopp-Bayat D, Ocalewicz K, Kucinski M, Jankun M, Laczynska B. Disturbances in the ploidy level in the gynogenetic sterlet Acipenser ruthenus. J Appl Genet. 2017;58: 373–380. doi: 10.1007/s13353-017-0389-2 28168627

32. Goda T, Abu-Daya A, Carruthers S, Clark MD, Stemple DL, Zimmerman LB. Genetic screens for mutations affecting development of Xenopus tropicalis. PLoS Genet. 2006;2: e91. doi: 10.1371/journal.pgen.0020091 16789825

33. Hiruta C, Nishida C, Tochinai S. Abortive meiosis in the oogenesis of parthenogenetic Daphnia pulex. Chromosom Res. 2010;18: 833–840. doi: 10.1007/s10577-010-9159-2 20949314

34. Severson AF, Ling L, van Zuylen V, Meyer BJ. The axial element protein HTP-3 promotes cohesin loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation. Genes Dev. 2009;23: 1763–1778. doi: 10.1101/gad.1808809 19574299

35. McNally KP, Panzica MT, Kim T, Cortes DB, McNally FJ. A novel chromosome segregation mechanism during female meiosis. Mol Biol Cell. 2016;27: 2576–2589. doi: 10.1091/mbc.E16-05-0331 27335123

36. Murdy WH, Carson HL. Parthenogenesis in Drosophila mangabeirai Malog. Am Nat. 1959;93: 355–363. doi: 10.1086/282095

37. Cutter AD, Baird SE, Charlesworth D. High nucleotide polymorphism and rapid decay of linkage disequilibrium in wild populations of Caenorhabditis remanei. Genetics. 2006;174: 901–913. doi: 10.1534/genetics.106.061879 16951062

38. Dey A, Chan CKW, Thomas CG, Cutter AD. Molecular hyperdiversity defines populations of the nematode Caenorhabditis brenneri. Proc Natl Acad Sci U S A. 2013;110: 11056–60. doi: 10.1073/pnas.1303057110 23776215

39. Jaquiéry J, Stoeckel S, Larose C, Nouhaud P, Rispe C, Mieuzet L, et al. Genetic Control of Contagious Asexuality in the Pea Aphid. PLoS Genet. 2014;10: e1004838. doi: 10.1371/journal.pgen.1004838 25473828

40. Lamatsch DK, Schmid M, Schartl M. A somatic mosaic of the gynogenetic Amazon molly. J Fish Biol. 2002;60: 1417–1422. doi: 10.1006/jfbi.2002.1939

41. Goddard KA, Megwinoff O, Wessner LL, Giaimo F. Confirmation of gynogenesis in Phoxinus eos-neogaeus (Pisces: Cyprinidae). J Hered. 1998;89: 151–157. doi: 10.1093/jhered/89.2.151

42. Aldrich JC, Leibholz A, Cheema MS, Ausió J, Ferree PM. A “selfish” B chromosome induces genome elimination by disrupting the histone code in the jewel wasp Nasonia vitripennis. Sci Rep. 2017;7: 42551. doi: 10.1038/srep42551 28211924

43. Werren JH, Baldo L, Clark ME. Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol. 2008;6: 741–751. doi: 10.1038/nrmicro1969 18794912

44. Yamaki T, Yasuda GK, Wakimoto BT. The deadbeat paternal effect of uncapped sperm telomeres on cell cycle progression and chromosome behavior in Drosophila melanogaster. Genetics. 2016;203: 799–816. doi: 10.1534/genetics.115.182436 27029731

45. Yasuda GK, Schubiger G, Wakimoto BT. Genetic Characterization of ms(3) K81, a paternal effect gene of Drosophila melanogaster. Genetics. 1995;140: 219–229. 7635287

46. Nelson-Rees WA, Hoy MA, Roush RT. Heterochromatinization, chromatin elimination and haploidization in the parahaploid mite Metaseiulus occidentalis (Nesbitt) (Acarina: Phytoseiidae). Chromosoma. 1980;77: 263–276. doi: 10.1007/bf00286052 7371455

47. Baker BS. PATERNAL LOSS (PAL): A MEIOTIC MUTANT IN DROSOPHILA MELANOGASTER CAUSING LOSS OF PATERNAL CHROMOSOMES. Genetics. 1975;80: 267–96. 805757

48. Kiontke KC, Félix M-A, Ailion M, Rockman M V., Braendle C, Pénigault J-B, et al. A phylogeny and molecular barcodes for Caenorhabditis, with numerous new species from rotting fruits. BMC Evol Biol. 2011;11: 339. doi: 10.1186/1471-2148-11-339 22103856

49. Stevens L, Félix M-A, Beltran T, Braendle C, Caurcel C, Fausett S, et al. Comparative genomics of 10 new Caenorhabditis species. Evol Lett. 2019; 3: 217–236. doi: 10.1002/evl3.110 31007946

50. Brenner S. The Genetics of Caenorhabditis elegans. Genetics. 1974;77: 71–94. doi: 10.1111/j.1749-6632.1999.tb07894.x 4366476

51. Edgar RC. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32: 1792–1797. doi: 10.1093/nar/gkh340 15034147

52. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst Biol. 2010;59: 307–321. doi: 10.1093/sysbio/syq010 20525638

53. Lamelza P, Ailion M. Cytoplasmic–Nuclear Incompatibility Between Wild Isolates of Caenorhabditis nouraguensis. G3. 2017;7: 823–834. doi: 10.1534/g3.116.037101 28064190

54. Collins TJ. ImageJ for microscopy. Biotechniques. 2007;43: S25–S30. doi: 10.2144/000112505

55. Palopoli MF, Rockman M V., TinMaung A, Ramsay C, Curwen S, Aduna A, et al. Molecular basis of the copulatory plug polymorphism in Caenorhabditis elegans. Nature. 2008;454: 1019–1022. doi: 10.1038/nature07171 18633349

56. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol. 2011;29: 24–26. doi: 10.1038/nbt.1754 21221095

57. Bhalla N, Dernburg AF. A conserved checkpoint monitors meiotic chromosome synapsis in Caenorhabditis elegans. Science. 2005;310: 1683–6. doi: 10.1126/science.1117468 16339446

58. Sunnucks P, Hales DF. Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol Biol Evol. 1996;13: 510–524. doi: 10.1093/oxfordjournals.molbev.a025612 8742640

59. Leggett RM, Clavijo BJ, Clissold L, Clark MD, Caccamo M. NextClip: an analysis and read preparation tool for Nextera Long Mate Pair libraries. Bioinformatics. 2014;30: 566–568. doi: 10.1093/bioinformatics/btt702 24297520

60. Davis MPA, van Dongen S, Abreu-Goodger C, Bartonicek N, Enright AJ. Kraken: A set of tools for quality control and analysis of high-throughput sequence data. Methods. 2013;63: 41–49. doi: 10.1016/j.ymeth.2013.06.027 23816787

61. Greenfield P, Duesing K, Papanicolaou A, Bauer DC. Blue: correcting sequencing errors using consensus and context. Bioinformatics. 2014;30: 2723–2732. doi: 10.1093/bioinformatics/btu368 24919879

62. Simpson JT, Durbin R. Efficient de novo assembly of large genomes using compressed data structures. Genome Res. 2012;22: 549–56. doi: 10.1101/gr.126953.111 22156294

63. English AC, Richards S, Han Y, Wang M, Vee V, Qu J, et al. Mind the Gap: Upgrading Genomes with Pacific Biosciences RS Long-Read Sequencing Technology. Liu Z, editor. PLoS One. 2012;7: e47768. doi: 10.1371/journal.pone.0047768 23185243

64. Hunt M, Kikuchi T, Sanders M, Newbold C, Berriman M, Otto TD. REAPR: a universal tool for genome assembly evaluation. Genome Biol. 2013;14: R47. doi: 10.1186/gb-2013-14-5-r47 23710727

65. Li H, Durbin R. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics. 2010;26: 589–595. doi: 10.1093/bioinformatics/btp698 20080505

66. 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

67. Kajitani R, Toshimoto K, Noguchi H, Toyoda A, Ogura Y, Okuno M, et al. Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads. Genome Res. 2013;24: 1384–1395. doi: 10.1038/nbt.2727

68. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, et al. Versatile and open software for comparing large genomes. Genome Biol. 2004;5: R12. doi: 10.1186/gb-2004-5-2-r12 14759262

69. Andolfatto P, Davison D, Erezyilmaz D, Hu TT, Mast J, Sunayama-Morita T, et al. Multiplexed shotgun genotyping for rapid and efficient genetic mapping. Genome Res. 2011;21: 610–7. doi: 10.1101/gr.115402.110 21233398

70. Broman KW, Wu H, Sen S, Churchill GA. R/qtl: QTL mapping in experimental crosses. Bioinformatics. 2003;19: 889–890. doi: 10.1093/bioinformatics/btg112 12724300

71. Taylor J, Butler D. R Package ASMap: Efficient Genetic Linkage Map Construction and Diagnosis. J Stat Softw. 2017;79: 1–29. doi: 10.18637/jss.v079.i04

72. Kent WJ, Baertsch R, Hinrichs A, Miller W, Haussler D. Evolution’s cauldron: duplication, deletion, and rearrangement in the mouse and human genomes. Proc Natl Acad Sci U S A. 2003;100: 11484–9. doi: 10.1073/pnas.1932072100 14500911

73. Laetsch DR, Blaxter ML. BlobTools: Interrogation of genome assemblies. F1000Research. 2017;6: 1287. doi: 10.12688/f1000research.12232.1

74. Wu TD, Nacu S. Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics. 2010;26: 873–881. doi: 10.1093/bioinformatics/btq057 20147302

75. Liu Y, Schröder J, Schmidt B. Musket: a multistage k-mer spectrum-based error corrector for Illumina sequence data. Bioinformatics. 2013;29: 308–315. doi: 10.1093/bioinformatics/bts690 23202746

76. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva E V., Zdobnov EM. BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31: 3210–3212. doi: 10.1093/bioinformatics/btv351 26059717

77. Hunter SS, Lyon RT, Sarver BAJ, Hardwick K, Forney LJ, Settles ML. Assembly by Reduced Complexity (ARC): a hybrid approach for targeted assembly of homologous sequences. bioRxiv. 2015; 014662. doi: 10.1101/014662

78. Dey A, Jeon Y, Wang G-X, Cutter AD. Global population genetic structure of Caenorhabditis remanei reveals incipient speciation. Genetics. 2012;191: 1257–1269. doi: 10.1534/genetics.112.140418 22649079

79. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

80. Huber W, Carey VJ, Gentleman R, Anders S, Carlson M, Carvalho BS, et al. Orchestrating high-throughput genomic analysis with Bioconductor. Nat Methods. 2015;12: 115–121. doi: 10.1038/nmeth.3252 25633503

81. Olshen AB, Venkatraman ES, Lucito R, Wigler M. Circular binary segmentation for the analysis of array-based DNA copy number data. Biostatistics. 2004;5: 557–572. doi: 10.1093/biostatistics/kxh008 15475419

82. Cutter AD, Jovelin R, Dey A. Molecular hyperdiversity and evolution in very large populations. Mol Ecol. 2013;22: 2074–2095. doi: 10.1111/mec.12281 23506466

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