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.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 13 June 2003:
Vol. 300. no. 5626, pp. 1742 - 1745
DOI: 10.1126/science.1085881

Reports

Sex-Dependent Gene Expression and Evolution of the Drosophila Transcriptome

José M. Ranz, Cristian I. Castillo-Davis, Colin D. Meiklejohn, Daniel L. Hartl*

Comparison of the gene-expression profiles between adults of Drosophila melanogaster and Drosophila simulans has uncovered the evolution of genes that exhibit sex-dependent regulation. Approximately half the genes showed differences in expression between the species, and among these, ~83% involved a gain, loss, increase, decrease, or reversal of sex-biased expression. Most of the interspecific differences in messenger RNA abundance affect male-biased genes. Genes that differ in expression between the species showed functional clustering only if they were sex-biased. Our results suggest that sex-dependent selection may drive changes in expression of many of the most rapidly evolving genes in the Drosophila transcriptome.

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.

* To whom correspondence should be addressed. E-mail: dhartl{at}oeb.harvard.edu

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Are sex-biased genes more dispensable?.
J. E. Mank and H. Ellegren (2009)
Biol Lett 5, 409-412
   Abstract »    Full Text »    PDF »
The Silkworm Z Chromosome Is Enriched in Testis-Specific Genes.
K. P. Arunkumar, K. Mita, and J. Nagaraju (2009)
Genetics 182, 493-501
   Abstract »    Full Text »    PDF »
General gene movement off the X chromosome in the Drosophila genus.
M. D. Vibranovski, Y. Zhang, and M. Long (2009)
Genome Res. 19, 897-903
   Abstract »    Full Text »    PDF »
Nonadditive Expression of Homoeologous Genes Is Established Upon Polyploidization in Hexaploid Wheat.
M. Pumphrey, J. Bai, D. Laudencia-Chingcuanco, O. Anderson, and B. S. Gill (2009)
Genetics 181, 1147-1157
   Abstract »    Full Text »    PDF »
The Influence of Demography and Weak Selection on the McDonald-Kreitman Test: An Empirical Study in Drosophila.
J. Parsch, Z. Zhang, and J. F. Baines (2009)
Mol. Biol. Evol. 26, 691-698
   Abstract »    Full Text »    PDF »
Sex-Specific Splicing in Drosophila: Widespread Occurrence, Tissue Specificity and Evolutionary Conservation.
M. Telonis-Scott, A. Kopp, M. L. Wayne, S. V. Nuzhdin, and L. M. McIntyre (2009)
Genetics 181, 421-434
   Abstract »    Full Text »    PDF »
Genetic Changes Accompanying the Evolution of Host Specialization in Drosophila sechellia.
I. Dworkin and C. D. Jones (2009)
Genetics 181, 721-736
   Abstract »    Full Text »    PDF »
Reduced X-Linked Rare Polymorphism in Males in Comparison to Females of Drosophila melanogaster.
K. H. Takahashi, K. Tanaka, M. Itoh, and T. Takano-Shimizu (2009)
J. Hered. 100, 97-105
   Abstract »    Full Text »    PDF »
The Phenomics and Expression Quantitative Trait Locus Mapping of Brain Transcriptomes Regulating Adaptive Divergence in Lake Whitefish Species Pairs (Coregonus sp.).
A. R. Whiteley, N. Derome, S. M. Rogers, J. St-Cyr, J. Laroche, A. Labbe, A. Nolte, S. Renaut, J. Jeukens, and L. Bernatchez (2008)
Genetics 180, 147-164
   Abstract »    Full Text »    PDF »
Pervasive Sex-Linked Effects on Transcription Regulation As Revealed by Expression Quantitative Trait Loci Mapping in Lake Whitefish Species Pairs (Coregonus sp., Salmonidae).
