Gonad morphogenesis defects drive hybrid male sterility in asymmetric hybrid breakdown of Caenorhabditis nematodes

Evolution and Development

Volumn 16, Issue 6, 2014, Pages 362-372

  Dey, Alivia ^a   Jin, Qi ^a   Chen, Yen Chu ^a   Cutter, Asher D ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FITNESS; GENE FLOW; HYBRID; MALE; MORPHOGENESIS; NEMATODE; SPECIATION (BIOLOGY); STERILITY;

CAENORHABDITIS; CAENORHABDITIS REMANEI; NEMATODA;

ANIMAL; CAENORHABDITIS; CLASSIFICATION; CYTOLOGY; FEMALE; GENETICS; GONAD; HYBRIDIZATION; MALE; PHYSIOLOGY;

ANIMALS; CAENORHABDITIS; FEMALE; GONADS; HYBRIDIZATION, GENETIC; MALE;

EID: 84922393281     PISSN: 1520541X     EISSN: 1525142X     Source Type: Journal    
DOI: 10.1111/ede.12097     Document Type: Article

References (78)

1. Abraham, M. C., Lu, Y., and Shaham, S. 2007. A morphologically conserved nonapoptotic program promotes linker cell death in Caenorhabditis elegans. Dev. Cell. 12: 73-86.
2. Artieri, C. G., Haerty, W., Gupta, B. P., and Singh, R. S. 2008. Sexual selection and maintenance of sex: evidence from comparisons of rates of genomic accumulation of mutations and divergence of sex-related genes in sexual and hermaphroditic species of Caenorhabditis. Mol. Biol. Evol. 25: 972-979.
3. Baird, S. E. 2002. Haldane's rule by sexual transformation in Caenorhabditis. Genetics 161: 1349-1353.
4. Baird, S. E., and Seibert, S. R. 2013. Reproductive isolation in the Elegans-Group of Caenorhabditis. Natural Sci. 5: 18-25.
5. Baird, S. E., and Stonesifer, R. 2012. Reproductive isolation in Caenorhabditis briggsae: dysgenic interactions between maternal- and zygotic-effect loci result in a delayed development phenotype. Worm 1: 189-195.
6. Baird, S. E., Sutherlin, M. E., and Emmons, S. W. 1992. Reproductive isolation in Rhabditidae (Nematoda, Secernentea): mechanisms that isolate 6 species of 3 genera. Evolution 46: 585-594.
7. Baird, S. E., and Yen, W.-C. 2000. Reproductive isolation in Caenorhabditis: terminal phenotypes of hybrid embryos. Evol. Dev. 2: 9-15.
8. Bao, Z. R., Murray, J. I., Boyle, T., Ooi, S. L., Sandel, M. J., and Waterston, R. H. 2006. Automated cell lineage tracing in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. 103: 2707-2712.
9. Barker, D. M. 1994. Copulatory plugs and paternity assurance in the nematode Caenorhabditis elegans. Anim. Behav. 48: 147-156.
10. Batista, P. J., et al. 2008. PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol. Cell. 31: 67-78.
11. Baugh, L. R., Hill, A. A., Slonim, D. K., Brown, E. L., and Hunter, C. P. 2003. Composition and dynamics of the Caenorhabditis elegans early embryonic transcriptome. Development 130: 889-900.
12. Blelloch, R., and Kimble, J. 1999. Control of organ shape by a secreted metalloprotease in the nematode Caenorhabditis elegans. Nature 399: 586-590.
13. Blelloch, R., Santa Anna-Arriola, S., Gao, D. L., Li, Y. J., Hodgkin, J., and Kimble, J. 1999. The gon-1 gene is required for gonadal morphogenesis in Caenorhabditis elegans. Dev. Biol. 216: 382-393.
14. Blum, E. S., Abraham, M. C., Yoshimura, S., Lu, Y., and Shaham, S. 2012. Control of nonapoptotic developmental cell death in Caenorhabditis elegans by a polyglutamine-repeat protein. Science 335: 970-973.
