• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Aug 2003; 164(4): 1383–1397.
PMCID: PMC1462656

Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. I. Differential accumulation of hybrid male sterility effects on the X and autosomes.

Abstract

The genetic basis of hybrid incompatibility in crosses between Drosophila mauritiana and D. simulans was investigated to gain insight into the evolutionary mechanisms of speciation. In this study, segments of the D. mauritiana third chromosome were introgressed into a D. simulans genetic background and tested as homozygotes for viability, male fertility, and female fertility. The entire third chromosome was covered with partially overlapping segments. Many segments were male sterile, while none were female sterile or lethal, confirming previous reports of the rapid evolution of hybrid male sterility (HMS). A statistical model was developed to quantify the HMS accumulation. In comparison with previous work on the X chromosome, we estimate that the X has approximately 2.5 times the density of HMS factors as the autosomes. We also estimate that the whole genome contains approximately 15 HMS "equivalents"-i.e., 15 times the minimum number of incompatibility factors necessary to cause complete sterility. Although some caveats for the quantitative estimate of a 2.5-fold density difference are described, this study supports the notion that the X chromosome plays a special role in the evolution of reproductive isolation. Possible mechanisms of a "large X" effect include selective fixation of new mutations that are recessive or partially recessive and the evolution of sex-ratio distortion systems.

