Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Science 20 November 1998:
Vol. 282. no. 5393, pp. 1501 - 1504
DOI: 10.1126/science.282.5393.1501
Prev | Table of Contents | Next

Reports

A Rapidly Evolving Homeobox at the Site of a Hybrid Sterility Gene

Chau-Ti Ting, Shun-Chern Tsaur, Mao-Lien Wu, Chung-I Wu *

The homeodomain is a DNA binding motif that is usually conserved among diverse taxa. Rapidly evolving homeodomains are thus of interest because their divergence may be associated with speciation. The exact site of the Odysseus (Ods) locus of hybrid male sterility in Drosophila contains such a homeobox gene. In the past half million years, this homeodomain has experienced more amino acid substitutions than it did in the preceding 700 million years; during this period, it has also evolved faster than other parts of the protein or even the introns. Such rapid sequence divergence is driven by positive selection and may contribute to reproductive isolation.

Department of Ecology and Evolution, The University of Chicago, Chicago, IL 60637, USA.
*   To whom correspondence should be addressed. E-mail: ciwu{at}uchicago.edu

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Reduced Fertility of Drosophila melanogaster Hybrid male rescue (Hmr) Mutant Females Is Partially Complemented by Hmr Orthologs From Sibling Species.
S. Aruna, H. A. Flores, and D. A. Barbash (2009)
Genetics 181, 1437-1450
   Abstract »    Full Text »    PDF »
Genetics and Lineage-Specific Evolution of a Lethal Hybrid Incompatibility Between Drosophila mauritiana and Its Sibling Species.
M. V. Cattani and D. C. Presgraves (2009)
Genetics 181, 1545-1555
   Abstract »    Full Text »    PDF »
Evolution of the Drosophila Nuclear Pore Complex Results in Multiple Hybrid Incompatibilities.
S. Tang and D. C. Presgraves (2009)
Science 323, 779-782
   Abstract »    Full Text »    PDF »
A Mouse Speciation Gene Encodes a Meiotic Histone H3 Methyltransferase.
O. Mihola, Z. Trachtulec, C. Vlcek, J. C. Schimenti, and J. Forejt (2009)
Science 323, 373-375
   Abstract »    Full Text »    PDF »
A Single Gene Causes Both Male Sterility and Segregation Distortion in Drosophila Hybrids.
N. Phadnis and H. A. Orr (2009)
Science 323, 376-379
   Abstract »    Full Text »    PDF »
Recurrent Positive Selection of the Drosophila Hybrid Incompatibility Gene Hmr.
S. Maheshwari, J. Wang, and D. A. Barbash (2008)
Mol. Biol. Evol. 25, 2421-2430
   Abstract »    Full Text »    PDF »
The strength and genetic basis of reproductive isolating barriers in flowering plants.
D. B Lowry, J. L Modliszewski, K. M Wright, C. A Wu, and J. H Willis (2008)
Phil Trans R Soc B 363, 3009-3021
   Abstract »    Full Text »    PDF »
From the Cover: A triallelic system of S5 is a major regulator of the reproductive barrier and compatibility of indica-japonica hybrids in rice.
J. Chen, J. Ding, Y. Ouyang, H. Du, J. Yang, K. Cheng, J. Zhao, S. Qiu, X. Zhang, J. Yao, et al. (2008)
PNAS 105, 11436-11441
   Abstract »    Full Text »    PDF »
A Complex Genetic Basis to X-Linked Hybrid Male Sterility Between Two Species of House Mice.
J. M. Good, M. D. Dean, and M. W. Nachman (2008)
Genetics 179, 2213-2228
   Abstract »    Full Text »    PDF »
An Empirical Test for Branch-Specific Positive Selection.
G. C. Nickel, D. L. Tefft, K. Goglin, and M. D. Adams (2008)
Genetics 179, 2183-2193
   Abstract »    Full Text »    PDF »
Accelerated Mitochondrial Evolution and "Darwin's Corollary": Asymmetric Viability of Reciprocal F1 Hybrids in Centrarchid Fishes.