15. Bolnick, D. I., Turelli, M., Lopez-Fernandez, H., Wainwright, P. C., and Near, T. J. 2008. Accelerated mitochondrial evolution and "Darwin's corollary": asymmetric viability of reciprocal F1 hybrids in Centrarchid fishes. Genetics 178: 1037-1048.
16. Brown, J. D., and O'Neill, R. J. 2010. Chromosomes, conflict, and epigenetics: chromosomal speciation revisited. Annu. Rev. Genom. Hum. Genet. 11: 291-316.
17. Campbell, P., Good, J. M., and Nachman, M. W. 2013. Meiotic sex chromosome inactivation is disrupted in sterile hybrid male house mice. Genetics 193: 819-828.
18. Conine, C. C., et al. 2009. Argonautes ALG-3 and ALG-4 are required for spermatogenesis-specific 26G-RNAs and thermotolerant sperm in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. 107: 3588-3593.
19. Coyne, J. A., and Orr, H. A. 2004. Speciation. Sinauer, Sunderland, MA.
20. Cutter, A. D. 2012. The polymorphic prelude to Bateson-Dobzhansky-Muller incompatibilities. Trends Ecol. Evol. 27: 209-218.
21. Cutter, A. D., Dey, A., and Murray, R. L. 2009. Evolution of the Caenorhabditis elegans genome. Mol. Biol. Evol. 26: 1199-1234.
22. Cutter, A. D., and Ward, S. 2005. Sexual and temporal dynamics of molecular evolution in C. elegans development. Mol. Biol. Evol. 22: 178-188.
23. Dey, A., Jeon, Y., Wang, G.-X., and Cutter, A. D. 2012. Global population genetic structure of Caenorhabditis remanei reveals incipient speciation. Genetics 191: 1257-1269.
24. Dobzhansky, T. 1936. Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21: 113-135.
25. Ellegren, H., and Parsch, J. 2007. The evolution of sex-biased genes and sex-biased gene expression. Nat. Rev. Genet. 8: 689-698.
26. Euling, S., Bettinger, J. C., and Rougvie, A. E. 1999. The LIN-29 transcription factor is required for proper morphogenesis of the Caenorhabditis elegans male tail. Dev. Biol. 206: 142-156.
27. Felix, M. A., Braendle, C., and Cutter, A. D. 2014. A streamlined system for species diagnosis in Caenorhabditis (Nematoda: Rhabditidae) with name designations for 15 distinct biological species. PLoS ONE 9: e94723.
28. Garcia, L. R., LeBoeuf, B., and Koo, P. 2007. Diversity in mating behavior of hermaphroditic and male-female Caenorhabditis nematodes. Genetics 175: 1761-1771.
29. Haag, E. S., Wang, S. P., and Kimble, J. 2002. Rapid coevolution of the nematode sex-determining genes fem-3 and tra-2. Curr. Biol. 12: 2035-2041.
30. Haldane, J. B. S. 1922. Sex ratio and unisexual sterility in hybrid animals. J. Genet. 12: 101-109.
31. Hedgecock, E. M., Culotti, J. G., and Hall, D. H. 1990. The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4: 61-85.
32. Hill, K. L., and L'Hernault, S. W. 2001. Analyses of reproductive interactions that occur after heterospecific matings within the genus Caenorhabditis. Dev. Biol. 232: 105-114.
33. Hill, R. C., and Haag, E. S. 2009. A sensitized genetic background reveals evolution near the terminus of the Caenorhabditis germline sex determination pathway. Evol. Dev. 11: 333-342.
34. Hodgkin, J., and Doniach, T. 1997. Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 146: 149-164.
35. Howard, D. J., Palumbi, S. R., Birge, L. M., and Manier, M. K. 2009. Sperm and speciation. In T. R. Birkhead, D. J. Hosken and S. Pitnick (eds.). Sperm Biology: An Evolutionary Perspective. Academic Press, Boston.
36. Hutter, P. 1997. Genetics of hybrid inviability Drosophila. Adv. Genet. 36: 157-185.
