Abstract
Most sexually reproducing species have sexual proportions around 1:1. This major biological phenomenon remained unexplained until 1930, when FISHER proposed that it results from a mechanism of natural selection. Here we report the first experimental test of his model that obeys all its assumptions. We used a naturally occurring X-Y meiotic drive system--the sex-ratio trait of Drosophila mediopunctat--to generate female-biased experimental populations. As predicted by FISHER, these populations evolved toward equal sex proportions due to natural selection, by accumulation of autosomal alleles that direct the parental reproductive effort toward the rare sex. Classical Fisherian evolution is a rather slow mechanism: despite a very large amount of genetic variability, the experimental populations evolved from 16% of males to 32% of males in 49 generations and would take 330 generations (29 years) to reach 49%. This slowness has important implications for species potentially endangered by skewed sexual proportions, such as reptiles with temperature sex determination.
Full Text
The Full Text of this article is available as a PDF (142.8 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Carvalho A. B., Vaz S. C., Klaczko L. B. Polymorphism for Y-linked suppressors of sex-ratio in two natural populations of Drosophila mediopunctata. Genetics. 1997 Jul;146(3):891–902. doi: 10.1093/genetics/146.3.891. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cazemajor M., Landré C., Montchamp-Moreau C. The sex-ratio trait in Drosophila simulans: genetic analysis of distortion and suppression. Genetics. 1997 Oct;147(2):635–642. doi: 10.1093/genetics/147.2.635. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Conover D. O., Van Voorhees D. A. Evolution of a balanced sex ratio by frequency-dependent selection in a fish. Science. 1990 Dec 14;250(4987):1556–1558. doi: 10.1126/science.250.4987.1556. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Gimelfarb A., Willis J. H. Linearity Versus nonlinearity of offspring-parent regression: an experimental study of Drosophila melanogaster. Genetics. 1994 Oct;138(2):343–352. doi: 10.1093/genetics/138.2.343. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Janzen F. J. Climate change and temperature-dependent sex determination in reptiles. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7487–7490. doi: 10.1073/pnas.91.16.7487. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Lyttle T. W. Experimental population genetics of meiotic drive systems. I. Pseudo-Y chromosomal drive as a means of eliminating cage populations of Drosophila melanogaster. Genetics. 1977 Jun;86(2 Pt 1):413–445. [PMC free article] [PubMed] [Google Scholar]
- Lyttle T. W. Experimental population genetics of meiotic drive systems. III. Neutralization of sex-ratio distortion in Drosophila through sex-chromosome aneuploidy. Genetics. 1981 Jun;98(2):317–334. doi: 10.1093/genetics/98.2.317. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nur U. The expected changes in the frequency of alleles affecting the sex ratio. Theor Popul Biol. 1974 Apr;5(2):143–147. doi: 10.1016/0040-5809(74)90036-7. [DOI] [PubMed] [Google Scholar]
- Orzack S. H., Gladstone J. Quantitative genetics of sex ratio traits in the parasitic wasp, Nasonia vitripennis. Genetics. 1994 May;137(1):211–220. doi: 10.1093/genetics/137.1.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Riska B., Prout T., Turelli M. Laboratory estimates of heritabilities and genetic correlations in nature. Genetics. 1989 Dec;123(4):865–871. doi: 10.1093/genetics/123.4.865. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shaw R F. The Theoretical Genetics of the Sex Ratio. Genetics. 1958 Mar;43(2):149–163. doi: 10.1093/genetics/43.2.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Sturtevant A H. Genetic Studies on DROSOPHILA SIMULANS. I. Introduction. Hybrids with DROSOPHILA MELANOGASTER. Genetics. 1920 Sep;5(5):488–500. doi: 10.1093/genetics/5.5.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Uyenoyama M. K., Bengtsson B. O. Towards a genetic theory for the evolution of the sex ratio. Genetics. 1979 Nov;93(3):721–736. doi: 10.1093/genetics/93.3.721. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Williams G. C. The question of adaptive sex ratio in outcrossed vertebrates. Proc R Soc Lond B Biol Sci. 1979 Sep 21;205(1161):567–580. doi: 10.1098/rspb.1979.0085. [DOI] [PubMed] [Google Scholar]
- de Carvalho A. B., Klaczko L. B. Age and sex-ratio expression in Drosophila mediopunctata. Genetica. 1992;87(2):107–111. doi: 10.1007/BF00121000. [DOI] [PubMed] [Google Scholar]
- de Carvalho A. B., Klaczko L. B. Autosomal suppressors of sex-ratio in Drosophila mediopunctata. Heredity (Edinb) 1993 Nov;71(Pt 5):546–551. doi: 10.1038/hdy.1993.174. [DOI] [PubMed] [Google Scholar]
- de Carvalho A. B., Klaczko L. B. Y-linked suppressors of the sex-ratio trait in Drosophila mediopunctata. Heredity (Edinb) 1994 Dec;73(Pt 6):573–579. doi: 10.1038/hdy.1994.164. [DOI] [PubMed] [Google Scholar]