• 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. Mar 2003; 163(3): 955–972.
PMCID: PMC1462496

A fine-scale genetic analysis of hybrid incompatibilities in Drosophila.


The sterility and inviability of species hybrids is thought to evolve by the accumulation of genes that cause generally recessive, incompatible epistatic interactions between species. Most analyses of the loci involved in such hybrid incompatibilities have suffered from low genetic resolution. Here I present a fine-resolution genetic screen that allows systematic counting, mapping, and characterizing of a large number of hybrid incompatibility loci in a model genetic system. Using small autosomal deletions from D. melanogaster and a hybrid rescue mutation from D. simulans, I measured the viability of hybrid males that are simultaneously hemizygous for a small region of the D. simulans autosomal genome and hemizygous for the D. melanogaster X chromosome. These hybrid males are exposed to the full effects of any recessive-recessive epistatic incompatibilities present in these regions. A screen of approximately 70% of the D. simulans autosomal genome reveals 20 hybrid-lethal and 20 hybrid-semilethal regions that are incompatible with the D. melanogaster X. In further crosses, I confirm the epistatic nature of hybrid lethality by showing that all of the incompatibilities are rescued when the D. melanogaster X is replaced with a D. simulans X. Combined with information from previous studies, these results show that the number of recessive incompatibilities is approximately eightfold larger than the number of dominant ones. Finally, I estimate that a total of approximately 191 hybrid-lethal incompatibilities separate D. melanogaster and D. simulans, indicating extensive functional divergence between these species' genomes.

Full Text

The Full Text of this article is available as a PDF (230K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Begun DJ, Whitley P, Todd BL, Waldrip-Dail HM, Clark AG. Molecular population genetics of male accessory gland proteins in Drosophila. Genetics. 2000 Dec;156(4):1879–1888. [PMC free article] [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]
  • Carvajal AR, Gandarela MR, Naveira HF. A three-locus system of interspecific incompatibility underlies male inviability in hybrids between Drosophila buzzatii and D. koepferae. Genetica. 1996 Jul;98(1):1–19. [PubMed]
  • Coyne JA, Simeonidis S, Rooney P. Relative paucity of genes causing inviability in hybrids between Drosophila melanogaster and D. simulans. Genetics. 1998 Nov;150(3):1091–1103. [PMC free article] [PubMed]
  • Davis AW, Roote J, Morley T, Sawamura K, Herrmann S, Ashburner M. Rescue of hybrid sterility in crosses between D. melanogaster and D. simulans. Nature. 1996 Mar 14;380(6570):157–159. [PubMed]
  • Deák P, Omar MM, Saunders RD, Pál M, Komonyi O, Szidonya J, Maróy P, Zhang Y, Ashburner M, Benos P, et al. P-element insertion alleles of essential genes on the third chromosome of Drosophila melanogaster: correlation of physical and cytogenetic maps in chromosomal region 86E-87F. Genetics. 1997 Dec;147(4):1697–1722. [PMC free article] [PubMed]
  • Granadino B, Penalva LO, Sánchez L. Indirect evidence of alteration in the expression of the rDNA genes in interspecific hybrids between Drosophila melanogaster and Drosophila simulans. Mol Gen Genet. 1996 Jan 15;250(1):89–96. [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]
  • Hutter P, Roote J, Ashburner M. A genetic basis for the inviability of hybrids between sibling species of Drosophila. Genetics. 1990 Apr;124(4):909–920. [PMC free article] [PubMed]
  • Arbeitman Michelle N, Furlong Eileen E M, Imam Farhad, Johnson Eric, Null Brian H, Baker Bruce S, Krasnow Mark A, Scott Matthew P, Davis Ronald W, White Kevin P. Gene expression during the life cycle of Drosophila melanogaster. Science. 2002 Sep 27;297(5590):2270–2275. [PubMed]
  • Barbash DA, Roote J, Ashburner M. The Drosophila melanogaster hybrid male rescue gene causes inviability in male and female species hybrids. Genetics. 2000 Apr;154(4):1747–1771. [PMC free article] [PubMed]
  • Turelli M, Orr HA. Dominance, epistasis and the genetics of postzygotic isolation. Genetics. 2000 Apr;154(4):1663–1679. [PMC free article] [PubMed]
  • Orr HA. Dobzhansky, Bateson, and the genetics of speciation. Genetics. 1996 Dec;144(4):1331–1335. [PMC free article] [PubMed]
  • Orr HA, Irving S. Genetic analysis of the hybrid male rescue locus of Drosophila. Genetics. 2000 May;155(1):225–231. [PMC free article] [PubMed]
  • Orr HA, Presgraves DC. Speciation by postzygotic isolation: forces, genes and molecules. Bioessays. 2000 Dec;22(12):1085–1094. [PubMed]
  • Orr HA, Turelli M. The evolution of postzygotic isolation: accumulating Dobzhansky-Muller incompatibilities. Evolution. 2001 Jun;55(6):1085–1094. [PubMed]
  • Presgraves Daven C. Patterns of postzygotic isolation in Lepidoptera. Evolution. 2002 Jun;56(6):1168–1183. [PubMed]
  • Presgraves DC, Orr HA. Haldane's rule in taxa lacking a hemizygous X. Science. 1998 Oct 30;282(5390):952–954. [PubMed]
  • Price Trevor D, Bouvier Michelle M. The evolution of F1 postzygotic incompatibilities in birds. Evolution. 2002 Oct;56(10):2083–2089. [PubMed]
  • Sawamura K, Watanabe TK, Yamamoto MT. Hybrid lethal systems in the Drosophila melanogaster species complex. Genetica. 1993;88(2-3):175–185. [PubMed]
  • Sawamura K, Davis AW, Wu CI. Genetic analysis of speciation by means of introgression into Drosophila melanogaster. Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2652–2655. [PMC free article] [PubMed]
  • Simmons MJ, Crow JF. Mutations affecting fitness in Drosophila populations. Annu Rev Genet. 1977;11:49–78. [PubMed]
  • Spradling AC, Stern D, Beaton A, Rhem EJ, Laverty T, Mozden N, Misra S, Rubin GM. The Berkeley Drosophila Genome Project gene disruption project: Single P-element insertions mutating 25% of vital Drosophila genes. Genetics. 1999 Sep;153(1):135–177. [PMC free article] [PubMed]
  • STEBBINS GL. The inviability, weakness, and sterility of interspecific hybrids. Adv Genet. 1958;9:147–215. [PubMed]
  • Swanson WJ, Clark AG, Waldrip-Dail HM, Wolfner MF, Aquadro CF. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc Natl Acad Sci U S A. 2001 Jun 19;98(13):7375–7379. [PMC free article] [PubMed]
  • Török T, Tick G, Alvarado M, Kiss I. P-lacW insertional mutagenesis on the second chromosome of Drosophila melanogaster: isolation of lethals with different overgrowth phenotypes. Genetics. 1993 Sep;135(1):71–80. [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]
  • Turelli M, Orr HA. The dominance theory of Haldane's rule. Genetics. 1995 May;140(1):389–402. [PMC free article] [PubMed]

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


Related citations in PubMed

Cited by other articles in PMC

See all...


Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...