Full Text

The Full Text of this article is available as a PDF (265K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Bauer VL, Aquadro CF. Rates of DNA sequence evolution are not sex-biased in Drosophila melanogaster and D. simulans. Mol Biol Evol. 1997 Dec;14(12):1252–1257. [PubMed]
  • Betancourt Andrea J, Presgraves Daven C, Swanson Willie J. A test for faster X evolution in Drosophila. Mol Biol Evol. 2002 Oct;19(10):1816–1819. [PubMed]
  • Cabot EL, Davis AW, Johnson NA, Wu CI. Genetics of reproductive isolation in the Drosophila simulans clade: complex epistasis underlying hybrid male sterility. Genetics. 1994 May;137(1):175–189. [PMC free article] [PubMed]
  • Kyriacou CP, Hall JC. Interspecific genetic control of courtship song production and reception in Drosophila. Science. 1986 Apr 25;232(4749):494–497. [PubMed]
  • Coyne JA, Charlesworth B. Location of an X-linked factor causing sterility in male hybrids of Drosophila simulans and D. mauritiana. Heredity (Edinb) 1986 Oct;57(Pt 2):243–246. [PubMed]
  • Coyne JA, 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. [PubMed]
  • Liu J, Mercer JM, Stam LF, Gibson GC, Zeng ZB, Laurie CC. Genetic analysis of a morphological shape difference in the male genitalia of Drosophila simulans and D. mauritiana. Genetics. 1996 Apr;142(4):1129–1145. [PMC free article] [PubMed]
  • Davis AW, Wu CI. The broom of the sorcerer's apprentice: the fine structure of a chromosomal region causing reproductive isolation between two sibling species of Drosophila. Genetics. 1996 Jul;143(3):1287–1298. [PMC free article] [PubMed]
  • Makova Kateryna D, Li Wen-Hsiung. Strong male-driven evolution of DNA sequences in humans and apes. Nature. 2002 Apr 11;416(6881):624–626. [PubMed]
  • Maside XR, Barral JP, Naveira HF. Hidden effects of X chromosome introgressions on spermatogenesis in Drosophila simulans x D. mauritiana hybrids unveiled by interactions among minor genetic factors. Genetics. 1998 Oct;150(2):745–754. [PMC free article] [PubMed]
  • Davis AW, Noonburg EG, Wu CI. Evidence for complex genic interactions between conspecific chromosomes underlying hybrid female sterility in the Drosophila simulans clade. Genetics. 1994 May;137(1):191–199. [PMC free article] [PubMed]
  • Mukai T, Chigusa SI, Mettler LE, Crow JF. Mutation rate and dominance of genes affecting viability in Drosophila melanogaster. Genetics. 1972 Oct;72(2):335–355. [PMC free article] [PubMed]
  • Dermitzakis ET, Masly JP, Waldrip HM, Clark AG. Non-Mendelian segregation of sex chromosomes in heterospecific Drosophila males. Genetics. 2000 Feb;154(2):687–694. [PMC free article] [PubMed]
  • Naisbit Russell E, Jiggins Chris D, Linares Mauricio, Salazar Camilo, Mallet James. Hybrid sterility, Haldane's rule and speciation in Heliconius cydno and H. melpomene. Genetics. 2002 Aug;161(4):1517–1526. [PMC free article] [PubMed]
  • Orr HA, Betancourt AJ. Haldane's sieve and adaptation from the standing genetic variation. Genetics. 2001 Feb;157(2):875–884. [PMC free article] [PubMed]
  • Ellegren H, Fridolfsson AK. Male-driven evolution of DNA sequences in birds. Nat Genet. 1997 Oct;17(2):182–184. [PubMed]
  • Orr HA, Presgraves DC. Speciation by postzygotic isolation: forces, genes and molecules. Bioessays. 2000 Dec;22(12):1085–1094. [PubMed]
  • Ewing AW. The genetic basis of sound production in Drosophila pseudoobscura and D. persimilis. Anim Behav. 1969 Aug;17(3):555–560. [PubMed]
  • Parisi Michael, Nuttall Rachel, Naiman Daniel, Bouffard Gerard, Malley James, Andrews Justen, Eastman Scott, Oliver Brian. Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science. 2003 Jan 31;299(5607):697–700. [PMC free article] [PubMed]
  • Perez DE, Wu CI. Further characterization of the Odysseus locus of hybrid sterility in Drosophila: one gene is not enough. Genetics. 1995 May;140(1):201–206. [PMC free article] [PubMed]
  • Fry JD, Keightley PD, Heinsohn SL, Nuzhdin SV. New estimates of the rates and effects of mildly deleterious mutation in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1999 Jan 19;96(2):574–579. [PMC free article] [PubMed]
  • Perez DE, Wu CI, Johnson NA, Wu ML. Genetics of reproductive isolation in the Drosophila simulans clade: DNA marker-assisted mapping and characterization of a hybrid-male sterility gene, Odysseus (Ods). Genetics. 1993 May;134(1):261–275. [PMC free article] [PubMed]
  • Presgraves Daven C. Patterns of postzygotic isolation in Lepidoptera. Evolution. 2002 Jun;56(6):1168–1183. [PubMed]
  • Hey J, Kliman RM. Population genetics and phylogenetics of DNA sequence variation at multiple loci within the Drosophila melanogaster species complex. Mol Biol Evol. 1993 Jul;10(4):804–822. [PubMed]
  • Hollocher H, Wu CI. The genetics of reproductive isolation in the Drosophila simulans clade: X vs. autosomal effects and male vs. female effects. Genetics. 1996 Jul;143(3):1243–1255. [PMC free article] [PubMed]
  • Saiki RK, Bugawan TL, Horn GT, Mullis KB, Erlich HA. Analysis of enzymatically amplified beta-globin and HLA-DQ alpha DNA with allele-specific oligonucleotide probes. Nature. 1986 Nov 13;324(6093):163–166. [PubMed]
  • Jiggins CD, Linares M, Naisbit RE, Salazar C, Yang ZH, Mallet J. Sex-linked hybrid sterility in a butterfly. Evolution. 2001 Aug;55(8):1631–1638. [PubMed]
  • Shimmin LC, Chang BH, Li WH. Male-driven evolution of DNA sequences. Nature. 1993 Apr 22;362(6422):745–747. [PubMed]
  • Simmons MJ, Crow JF. Mutations affecting fitness in Drosophila populations. Annu Rev Genet. 1977;11:49–78. [PubMed]
  • Keightley PD. Nature of deleterious mutation load in Drosophila. Genetics. 1996 Dec;144(4):1993–1999. [PMC free article] [PubMed]
  • Keightley PD. Inference of genome-wide mutation rates and distributions of mutation effects for fitness traits: a simulation study. Genetics. 1998 Nov;150(3):1283–1293. [PMC free article] [PubMed]
  • Tan CC. Genetics of Sexual Isolation between DROSOPHILA PSEUDOOBSCURA and DROSOPHILA PERSIMILIS. Genetics. 1946 Nov;31(6):558–573. [PMC free article] [PubMed]
  • Tao Y, Hartl DL, Laurie CC. Sex-ratio segregation distortion associated with reproductive isolation in Drosophila. Proc Natl Acad Sci U S A. 2001 Nov 6;98(23):13183–13188. [PMC free article] [PubMed]
  • Tao Yun, Zeng Zhao-Bang, Li Jian, Hartl Daniel L, Laurie Cathy C. Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. II. Mapping hybrid male sterility loci on the third chromosome. Genetics. 2003 Aug;164(4):1399–1418. [PMC free article] [PubMed]
  • True JR, Mercer JM, Laurie CC. Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics. 1996 Feb;142(2):507–523. [PMC free article] [PubMed]
  • True JR, Weir BS, Laurie CC. A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. Genetics. 1996 Mar;142(3):819–837. [PMC free article] [PubMed]
  • Zeng ZB, Liu J, Stam LF, Kao CH, Mercer JM, Laurie CC. Genetic architecture of a morphological shape difference between two Drosophila species. Genetics. 2000 Jan;154(1):299–310. [PMC free article] [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links