37. Johnson, C. L., and Spence, A. M. 2011. Epigenetic licensing of germline gene expression by maternal RNA in C. elegans. Science 333: 1311-1314.
38. Kato, M., and Sternberg, P. W. 2009. The C. elegans tailless/Tlx homolog nhr-67 regulates a stage-specific program of linker cell migration in male gonadogenesis. Development 136: 3907-3915.
39. Kelleher, E. S., Edelman, N. B., and Barbash, D. A. 2012. Drosophila interspecific hybrids phenocopy piRNA-pathway mutants. PLoS Biol. 10: e1001428.
40. Kimble, J. E., and White, J. G. 1981. On the control of germ-cell development in Caenorhabditis elegans. Dev. Biol. 81: 208-219.
41. Kiontke, K., et al. 2011. A phylogeny and molecular barcodes for Caenorhabditis, with numerous new species from rotting fruits. BMC Evol. Biol. 11: 339.
42. Klass, M., Wolf, N., and Hirsh, D. 1976. Development of male reproductive-system and sexual transformation in nematode Caenorhabditis elegans. Dev. Biol. 52: 1-118.
43. Koevoets, T., van de Zande, L., and Beukeboom, L. W. 2012. Temperature stress increases hybrid incompatibilities in the parasitic wasp genus Nasonia. J. Evol. Biol. 25: 304-316.
44. Kozlowska, J. L., Ahmad, A. R., Jahesh, E., and Cutter, A. D. 2012. Genetic variation for post-zygotic reproductive isolation between Caenorhabditis briggsae and Caenorhabditis sp. 9. Evolution 66: 1180-1195.
45. LaMunyon, C. W., and Ward, S. 1997. Increased competitiveness of nematode sperm bearing the male X chromosome. Proc. Natl. Acad. Sci. USA. 94: 185-189.
46. Levin, M., Hashimshony, T., Wagner, F., and Yanai, I. 2012. Developmental milestones punctuate gene expression in the Caenorhabditis embryo. Dev. Cell. 22: 1101-1108.
47. Lipton, J., Kleemann, G., Ghosh, R., Lints, R., and Emmons, S. W. 2004. Mate searching in Caenorhabditis elegans: a genetic model for sex drive in a simple invertebrate. J. Neurosci. 24: 7427-7434.
48. Maheshwari, S., and Barbash, D. A. 2011. The genetics of hybrid incompatibilities. Annu. Rev. Genet. 45: 331-355.
49. Martin-Coello, J., Benavent-Corai, J., Roldan, E. R. S., and Gomendio, M. 2009. Sperm competition promotes asymmetries in reproductive barriers between closely related species. Evolution 63: 613-623.
50. Martin, N. H., and Willis, J. H. 2010. Geographical variation in postzygotic isolation and its genetic basis within and between two Mimulus species. Philos. Trans. R. Soc. B 365: 2469-2478.
51. Michalak, P., and Noor, M. A. F. 2003. Genome-wide patterns of expression in Drosophila pure species and hybrid males. Mol. Biol. Evol. 20: 1070-1076.
52. Miller, M. A., et al. 2001. A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 291: 2144-2147.
53. Muller, H. J. 1940. Bearings of the Drosophila work on systematics. In J. Huxley (ed.). New Systematics. Clarendon Press, Oxford.
54. Muller, H. J. 1942. Isolating mechanisms, evolution and temperature. Biol. Symp. 6: 71-125.
55. Nishiwaki, K., Hisamoto, N., and Matsumoto, K. 2000. A metalloprotease disintegrin that controls cell migration in Caenorhabditis elegans. Science 288: 2205-2208.
56. Orr, H. A. 1993. Haldane rule has multiple genetic causes. Nature 361: 532-533.
57. Palopoli, M. F., et al. 2008. Molecular basis of the copulatory plug polymorphism in Caenorhabditis elegans. Nature 454: 1019-1022.
58. Presgraves, D. C. 2010. Darwin and the origin of interspecific genetic incompatibilities. Am. Nat. 176: S45-S60.
59. Presgraves, D. C. 2010. The molecular evolutionary basis of species formation. Nat. Rev. Genet. 11: 175-180.
60. Ranz, J. M., Namgyal, K., Gibson, G., and Hartl, D. L. 2004. Anomalies in the expression profile of interspecific hybrids of Drosophila melanogaster and Drosophila simulans. Genome Res. 14: 373-379.
61. Riche, S., Zouak, M., Argoul, Fo., Arneodo, A., Pecreaux, J., and Delattre, M. 2013. Evolutionary comparisons reveal a positional switch for spindle pole oscillations in Caenorhabditis embryos. J. Cell Biol. 201: 653-662.
62. Schilthuizen, M., Giesbers, M. C. W. G., and Beukeboom, L. W. 2011. Haldane's rule in the 21st century. Heredity 107: 95-102.
63. Smith, J. R., and Stanfield, G. M. 2011. TRY-5 is a sperm-activating protease in Caenorhabditis elegans seminal fluid. PLoS Genet. 7: e1002375.
64. Stiernagle, T. L. 1999. Maintenance of C. elegans. In I. A. Hope (ed.). C. elegans: A Practical Approach. Oxford University Press, New York.
65. Tiffin, P., Olson, M. S., and Moyle, L. C. 2001. Asymmetrical crossing barriers in angiosperms. Proc. R. Soc. B 268: 861-867.
66. Ting, J. J., Woodruff, G. C., Leung, G., Shin, N.-R., Cutter, A. D., and Haag, E. S. 2014. Intense sperm-mediated sexual conflict promotes gametic isolation in Caenorhabditis nematodes. PLoS Biol. 12: e1001915.
67. Turelli, M., and Moyle, L. C. 2007. Asymmetric postmating isolation: Darwin's corollary to Haldane's rule. Genetics 176: 1059-1088.
68. Turelli, M., and Orr, H. A. 1995. The dominance theory of Haldane's rule. Genetics 140: 389-402.
69. Vogel, B. E., and Hedgecock, E. M. 2001. Hemicentin, a conserved extracellular member of the immunoglobulin superfamily, organizes epithelial and other cell attachments into oriented line-shaped junctions. Development 128: 883-894.
70. Vrana, P. B. 2007. Genomic imprinting as a mechanism of reproductive isolation in mammals. J. Mammal. 88: 5-23.
71. Wade, M. J., Johnson, N. A., and Toquenaga, Y. 1999. Temperature effects and genotype-by-environment interactions in hybrids: Haldane's rule in flour beetles. Evolution 53: 855-865.
72. Wang, G., and Reinke, V. 2008. A C. elegans Piwi, PRG-1, regulates 21U-RNAs during spermatogenesis. Curr. Biol. 18: 861-867.
73. Woodruff, G. C., Eke, O., Baird, S. E., Felix, M. A., and Haag, E. S. 2010. Insights into species divergence and the evolution of hermaphroditism from fertile interspecies hybrids of Caenorhabditis nematodes. Genetics 186: 997-1012.
74. Wu, C. I., and Davis, A. W. 1993. Evolution of postmating reproductive isolation: the composite nature of Haldane rule and its genetic bases. Am. Nat. 142: 187-212.
75. Wu, C. I., Johnson, N. A., and Palopoli, M. F. 1996. Haldane's rule and its legacy: why are there so many sterile males? Trends Ecol. Evol. 11: 281-284.
76. Wu, T. F., Nera, B., Chu, D. S., and Shakes, D. C. 2010. Elucidating gene regulatory mechanisms for sperm function through the integration of classical and systems approaches in C. elegans. Syst. Biol. Reprod. Med. 56: 222-235.
77. Yan, C., Bi, Y., Yin, D., and Zhao, Z. 2012. A method for rapid and simultaneous mapping of genetic loci and introgression sizes in nematode species. PLoS ONE 7: e43770.
78. Zhao, Z., Boyle, T. J., Bao, Z., Murray, J. I., Mericle, B., and Waterston, R. H. 2008. Comparative analysis of embryonic cell lineage between Caenorhabditis briggsae and Caenorhabditis elegans. Dev. Biol. 314: 93-99.