HYBRID DYSGENESIS IN DROSOPHILA MELANOGASTER: A SYNDROME OF ABERRANT TRAITS INCLUDING MUTATION, STERILITY AND MALE RECOMBINATION

Margaret G. Kidwell ¹, James F. Kidwell ², and John A. Sved ³

¹ Division of Biology, Brown University, Providence, Rhode Island 02912
² Division of Medicine, Brown University, Providence, Rhode Island 02912
³ School of Biological Sciences, University of Sydney, N. S. W. 2006, Australia

A syndrome of associated aberrant traits is described in Drosophila melanogaster. Six of these traits, mutation, sterility, male recombination, transmission ratio distortion, chromosomal aberrations and local increases in female recombination, have previously been reported. A seventh trait, nondisjunction, is described for the first time. All of the traits we have examined are found nonreciprocally in F₁ hybrids. We present evidence that at least four of the traits are not found in nonhybrids. Therefore we have proposed the name hybrid dysgenesis to describe this syndrome.—A partition of tested strains into two types, designated P and M, was made according to the paternal or maternal contribution required to produce hybrid dysgenesis. This classification seems to hold for crosses of strains from within the United States and Australia, as well as for crosses between strains from the two countries. Strains collected recently from natural populations are typically of the P type and those having a long laboratory history are generally of the M type. However, a group of six strains collected from the wild in the 1960's are unambiguously divided equally between the P and M types. The dichotomy of this latter group raises interesting questions concerning possible implications for speciation.—Temperature often has a critical effect on the manifestation of hybrid dysgenesis. High F₁ developmental temperatures tend to increase the expression of sterility, sometimes to extreme levels. Conversely, low developmental temperatures tend to inhibit the expression of some dysgenic traits.—There are potentially important practical implications of hybrid dysgenesis for laboratory experimentation. The results suggest that care should be exercised in planning experiments involving strain crosses.

This article has been cited by other articles:

				P. A. Jensen, J. R. Stuart, M. P. Goodpaster, J. W. Goodman, and M. J. Simmons Cytotype Regulation of P Transposable Elements in Drosophila melanogaster: Repressor Polypeptides or piRNAs? Genetics, August 1, 2008; 179(4): 1785 - 1793. [Abstract] [Full Text] [PDF]

				J. Sudi, S. Zhang, G. Intrieri, X. Hao, and P. Zhang Coincidence of P-Insertion Sites and Breakpoints of Deletions Induced by Activating P Elements in Drosophila Genetics, May 1, 2008; 179(1): 227 - 235. [Abstract] [Full Text] [PDF]

				M. J. Simmons, J. B. Niemi, D.-F. Ryzek, C. Lamour, J. W. Goodman, W. Kraszkiewicz, and R. Wolff Cytotype Regulation by Telomeric P Elements in Drosophila melanogaster: Interactions With P Elements From M' Strains Genetics, August 1, 2007; 176(4): 1957 - 1966. [Abstract] [Full Text] [PDF]

				M. J. Simmons, D.-F. Ryzek, C. Lamour, J. W. Goodman, N. E. Kummer, and P. J. Merriman Cytotype Regulation by Telomeric P Elements in Drosophila melanogaster: Evidence for Involvement of an RNA Interference Gene Genetics, August 1, 2007; 176(4): 1945 - 1955. [Abstract] [Full Text] [PDF]

				E. Pomerantseva, I. Biryukova, R. Silicheva, E. Savitskaya, A. Golovnin, and P. Georgiev Transposition of Regulatory Elements by P-Element-Mediated Rearrangements in Drosophila melanogaster Genetics, April 1, 2006; 172(4): 2283 - 2291. [Abstract] [Full Text] [PDF]

				K. J. Haley, J. R. Stuart, J. D. Raymond, J. B. Niemi, and M. J. Simmons Impairment of Cytotype Regulation of P-Element Activity in Drosophila melanogaster by Mutations in the Su(var)205 Gene Genetics, October 1, 2005; 171(2): 583 - 595. [Abstract] [Full Text] [PDF]

				M. E. Clark, C. L. Anderson, J. Cande, and T. L. Karr Widespread Prevalence of Wolbachia in Laboratory Stocks and the Implications for Drosophila Research Genetics, August 1, 2005; 170(4): 1667 - 1675. [Abstract] [Full Text] [PDF]

				T. F. C. Mackay, R. F. Lyman, and F. Lawrence Polygenic Mutation in Drosophila melanogaster: Mapping Spontaneous Mutations Affecting Sensory Bristle Number Genetics, August 1, 2005; 170(4): 1723 - 1735. [Abstract] [Full Text] [PDF]

				X. Zhang and T. H. Eickbush Characterization of Active R2 Retrotransposition in the rDNA Locus of Drosophila simulans Genetics, May 1, 2005; 170(1): 195 - 205. [Abstract] [Full Text] [PDF]

				S. E. Hammer, S. Strehl, and S. Hagemann Homologs of Drosophila P Transposons Were Mobile in Zebrafish but Have Been Domesticated in a Common Ancestor of Chicken and Human Mol. Biol. Evol., April 1, 2005; 22(4): 833 - 844. [Abstract] [Full Text] [PDF]

				M. M. Tanaka, N. A. Rosenberg, and P. M. Small The Control of Copy Number of IS6110 in Mycobacterium tuberculosis Mol. Biol. Evol., December 1, 2004; 21(12): 2195 - 2201. [Abstract] [Full Text] [PDF]

				M. J. Simmons, J. D. Raymond, J. B. Niemi, J. R. Stuart, and P. J. Merriman The P Cytotype in Drosophila melanogaster: A Maternally Transmitted Regulatory State of the Germ Line Associated With Telomeric P Elements Genetics, January 1, 2004; 166(1): 243 - 254. [Abstract] [Full Text] [PDF]

				J. B. Niemi, J. D. Raymond, R. Patrek, and M. J. Simmons Establishment and Maintenance of the P Cytotype Associated With Telomeric P Elements in Drosophila melanogaster Genetics, January 1, 2004; 166(1): 255 - 264. [Abstract] [Full Text] [PDF]

				J. R. Stuart, K. J. Haley, D. Swedzinski, S. Lockner, P. E. Kocian, P. J. Merriman, and M. J. Simmons Telomeric P elements Associated With Cytotype Regulation of the P Transposon Family in Drosophila melanogaster Genetics, December 1, 2002; 162(4): 1641 - 1654. [Abstract] [Full Text] [PDF]

				C. E. Perez-Gonzalez and T. H. Eickbush Rates of R1 and R2 Retrotransposition and Elimination From the rDNA Locus of Drosophila melanogaster Genetics, October 1, 2002; 162(2): 799 - 811. [Abstract] [Full Text] [PDF]

				M. J. Simmons, K. J. Haley, and S. J. Thompson Maternal transmission of P element transposase activity in Drosophila melanogaster depends on the last P intron PNAS, July 9, 2002; 99(14): 9306 - 9309. [Abstract] [Full Text] [PDF]

				M. J. Simmons, K. J. Haley, C. D. Grimes, J. D. Raymond, and J. B. Niemi A hobo Transgene That Encodes the P-Element Transposase in Drosophila melanogaster: Autoregulation and Cytotype Control of Transposase Activity Genetics, May 1, 2002; 161(1): 195 - 204. [Abstract] [Full Text] [PDF]

				M. J. Simmons, K. J. Haley, C. D. Grimes, J. D. Raymond, and J. C. L. Fong Regulation of P-Element Transposase Activity in Drosophila melanogaster by hobo Transgenes That Contain KP Elements Genetics, May 1, 2002; 161(1): 205 - 215. [Abstract] [Full Text] [PDF]

				S. Ronsseray, A. Boivin, and D. Anxolabehere P-Element Repression in Drosophila melanogaster by Variegating Clusters of P-lacZ-white Transgenes Genetics, December 1, 2001; 159(4): 1631 - 1642. [Abstract] [Full Text] [PDF]

				S. Hagemann and W. Pinsker Drosophila P Transposons in the Human Genome? Mol. Biol. Evol., October 1, 2001; 18(10): 1979 - 1982. [Full Text] [PDF]

				L. Marin, M. Lehmann, D. Nouaud, H. Izaabel, D. Anxolabéhère, and S. Ronsseray P-Element Repression in Drosophila melanogaster by a Naturally Occurring Defective Telomeric P Copy Genetics, August 1, 2000; 155(4): 1841 - 1854. [Abstract] [Full Text]

				S. Kusakabe, Y. Yamaguchi, H. Baba, and T. Mukai The Genetic Structure of the Raleigh Natural Population of Drosophila melanogaster Revisited Genetics, February 1, 2000; 154(2): 679 - 685. [Abstract] [Full Text]

				P. D. Keightley and A. Eyre-Walker Terumi Mukai and the Riddle of Deleterious Mutation Rates Genetics, October 1, 1999; 153(2): 515 - 523. [Abstract] [Full Text] [PDF]

				M. C. Gurganus, S. V. Nuzhdin, J. W. Leips, and T. F. C. Mackay High-Resolution Mapping of Quantitative Trait Loci for Sternopleural Bristle Number in Drosophila melanogaster Genetics, August 1, 1999; 152(4): 1585 - 1604. [Abstract] [Full Text]

				S. V. Nuzhdin, E. G. Pasyukova, E. A. Morozova, and A. J. Flavell Quantitative Genetic Analysis of copia Retrotransposon Activity in Inbred Drosophila melanogaster Lines Genetics, October 1, 1998; 150(2): 755 - 766. [Abstract] [Full Text]

				S. Ronsseray, L. Marin, M. Lehmann, and D. Anxolabehere Repression of Hybrid Dysgenesis in Drosophila melanogaster by Combinations of Telomeric P-Element Reporters and Naturally Occurring P Elements Genetics, August 1, 1998; 149(4): 1857 - 1866. [Abstract] [Full Text] [PDF]

				B. Chen, T. Chu, E. Harms, J. P. Gergen, and S. Strickland Mapping of Drosophila Mutations Using Site-Specific Male Recombination Genetics, May 1, 1998; 149(1): 157 - 163. [Abstract] [Full Text] [PDF]

				R. Beeman, K. Friesen, and R. Denell Maternal-effect selfish genes in flour beetles Science, April 3, 1992; 256(5053): 89 - 92. [Abstract] [PDF]

				R. Woodruff, J. Blount, and J. Thompson Jr Hybrid dysgenesis in D. melanogaster is not a general release mechanism for DNA transpositions Science, September 4, 1987; 237(4819): 1206 - 1218. [Abstract] [PDF]

				L. Miller, R. Sakai, P Romans, R. Gwadz, P Kantoff, and H. Coon Stable integration and expression of a bacterial gene in the mosquito Anopheles gambiae Science, August 14, 1987; 237(4816): 779 - 781. [Abstract] [PDF]

				W. Engels A trans-acting product needed for P factor transposition in Drosophila Science, December 7, 1984; 226(4679): 1194 - 1196. [Abstract] [PDF]

				M. R. Rose and W. F. Doolittle Molecular Biological Mechanisms of Speciation Science, April 8, 1983; 220(4593): 157 - 162. [Abstract] [PDF]

				A. Spradling and G. Rubin Transposition of cloned P elements into Drosophila germ line chromosomes Science, October 22, 1982; 218(4570): 341 - 347. [Abstract] [PDF]

				R Berg, W. Engels, and R. Kreber Site-specific X-chromosome rearrangements from hybrid dysgenesis in Drosophila melanogaster Science, October 24, 1980; 210(4468): 427 - 429. [Abstract] [PDF]

				J. Bregliano, G Picard, A Bucheton, A Pelisson, J. Lavige, and P L'Heritier Hybrid dysgenesis in Drosophila melanogaster Science, February 8, 1980; 207(4431): 606 - 611. [Abstract] [PDF]