D. I. Bolnick, M. Turelli, H. Lopez-Fernandez, P. C. Wainwright, and T. J. Near (2008)
Genetics 178, 1037-1048
   Abstract »    Full Text »    PDF »
Significant Variation for Fitness Impacts of ETS Loci in Hybrids between Populations of Tigriopus californicus.
C. S. Willett (2008)
J. Hered. 99, 56-65
   Abstract »    Full Text »    PDF »
Cytonuclear Genic Incompatibilities Cause Increased Mortality in Male F2 Hybrids of Nasonia giraulti and N. vitripennis.
O. Niehuis, A. K. Judson, and J. Gadau (2008)
Genetics 178, 413-426
   Abstract »    Full Text »    PDF »
A new approach to estimate parameters of speciation models with application to apes.
C. Becquet and M. Przeworski (2007)
Genome Res. 17, 1505-1519
   Abstract »    Full Text »    PDF »
A Genomewide Study of Reproductive Barriers Between Allopatric Populations of a Homosporous Fern, Ceratopteris richardii.
T. Nakazato, M.-K. Jung, E. A. Housworth, L. H. Rieseberg, and G. J. Gastony (2007)
Genetics 177, 1141-1150
   Abstract »    Full Text »    PDF »
Rapid evolution of primate ESX1, an X-linked placenta- and testis-expressed homeobox gene.
X. Wang and J. Zhang (2007)
Hum. Mol. Genet. 16, 2053-2060
   Abstract »    Full Text »    PDF »
Rapid Detection of Positive Selection in Genes and Genomes Through Variation Clusters.
A. Wagner (2007)
Genetics 176, 2451-2463
   Abstract »    Full Text »    PDF »
Searching the Genomes of Inbred Mouse Strains for Incompatibilities That Reproductively Isolate Their Wild Relatives.
B. A. Payseur and M. Place (2007)
J. Hered. 98, 115-122
   Abstract »    Full Text »    PDF »
Genome-Wide Patterns of Expression in Drosophila Pure Species and Hybrid Males. II. Examination of Multiple-Species Hybridizations, Platforms, and Life Cycle Stages.
A. J. Moehring, K. C. Teeter, and M. A. F. Noor (2007)
Mol. Biol. Evol. 24, 137-145
   Abstract »    Full Text »    PDF »
Pervasive Adaptive Evolution among Interactors of the Drosophila Hybrid Inviability Gene, Nup96.
D. C. Presgraves and W. Stephan (2007)
Mol. Biol. Evol. 24, 306-314
   Abstract »    Full Text »    PDF »
Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila..
N. J. Brideau, H. A. Flores, J. Wang, S. Maheshwari, X. Wang, and D. A. Barbash (2006)
Science 314, 1292-1295
   Abstract »    Full Text »    PDF »
DNA Barcoding Will Often Fail to Discover New Animal Species over Broad Parameter Space.
M. J. Hickerson, C. P. Meyer, and C. Moritz (2006)
Syst Biol 55, 729-739
   Abstract »    Full Text »    PDF »
Widespread Adaptive Evolution of Drosophila Genes With Sex-Biased Expression.
M. Proschel, Z. Zhang, and J. Parsch (2006)
Genetics 174, 893-900
   Abstract »    Full Text »    PDF »
Gene transposition as a cause of hybrid sterility in Drosophila..
J. P. Masly, C. D. Jones, M. A. F. Noor, J. Locke, and H. A. Orr (2006)
Science 313, 1448-1450
   Abstract »    Full Text »    PDF »
Gene Regulation Divergence Is a Major Contributor to the Evolution of Dobzhansky-Muller Incompatibilities between Species of Drosophila.
W. Haerty and R. S. Singh (2006)
Mol. Biol. Evol. 23, 1707-1714
   Abstract »    Full Text »    PDF »
Deleterious Epistatic Interactions Between Electron Transport System Protein-Coding Loci in the Copepod Tigriopus californicus.
