Skip to main content
Genetics logoLink to Genetics
. 1991 Aug;128(4):841–858. doi: 10.1093/genetics/128.4.841

Causes of Sex Ratio Bias May Account for Unisexual Sterility in Hybrids: A New Explanation of Haldane's Rule and Related Phenomena

L D Hurst 1, A Pomiankowski 1
PMCID: PMC1204557  PMID: 1916248

Abstract

Unisexual hybrid disruption can be accounted for by interactions between sex ratio distorters which have diverged in the species of the hybrid cross. One class of unisexual hybrid disruption is described by Haldane's rule, namely that the sex which is absent, inviable or sterile is the heterogametic sex. This effect is mainly due to incompatibility between X and Y chromosomes. We propose that this incompatibility is due to a mutual imbalance between meiotic drive genes, which are more likely to evolve on sex chromosomes than autosomes. The incidences of taxa with sex chromosome drive closely matches those where Haldane's rule applies: Aves, Mammalia, Lepidoptera and Diptera. We predict that Haldane's rule is not universal but is correct for taxa with sex chromosome meiotic drive. A second class of hybrid disruption affects the male of the species regardless of which sex is heterogametic. Typically the genes responsible for this form of disruption are cytoplasmic. These instances are accounted for by the release from suppression of cytoplasmic sex ratio distorters when in a novel nuclear cytotype. Due to the exclusively maternal transmission of cytoplasm, cytoplasmic sex ratio distorters cause only female-biased sex ratios. This asymmetry explains why hybrid disruption is limited to the male.

