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. 2000 Jul;155(3):1469–1479. doi: 10.1093/genetics/155.3.1469

Maternal-zygotic gene conflict over sex determination: effects of inbreeding.

J H Werren 1, M J Hatcher 1
PMCID: PMC1461153  PMID: 10880504

Abstract

There is growing evidence that sex determination in a wide range of organisms is determined by interactions between maternal-effect genes and zygotically expressing genes. Maternal-effect genes typically produce products (e.g., mRNA or proteins) that are placed into the egg during oogenesis and therefore depend upon maternal genotype. Here it is shown that maternal-effect and zygotic genes are subject to conflicting selective pressures over sex determination in species with partial inbreeding or subdivided populations. The optimal sex ratios for maternal-effect genes and zygotically expressing genes are derived for two models: partial inbreeding (sibmating) and subdivided populations with local mating in temporary demes (local mate competition). In both cases, maternal-effect genes are selected to bias sex determination more toward females than are zygotically expressed genes. By investigating the invasion criteria for zygotic genes in a population producing the maternal optimum (and vice versa), it is shown that genetic conflict occurs between these genes. Even relatively low levels of inbreeding or subdivision can result in maternal-zygotic gene conflict over sex determination. The generality of maternal-zygotic gene conflict to sex determination evolution is discussed; such conflict should be considered in genetic studies of sex-determining mechanisms.