C. S. Willett (2006)
Genetics 173, 1465-1477
   Abstract »    Full Text »    PDF »
Contrasting Patterns of Introgression at X-Linked Loci Across the Hybrid Zone Between Subspecies of the European Rabbit (Oryctolagus cuniculus).
A. Geraldes, N. Ferrand, and M. W. Nachman (2006)
Genetics 173, 919-933
   Abstract »    Full Text »    PDF »
Reinforcement and the Genetics of Hybrid Incompatibilities.
A. R. Lemmon and M. Kirkpatrick (2006)
Genetics 173, 1145-1155
   Abstract »    Full Text »    PDF »
The Genetic Basis of Postzygotic Reproductive Isolation Between Drosophila santomea and D. yakuba Due to Hybrid Male Sterility.
A. J. Moehring, A. Llopart, S. Elwyn, J. A. Coyne, and T. F. C. Mackay (2006)
Genetics 173, 225-233
   Abstract »    Full Text »    PDF »
Molecular Genetics of Natural Populations.
A. J. Greenberg and C.-I Wu (2006)
Mol. Biol. Evol. 23, 883-886
   Abstract »    Full Text »    PDF »
X chromosomes and autosomes evolve at similar rates in Drosophila: No evidence for faster-X protein evolution.
K. Thornton, D. Bachtrog, and P. Andolfatto (2006)
Genome Res. 16, 498-504
   Abstract »    Full Text »    PDF »
A Simple Genetic Incompatibility Causes Hybrid Male Sterility in Mimulus.
A. L. Sweigart, L. Fishman, and J. H. Willis (2006)
Genetics 172, 2465-2479
   Abstract »    Full Text »    PDF »
Rapid Evolution and Gene-Specific Patterns of Selection for Three Genes of Spermatogenesis in Drosophila.
A. Civetta, S. A. Rajakumar, B. Brouwers, and J. P. Bacik (2006)
Mol. Biol. Evol. 23, 655-662
   Abstract »    Full Text »    PDF »
Negative epistasis between natural variants of the Saccharomyces cerevisiae MLH1 and PMS1 genes results in a defect in mismatch repair.
J. A. Heck, J. L. Argueso, Z. Gemici, R. G. Reeves, A. Bernard, C. F. Aquadro, and E. Alani (2006)
PNAS 103, 3256-3261
   Abstract »    Full Text »    PDF »
Adaptive Loss of an Old Duplicated Gene During Incipient Speciation.
A. J. Greenberg, J. R. Moran, S. Fang, and C.-I Wu (2006)
Mol. Biol. Evol. 23, 401-410
   Abstract »    Full Text »    PDF »
Patterns of male sterility in a grasshopper hybrid zone imply accumulation of hybrid incompatibilities without selection.
D. M Shuker, K. Underwood, T. M King, and R. K Butlin (2005)
Proc R Soc B 272, 2491-2497
   Abstract »    Full Text »    PDF »
Quantitative Trait Loci for Cuticular Hydrocarbons Associated With Sexual Isolation Between Drosophila simulans and D. sechellia.
J. M. Gleason, J.-M. Jallon, J.-D. Rouault, and M. G. Ritchie (2005)
Genetics 171, 1789-1798
   Abstract »    Full Text »    PDF »
Signatures of Reproductive Isolation in Patterns of Single Nucleotide Diversity Across Inbred Strains of Mice.
B. A. Payseur and H. E. Hoekstra (2005)
Genetics 171, 1905-1916
   Abstract »    Full Text »    PDF »
Selectionism and Neutralism in Molecular Evolution.
M. Nei (2005)
Mol. Biol. Evol. 22, 2318-2342
   Abstract »    Full Text »    PDF »
Patterns of Synonymous Codon Usage in Drosophila melanogaster Genes With Sex-Biased Expression.