Full Text

The Full Text of this article is available as a PDF (1.9 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Artzt K., Shin H. S., Bennett D. Gene mapping within the T/t complex of the mouse. II. Anomalous position of the H-2 complex in t haplotypes. Cell. 1982 Mar;28(3):471–476. doi: 10.1016/0092-8674(82)90201-x. [DOI] [PubMed] [Google Scholar]
  2. Charlesworth B., Hartl D. L. Population Dynamics of the Segregation Distorter Polymorphism of DROSOPHILA MELANOGASTER. Genetics. 1978 May;89(1):171–192. doi: 10.1093/genetics/89.1.171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cobbs G. Modifier Genes of the Sex Ratio Trait in Drosophila pseudoobscura. Genetics. 1987 Jun;116(2):275–283. doi: 10.1093/genetics/116.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Coyne J. A., Charlesworth B. Genetic analysis of X-linked sterility in hybrids between three sibling species of Drosophila. Heredity (Edinb) 1989 Feb;62(Pt 1):97–106. doi: 10.1038/hdy.1989.13. [DOI] [PubMed] [Google Scholar]
  5. Curtsinger J. W. Components of selection in X chromosome lines of Drosophila melanogaster: sex ratio modification by meiotic drive and viability selection. Genetics. 1984 Dec;108(4):941–952. doi: 10.1093/genetics/108.4.941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dunn L. C., Bennett D. A new case of transmission ratio distortion in the house mouse. Proc Natl Acad Sci U S A. 1968 Oct;61(2):570–573. doi: 10.1073/pnas.61.2.570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Eshel I. Selection of sex-ratio and the evolution of sex-determination. Heredity (Edinb) 1975 Jun;34(3):351–361. doi: 10.1038/hdy.1975.44. [DOI] [PubMed] [Google Scholar]
  8. Faulhaber S. H. An abnormal sex ratio in Drosophila simulans. Genetics. 1967 May;56(1):189–213. doi: 10.1093/genetics/56.1.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Forejt J., Iványi P. Genetic studies on male sterility of hybrids between laboratory and wild mice (Mus musculus L.). Genet Res. 1974 Oct;24(2):189–206. doi: 10.1017/s0016672300015214. [DOI] [PubMed] [Google Scholar]
  10. Gall J. C., Jr, Stern A. M., Cohen M. M., Adams M. S., Davidson R. T. Holt-Oram syndrome: clinical and genetic study of a large family. Am J Hum Genet. 1966 Mar;18(2):187–200. [PMC free article] [PubMed] [Google Scholar]
  11. Gershenson S. A New Sex-Ratio Abnormality in DROSOPHILA OBSCURA. Genetics. 1928 Nov;13(6):488–507. doi: 10.1093/genetics/13.6.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Golic K. G. Examination of a mutable system affecting the components of the segregation distorter meiotic drive system of Drosophila melanogaster. Genetics. 1990 May;125(1):51–76. doi: 10.1093/genetics/125.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gropp A., Winking H., Frank F., Noack G., Fredga K. Sex-chromosome aberrations in wood lemmings (Myopus schisticolor). Cytogenet Cell Genet. 1976;17(6):343–358. doi: 10.1159/000130737. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Hartl D. L. Complementation analysis of male fertility among the segregation distorter chromosomes of Drosophila melanogaster. Genetics. 1973 Apr;73(4):613–629. doi: 10.1093/genetics/73.4.613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hartl D. L. Genetic dissection of segregation distortion. I. Suicide combinations of SD genes. Genetics. 1974 Mar;76(3):477–486. doi: 10.1093/genetics/76.3.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hartl D. L., Hiraizumi Y., Crow J. F. Evidence for sperm dysfunction as the mechanism of segregation distortion in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1967 Dec;58(6):2240–2245. doi: 10.1073/pnas.58.6.2240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Herrmann B., Bućan M., Mains P. E., Frischauf A. M., Silver L. M., Lehrach H. Genetic analysis of the proximal portion of the mouse t complex: evidence for a second inversion within t haplotypes. Cell. 1986 Feb 14;44(3):469–476. doi: 10.1016/0092-8674(86)90468-x. [DOI] [PubMed] [Google Scholar]
  19. Heuch I. Maintenance of butterfly populations with all-female broods under recurrent extinction and recolonization. J Theor Biol. 1978 Nov 7;75(1):115–122. doi: 10.1016/0022-5193(78)90205-9. [DOI] [PubMed] [Google Scholar]
  20. Ikeda H. The cytoplasmically-inherited "sex-ratio" condition in natural and experimental populations of Drosophila bifasciata. Genetics. 1970 Jun;65(2):311–333. doi: 10.1093/genetics/65.2.311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. James A. C., Jaenike J. "Sex ratio" meiotic drive in Drosophila testacea. Genetics. 1990 Nov;126(3):651–656. doi: 10.1093/genetics/126.3.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kaufman M. H. Non-random segregation during mammalian oogenesis. Nature. 1972 Aug 25;238(5365):465–466. doi: 10.1038/238465a0. [DOI] [PubMed] [Google Scholar]
  23. Kettaneh N. P., Hartl D. L. Ultrastructural analysis of spermiogenesis in segregation distorter males of Drosophila melanogaster: the homozygotes. Genetics. 1980 Nov;96(3):665–683. doi: 10.1093/genetics/96.3.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lansman R. A., Avise J. C., Huettel M. D. Critical experimental test of the possibility of "paternal leakage" of mitochondrial DNA. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1969–1971. doi: 10.1073/pnas.80.7.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lyon M. F. Male sterility of the mouse t-complex is due to homozygosity of the distorter genes. Cell. 1986 Jan 31;44(2):357–363. doi: 10.1016/0092-8674(86)90770-1. [DOI] [PubMed] [Google Scholar]