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Selected References

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  1. Ahringer J., Rosenquist T. A., Lawson D. N., Kimble J. The Caenorhabditis elegans sex determining gene fem-3 is regulated post-transcriptionally. EMBO J. 1992 Jun;11(6):2303–2310. doi: 10.1002/j.1460-2075.1992.tb05289.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ardlie K. G. Putting the brake on drive: meiotic drive of t haplotypes in natural populations of mice. Trends Genet. 1998 May;14(5):189–193. doi: 10.1016/s0168-9525(98)01455-3. [DOI] [PubMed] [Google Scholar]
  3. Bianchi N. O., de la Chapelle A., Vidal-Rioja L., Merani S. The sex-determining zinc finger sequences in XY females of Akodon azarae (Rodentia, Cricetidae). Cytogenet Cell Genet. 1989;52(3-4):162–166. doi: 10.1159/000132869. [DOI] [PubMed] [Google Scholar]
  4. Burgoyne P. S. Mammalian sex determination: thumbs down for zinc finger? Nature. 1989 Dec 21;342(6252):860–862. doi: 10.1038/342860a0. [DOI] [PubMed] [Google Scholar]
  5. Cline T. W. The Drosophila sex determination signal: how do flies count to two? Trends Genet. 1993 Nov;9(11):385–390. doi: 10.1016/0168-9525(93)90138-8. [DOI] [PubMed] [Google Scholar]
  6. Cosmides L. M., Tooby J. Cytoplasmic inheritance and intragenomic conflict. J Theor Biol. 1981 Mar 7;89(1):83–129. doi: 10.1016/0022-5193(81)90181-8. [DOI] [PubMed] [Google Scholar]
  7. Dallas J. F., Dod B., Boursot P., Prager E. M., Bonhomme F. Population subdivision and gene flow in Danish house mice. Mol Ecol. 1995 Jun;4(3):311–320. doi: 10.1111/j.1365-294x.1995.tb00224.x. [DOI] [PubMed] [Google Scholar]
  8. Eberhard W. G. Evolutionary consequences of intracellular organelle competition. Q Rev Biol. 1980 Sep;55(3):231–249. doi: 10.1086/411855. [DOI] [PubMed] [Google Scholar]
  9. Foster J. W., Dominguez-Steglich M. A., Guioli S., Kwok C., Weller P. A., Stevanović M., Weissenbach J., Mansour S., Young I. D., Goodfellow P. N. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature. 1994 Dec 8;372(6506):525–530. doi: 10.1038/372525a0. [DOI] [PubMed] [Google Scholar]
  10. Foster J. W., Graves J. A. An SRY-related sequence on the marsupial X chromosome: implications for the evolution of the mammalian testis-determining gene. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1927–1931. doi: 10.1073/pnas.91.5.1927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gerbi S. A. Unusual chromosome movements in sciarid flies. Results Probl Cell Differ. 1986;13:71–104. doi: 10.1007/978-3-540-39838-7_2. [DOI] [PubMed] [Google Scholar]
  12. Haig D. Genetic conflicts in human pregnancy. Q Rev Biol. 1993 Dec;68(4):495–532. doi: 10.1086/418300. [DOI] [PubMed] [Google Scholar]
  13. Hamilton W. D. Extraordinary sex ratios. A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. Science. 1967 Apr 28;156(3774):477–488. doi: 10.1126/science.156.3774.477. [DOI] [PubMed] [Google Scholar]
  14. Hurst L. D. Embryonic growth and the evolution of the mammalian Y chromosome. I. The Y as an attractor for selfish growth factors. Heredity (Edinb) 1994 Sep;73(Pt 3):223–232. doi: 10.1038/hdy.1994.127. [DOI] [PubMed] [Google Scholar]
  15. Inoue H., Hiroyoshi T. A Maternal-Effect Sex-Transformation Mutant of the Housefly, MUSCA DOMESTICA L. Genetics. 1986 Mar;112(3):469–482. doi: 10.1093/genetics/112.3.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Janzen F. J., Paukstis G. L. Environmental sex determination in reptiles: ecology, evolution, and experimental design. Q Rev Biol. 1991 Jun;66(2):149–179. doi: 10.1086/417143. [DOI] [PubMed] [Google Scholar]
  17. Lau Y. F., Yang-Feng T. L., Elder B., Fredga K., Wiberg U. H. Unusual distribution of Zfy and Zfx sequences on the sex chromosomes of the wood lemming, a species exhibiting XY sex reversal. Cytogenet Cell Genet. 1992;60(1):48–54. doi: 10.1159/000133294. [DOI] [PubMed] [Google Scholar]
  18. McElreavey K., Vilain E., Abbas N., Herskowitz I., Fellous M. A regulatory cascade hypothesis for mammalian sex determination: SRY represses a negative regulator of male development. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3368–3372. doi: 10.1073/pnas.90.8.3368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. McVean G., Hurst L. D. Genetic conflicts and the paradox of sex determination: three paths to the evolution of female intersexuality in a mammal. J Theor Biol. 1996 Apr 7;179(3):199–211. doi: 10.1006/jtbi.1996.0061. [DOI] [PubMed] [Google Scholar]
  20. Morais da Silva S., Hacker A., Harley V., Goodfellow P., Swain A., Lovell-Badge R. Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat Genet. 1996 Sep;14(1):62–68. doi: 10.1038/ng0996-62. [DOI] [PubMed] [Google Scholar]
  21. Nagamine C. M., Shiroishi T., Miyashita N., Tsuchiya K., Ikeda H., Takao N., Wu X. L., Jin M. L., Wang F. S., Kryukov A. P. Distribution of the molossinus allele of Sry, the testis-determining gene, in wild mice. Mol Biol Evol. 1994 Nov;11(6):864–874. doi: 10.1093/oxfordjournals.molbev.a040169. [DOI] [PubMed] [Google Scholar]
  22. Pask A., Toder R., Wilcox S. A., Camerino G., Graves J. A. The candidate sex-reversing DAX1 gene is autosomal in marsupials: implications for the evolution of sex determination in mammals. Genomics. 1997 May 1;41(3):422–426. doi: 10.1006/geno.1997.4651. [DOI] [PubMed] [Google Scholar]
  23. Schmidt R., Hediger M., Nöthiger R., Dübendorfer A. The mutation masculinizer (man) defines a sex-determining gene with maternal and zygotic functions in Musca domestica L. Genetics. 1997 Jan;145(1):173–183. doi: 10.1093/genetics/145.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Steinmann-Zwicky M., Amrein H., Nöthiger R. Genetic control of sex determination in Drosophila. Adv Genet. 1990;27:189–237. doi: 10.1016/s0065-2660(08)60026-7. [DOI] [PubMed] [Google Scholar]
  25. Swain A., Narvaez V., Burgoyne P., Camerino G., Lovell-Badge R. Dax1 antagonizes Sry action in mammalian sex determination. Nature. 1998 Feb 19;391(6669):761–767. doi: 10.1038/35799. [DOI] [PubMed] [Google Scholar]
  26. Taylor P. D., Bulmer M. G. Local male competition and the sex ratio. J Theor Biol. 1980 Oct 7;86(3):409–419. doi: 10.1016/0022-5193(80)90342-2. [DOI] [PubMed] [Google Scholar]
  27. Trivers R. L., Hare H. Haploidploidy and the evolution of the social insect. Science. 1976 Jan 23;191(4224):249–263. doi: 10.1126/science.1108197. [DOI] [PubMed] [Google Scholar]
  28. Tucker P. K., Lundrigan B. L. Rapid evolution of the sex determining locus in Old World mice and rats. Nature. 1993 Aug 19;364(6439):715–717. doi: 10.1038/364715a0. [DOI] [PubMed] [Google Scholar]
  29. Uyenoyama M. K., Bengtsson B. O. Towards a genetic theory for the evolution of the sex ratio. III. Parental and sibling control of brood investment ratio under partial sib-mating. Theor Popul Biol. 1982 Aug;22(1):43–68. doi: 10.1016/0040-5809(82)90035-1. [DOI] [PubMed] [Google Scholar]
  30. Wagner T., Wirth J., Meyer J., Zabel B., Held M., Zimmer J., Pasantes J., Bricarelli F. D., Keutel J., Hustert E. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell. 1994 Dec 16;79(6):1111–1120. doi: 10.1016/0092-8674(94)90041-8. [DOI] [PubMed] [Google Scholar]
  31. Whitfield L. S., Lovell-Badge R., Goodfellow P. N. Rapid sequence evolution of the mammalian sex-determining gene SRY. Nature. 1993 Aug 19;364(6439):713–715. doi: 10.1038/364713a0. [DOI] [PubMed] [Google Scholar]

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