T. M. Hambuch and J. Parsch (2005)
Genetics 170, 1691-1700
   Abstract »    Full Text »    PDF »
The genetic basis of reproductive isolation: Insights from Drosophila.
H. A. Orr (2005)
PNAS 102, 6522-6526
   Abstract »    Full Text »    PDF »
Comparative Genomics of Accessory Gland Protein Genes in Drosophila melanogaster and D. pseudoobscura.
B. J. Wagstaff and D. J. Begun (2005)
Mol. Biol. Evol. 22, 818-832
   Abstract »    Full Text »    PDF »
Genetics of Hybrid Incompatibility Between Lycopersicon esculentum and L. hirsutum.
L. C. Moyle and E. B. Graham (2005)
Genetics 169, 355-373
   Abstract »    Full Text »    PDF »
MSAP, the Meichroacidin Homolog of Carp (Cyprinus carpio), Differs from the Rodent Counterpart in Germline Expression and Involves Flagellar Differentiation.
T.-K. Ju and F.-L. Huang (2004)
Biol Reprod 71, 1419-1429
   Abstract »    Full Text »    PDF »
Molecular Evolution of Sex-Biased Genes in Drosophila.
Z. Zhang, T. M. Hambuch, and J. Parsch (2004)
Mol. Biol. Evol. 21, 2130-2139
   Abstract »    Full Text »    PDF »
Gene duplication and speciation in Drosophila: Evidence from the Odysseus locus.
C.-T. Ting, S.-C. Tsaur, S. Sun, W. E. Browne, Y.-C. Chen, N. H. Patel, and C.-I Wu (2004)
PNAS 101, 12232-12235
   Abstract »    Full Text »    PDF »
The Normal Function of a Speciation Gene, Odysseus, and Its Hybrid Sterility Effect.
S. Sun, C.-T. Ting, and C.-I Wu (2004)
Science 305, 81-83
   Abstract »    Full Text »    PDF »
Quantitative Trait Loci for Sexual Isolation Between Drosophila simulans and D. mauritiana.
A. J. Moehring, J. Li, M. D. Schug, S. G. Smith, M. deAngelis, T. F. C. Mackay, and J. A. Coyne (2004)
Genetics 167, 1265-1274
   Abstract »    Full Text »    PDF »
Molecular Population Genetics of Male Accessory Gland Proteins in the Drosophila simulans Complex.
A. D. Kern, C. D. Jones, and D. J. Begun (2004)
Genetics 167, 725-735
   Abstract »    Full Text »    PDF »
Rapid Evolution of Mammalian X-Linked Testis-Expressed Homeobox Genes.
X. Wang and J. Zhang (2004)
Genetics 167, 879-888
   Abstract »    Full Text »    PDF »
Nucleotide Variation in the tinman and bagpipe Homeobox Genes of Drosophila melanogaster.
E. S. Balakirev and F. J. Ayala (2004)
Genetics 166, 1845-1856
   Abstract »    Full Text »    PDF »
Evolution of DMY, a Newly Emergent Male Sex-Determination Gene of Medaka Fish.
J. Zhang (2004)
Genetics 166, 1887-1895
   Abstract »    Full Text »    PDF »
Genetics of Postzygotic Isolation in Eucalyptus: Whole-Genome Analysis of Barriers to Introgression in a Wide Interspecific Cross of Eucalyptus grandis and E. globulus.
A. A. Myburg, C. Vogl, A. R. Griffin, R. R. Sederoff, and R. W. Whetten (2004)
Genetics 166, 1405-1418
   Abstract »    Full Text »    PDF »
Genetic Complexity Underlying Hybrid Male Sterility in Drosophila.
K. Sawamura, J. Roote, C.-I Wu, and M.-T. Yamamoto (2004)
Genetics 166, 789-796
   Abstract »    Full Text »    PDF »
Characterization of a Male-Predominant Antisense Transcript Underexpressed in Hybrids of Drosophila pseudoobscura and D. persimilis.
M. A. F. Noor, P. Michalak, and D. Donze (2003)
Genetics 165, 1823-1830
   Abstract »    Full Text »    PDF »
Rapidly Evolving Genes in Human. I. The Glycophorins and Their Possible Role in Evading Malaria Parasites.
H.-Y. Wang, H. Tang, C.-K. J. Shen, and C.-I Wu (2003)
Mol. Biol. Evol. 20, 1795-1804
   Abstract »    Full Text »    PDF »
The complexity of alternative splicing of hagoromo mRNAs is increased in an explosively speciated lineage in East African cichlids.
Y. Terai, N. Morikawa, K. Kawakami, and N. Okada (2003)
PNAS 100, 12798-12803
   Abstract »    Full Text »    PDF »
The Evolution of Transcriptional Regulation in Eukaryotes.
G. A. Wray, M. W. Hahn, E. Abouheif, J. P. Balhoff, M. Pizer, M. V. Rockman, and L. A. Romano (2003)
Mol. Biol. Evol. 20, 1377-1419
   Abstract »    Full Text »    PDF »
Sex peptide and the sperm effect in Drosophila melanogaster.
W. J. Swanson (2003)
PNAS 100, 9643-9644
   Full Text »    PDF »
Genetic Dissection of Hybrid Incompatibilities Between Drosophila simulans and D. mauritiana. II. Mapping Hybrid Male Sterility Loci on the Third Chromosome.
Y. Tao, Z.-B. Zeng, J. Li, D. L. Hartl, and C. C. Laurie (2003)
Genetics 164, 1399-1418
   Abstract »    Full Text »    PDF »
Paleomolecular biology unravels the evolutionary mystery of vertebrate UV vision.
J. Zhang (2003)
PNAS 100, 8045-8047
   Full Text »    PDF »
Dntf-2r, a Young Drosophila Retroposed Gene With Specific Male Expression Under Positive Darwinian Selection.
E. Betran and M. Long (2003)
Genetics 164, 977-988
   Abstract »    Full Text »    PDF »
Genome-Wide Patterns of Expression in Drosophila Pure Species and Hybrid Males.
P. Michalak and M. A. F. Noor (2003)
Mol. Biol. Evol. 20, 1070-1076
   Abstract »    Full Text »    PDF »
A rapidly evolving MYB-related protein causes species isolation in Drosophila.
D. A. Barbash, D. F. Siino, A. M. Tarone, and J. Roote (2003)
PNAS 100, 5302-5307
   Abstract »    Full Text »    PDF »
Evidence for Inversion Polymorphism Related to Sympatric Host Race Formation in the Apple Maggot Fly, Rhagoletis pomonella.
J. L. Feder, J. B. Roethele, K. Filchak, J. Niedbalski, and J. Romero-Severson (2003)
Genetics 163, 939-953
   Abstract »    Full Text »    PDF »
Positive Selection Within Sperm-Egg Adhesion Domains of Fertilin: An ADAM Gene with a Potential Role in Fertilization.
A. Civetta (2003)
Mol. Biol. Evol. 20, 21-29
   Abstract »    Full Text »    PDF »
A Mutation in the Promoter of Desaturase 2 Is Correlated With Sexual Isolation Between Drosophila Behavioral Races.
S. Fang, A. Takahashi, and C.-I Wu (2002)
Genetics 162, 781-784
   Abstract »    Full Text »    PDF »
Intron presence-absence polymorphism in Drosophila driven by positive Darwinian selection.
A. Llopart, J. M. Comeron, F. G. Brunet, D. Lachaise, and M. Long (2002)
PNAS 99, 8121-8126
   Abstract »    Full Text »    PDF »
Diverse Variation of Reproductive Barriers in Three Intraspecific Rice Crosses.
Y. Harushima, M. Nakagahra, M. Yano, T. Sasaki, and N. Kurata (2002)
Genetics 160, 313-322
   Abstract »    Full Text »    PDF »
Comparative Genomics and Regulatory Evolution: Conservation and Function of the Chs and Apetala3 Promoters.
M. A. Koch, B. Weisshaar, J. Kroymann, B. Haubold, and T. Mitchell-Olds (2001)
Mol. Biol. Evol. 18, 1882-1891
   Abstract »    Full Text »    PDF »
Complex Epistasis and the Genetic Basis of Hybrid Sterility in the Drosophila pseudoobscura Bogota-USA Hybridization.
H. A. Orr and S. Irving (2001)
Genetics 158, 1089-1100
   Abstract »    Full Text »    PDF »
Rolling back to BOULE.
E. S. Haag (2001)
PNAS 98, 6983-6985
   Full Text »    PDF »
Incipient speciation by sexual isolation in Drosophila: Concurrent evolution at multiple loci.
C.-T. Ting, A. Takahashi, and C.-I Wu (2001)
PNAS 98, 6709-6713
   Abstract »    Full Text »    PDF »
A locus for female discrimination behavior causing sexual isolation in Drosophila.
M. Doi, M. Matsuda, M. Tomaru, H. Matsubayashi, and Y. Oguma (2001)
PNAS 98, 6714-6719
   Abstract »    Full Text »    PDF »
The nucleotide changes governing cuticular hydrocarbon variation and their evolution in Drosophila melanogaster.
A. Takahashi, S.-C. Tsaur, J. A. Coyne, and C.-I Wu (2001)
PNAS
   Abstract »    Full Text »
Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals.
W. J. Swanson, Z. Yang, M. F. Wolfner, and C. F. Aquadro (2001)
PNAS
   Abstract »    Full Text »
A New Function Evolved from Gene Fusion.
M. Long (2000)
Genome Res. 10, 1655-1657
   Full Text »
Contrasting Molecular Population Genetics of Four Hexokinases in Drosophila melanogaster, D. simulans and D. yakuba.
D. D. Duvernell and W. F. Eanes (2000)
Genetics 156, 1191-1201
   Abstract »    Full Text »
The Drosophila melanogaster Hybrid male rescue Gene Causes Inviability in Male and Female Species Hybrids.
D. A. Barbash, J. Roote, and M. Ashburner (2000)
Genetics 154, 1747-1771
   Abstract »    Full Text »
The Role of Population Size, Pleiotropy and Fitness Effects of Mutations in the Evolution of Overlapping Gene Functions.
A. Wagner (2000)
Genetics 154, 1389-1401
   Abstract »    Full Text »
Human-mouse differences in the embryonic expression patterns of developmental control genes and disease genes.
F. Fougerousse, P. Bullen, M. Herasse, S. Lindsay, I. Richard, D. Wilson, L. Suel, M. Durand, S. Robson, M. Abitbol, et al. (2000)
Hum. Mol. Genet. 9, 165-173
   Abstract »    Full Text »    PDF »
Major recent and independent changes in levels and patterns of expression have occurred at the b gene, a regulatory locus in maize.
D. A. Selinger and V. L. Chandler (1999)
PNAS 96, 15007-15012
   Abstract »    Full Text »    PDF »
Genetic analysis of speciation by means of introgression into Drosophila melanogaster.
K. Sawamura, A. W. Davis, and C.-I Wu (2000)
PNAS 97, 2652-2655
   Abstract »    Full Text »    PDF »
Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals.
W. J. Swanson, Z. Yang, M. F. Wolfner, and C. F. Aquadro (2001)
PNAS 98, 2509-2514
   Abstract »    Full Text »    PDF »
The nucleotide changes governing cuticular hydrocarbon variation and their evolution in Drosophila melanogaster.
A. Takahashi, S.-C. Tsaur, J. A. Coyne, and C.-I Wu (2001)
PNAS 98, 3920-3925
   Abstract »    Full Text »    PDF »
The phylogeny of closely related species as revealed by the genealogy of a speciation gene, Odysseus.
C.-T. Ting, S.-C. Tsaur, and C.-I Wu (2000)
PNAS 97, 5313-5316
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)