  26. Lyttle T. W. Experimental Population Genetics of Meiotic Drive Systems II. Accumulation of Genetic Modifiers of Segregation Distorter (SD) in Laboratory Populations. Genetics. 1979 Feb;91(2):339–357. doi: 10.1093/genetics/91.2.339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lyttle T. W. The effect of novel chromosome position and variable dose on the genetic behavior of the Responder (Rsp) element of the Segregation distorter (SD) system of Drosophila melanogaster. Genetics. 1989 Apr;121(4):751–763. doi: 10.1093/genetics/121.4.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. MALOGOLOWKIN C., POULSON D. F. Infective transfer of maternally inherited abnormal sex-ratio in Drosophila willistoni. Science. 1957 Jul 5;126(3262):32–32. doi: 10.1126/science.126.3262.32. [DOI] [PubMed] [Google Scholar]
  29. Malogolowkin C. Maternally Inherited "Sex-Ratio" Conditions in Drosophila Willistoni and Drosophila Paulistorum. Genetics. 1958 Mar;43(2):274–286. doi: 10.1093/genetics/43.2.274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Miyata T., Hayashida H., Kuma K., Mitsuyasu K., Yasunaga T. Male-driven molecular evolution: a model and nucleotide sequence analysis. Cold Spring Harb Symp Quant Biol. 1987;52:863–867. doi: 10.1101/sqb.1987.052.01.094. [DOI] [PubMed] [Google Scholar]
  31. Novitski E., Sandler I. ARE ALL PRODUCTS OF SPERMATOGENESIS REGULARLY FUNCTIONAL? Proc Natl Acad Sci U S A. 1957 Apr 15;43(4):318–324. doi: 10.1073/pnas.43.4.318. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. OHNO S., JAINCHILL J., STENIUS C. THE CREEPING VOLE (MICROTUS OREGONI) AS A GONOSOMIC MOSAIC. I. THE OY/XY CONSTITUTION OF THE MALE. Cytogenetics. 1963;2:232–239. doi: 10.1159/000129781. [DOI] [PubMed] [Google Scholar]
  33. Sarvetnick N., Fox H. S., Mann E., Mains P. E., Elliott R. W., Silver L. M. Nonhomologous pairing in mice heterozygous for a t haplotype can produce recombinant chromosomes with duplications and deletions. Genetics. 1986 Jul;113(3):723–734. doi: 10.1093/genetics/113.3.723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Shaw R. F., Glover R. A. Abnormal Segregation in Hereditary Renal Disease with Deafness. Am J Hum Genet. 1961 Mar;13(1 Pt 1):89–97. [PMC free article] [PubMed] [Google Scholar]
  35. Silver L. M. Mouse t haplotypes. Annu Rev Genet. 1985;19:179–208. doi: 10.1146/annurev.ge.19.120185.001143. [DOI] [PubMed] [Google Scholar]
  36. Smith D. A. Evidence for autosomal meiotic drive in the butterfly Danaus chrysippus L. Heredity (Edinb) 1976 Feb;36(1):139–142. doi: 10.1038/hdy.1976.13. [DOI] [PubMed] [Google Scholar]
  37. Stalker H D. The Genetic Systems Modifying Meiotic Drive in Drosophila Paramelanica. Genetics. 1961 Feb;46(2):177–202. doi: 10.1093/genetics/46.2.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Stouthamer R., Luck R. F., Hamilton W. D. Antibiotics cause parthenogenetic Trichogramma (Hymenoptera/Trichogrammatidae) to revert to sex. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2424–2427. doi: 10.1073/pnas.87.7.2424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sturtevant A H, Dobzhansky T. Geographical Distribution and Cytology of "Sex Ratio" in Drosophila Pseudoobscura and Related Species. Genetics. 1936 Jul;21(4):473–490. doi: 10.1093/genetics/21.4.473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sweeny T. L., Barr A. R. Sex Ratio Distortion Caused by Meiotic Drive in a Mosquito, Culex pipiens L. Genetics. 1978 Mar;88(3):427–446. doi: 10.1093/genetics/88.3.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Temin R. G., Marthas M. Factors Influencing the Effect of Segregation Distortion in Natural Populations of DROSOPHILA MELANOGASTER. Genetics. 1984 Jul;107(3):375–393. doi: 10.1093/genetics/107.3.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Thomson G. J., Feldman M. W. Population genetics of modifiers of meiotic drive. III. Equilibrium analysis of a general model for the genetic control of segregation distortion. Theor Popul Biol. 1976 Aug;10(1):10–25. doi: 10.1016/0040-5809(76)90003-4. [DOI] [PubMed] [Google Scholar]
  43. Thomson G. J., Feldman M. W. Population genetics of modifiers of meiotic drive: IV. On the evolution of sex-ratio distortion. Theor Popul Biol. 1975 Oct;8(2):202–211. doi: 10.1016/0040-5809(75)90032-5. [DOI] [PubMed] [Google Scholar]
  44. Uyenoyama M. K., Feldman M. W. The genetics of sex ratio distortion by cytoplasmic infection under maternal and contagious transmission: an epidemiological study. Theor Popul Biol. 1978 Dec;14(3):471–497. doi: 10.1016/0040-5809(78)90019-9. [DOI] [PubMed] [Google Scholar]
  45. Voelker R. A. Preliminary characterization of "sex ratio" and rediscovery and reinterpretation of "male sex ratio" in Drosophila affinis. Genetics. 1972 Aug;71(4):597–606. doi: 10.1093/genetics/71.4.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Wagoner D. E. Presence of male determining factors found on three autosomes in the house fly, Musca domestica. Nature. 1969 Jul 12;223(5202):187–188. doi: 10.1038/223187a0. [DOI] [PubMed] [Google Scholar]
  47. Wu C. I., Beckenbach A. T. Evidence for Extensive Genetic Differentiation between the Sex-Ratio and the Standard Arrangement of DROSOPHILA PSEUDOOBSCURA and D. PERSIMILIS and Identification of Hybrid Sterility Factors. Genetics. 1983 Sep;105(1):71–86. doi: 10.1093/genetics/105.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wu C. I. Virility Deficiency and the Sex-Ratio Trait in DROSOPHILA PSEUDOOBSCURA. I. Sperm Displacement and Sexual Selection. Genetics. 1983 Nov;105(3):651–662. doi: 10.1093/genetics/105.3.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Zimmering S. Modification of Abnormal Gametic Ratios in Drosophila. I. Evidence for an Influence of Y Chromosomes and Major Autosomes on Gametic Ratios from Bar-Stone Translocation Males. Genetics. 1960 Sep;45(9):1253–1268. doi: 10.1093/genetics/45.9.1253. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES