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
prolekare.web.journal.doi_sk:
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 – Meiosis – Genomic libraries – Sperm – Oocytes – Homologous chromosomes – 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
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2019 Číslo 12
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