N. Derome, B. Bougas, S. M. Rogers, A. R. Whiteley, A. Labbe, J. Laroche, and L. Bernatchez (2008)
Genetics 179, 1903-1917
   Abstract »    Full Text »    PDF »
Effects of X-Linkage and Sex-Biased Gene Expression on the Rate of Adaptive Protein Evolution in Drosophila.
J. F. Baines, S. A. Sawyer, D. L. Hartl, and J. Parsch (2008)
Mol. Biol. Evol. 25, 1639-1650
   Abstract »    Full Text »    PDF »
Recurrent Events of Positive Selection in Independent Drosophila Lineages at the Spermatogenesis Gene roughex.
A. Llopart and J. M. Comeron (2008)
Genetics 179, 1009-1020
   Abstract »    Full Text »    PDF »
The evolution of courtship behaviors through the origination of a new gene in Drosophila.
H. Dai, Y. Chen, S. Chen, Q. Mao, D. Kennedy, P. Landback, A. Eyre-Walker, W. Du, and M. Long (2008)
PNAS 105, 7478-7483
   Abstract »    Full Text »    PDF »
Null mutations in human and mouse orthologs frequently result in different phenotypes.
B.-Y. Liao and J. Zhang (2008)
PNAS 105, 6987-6992
   Abstract »    Full Text »    PDF »
Sexual and social stimuli elicit rapid and contrasting genomic responses.
M. E Cummings, J. Larkins-Ford, C. R.L Reilly, R. Y Wong, M. Ramsey, and H. A Hofmann (2008)
Proc R Soc B 275, 393-402
   Abstract »    Full Text »    PDF »
Contrasting the Efficacy of Selection on the X and Autosomes in Drosophila.
N. D. Singh, A. M. Larracuente, and A. G. Clark (2008)
Mol. Biol. Evol. 25, 454-467
   Abstract »    Full Text »    PDF »
Polymorphic Y Chromosomes Harbor Cryptic Variation with Manifold Functional Consequences.
B. Lemos, L. O. Araripe, and D. L. Hartl (2008)
Science 319, 91-93
   Abstract »    Full Text »    PDF »
Rapid Evolution of Female-Biased, but Not Male-Biased, Genes Expressed in the Avian Brain.
J. E. Mank, L. Hultin-Rosenberg, E. Axelsson, and H. Ellegren (2007)
Mol. Biol. Evol. 24, 2698-2706
   Abstract »    Full Text »    PDF »
Simpler mode of inheritance of transcriptional variation in male Drosophila melanogaster.
M. L. Wayne, M. Telonis-Scott, L. M. Bono, L. Harshman, A. Kopp, S. V. Nuzhdin, and L. M. McIntyre (2007)
PNAS 104, 18577-18582
   Abstract »    Full Text »    PDF »
Evolution in the Fast Lane: Rapidly Evolving Sex-Related Genes in Drosophila.
W. Haerty, S. Jagadeeshan, R. J. Kulathinal, A. Wong, K. Ravi Ram, L. K. Sirot, L. Levesque, C. G. Artieri, M. F. Wolfner, A. Civetta, et al. (2007)
Genetics 177, 1321-1335
   Abstract »    Full Text »    PDF »
Adaptive Protein Evolution of X-linked and Autosomal Genes in Drosophila: Implications for Faster-X Hypotheses.
T. Connallon (2007)
Mol. Biol. Evol. 24, 2566-2572
   Abstract »    Full Text »    PDF »
Origins of New Male Germ-line Functions from X-Derived Autosomal Retrogenes in the Mouse.
M.-S. Shiao, P. Khil, R. D. Camerini-Otero, T. Shiroishi, K. Moriwaki, H.-T. Yu, and M. Long (2007)
Mol. Biol. Evol. 24, 2242-2253
   Abstract »    Full Text »    PDF »
Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction.
K. Ravi Ram and M. F. Wolfner (2007)
Integr. Comp. Biol. 47, 427-445
   Abstract »    Full Text »    PDF »
Using DNA microarrays to study gene expression in closely related species.
A. Oshlack, A. E. Chabot, G. K. Smyth, and Y. Gilad (2007)
Bioinformatics 23, 1235-1242
   Abstract »    Full Text »    PDF »
Comparative environmental genomics in non-model species: using heterologous hybridization to DNA-based microarrays.
B. A. Buckley (2007)
J. Exp. Biol. 210, 1602-1606
   Abstract »    Full Text »    PDF »
Fast-X on the Z: Rapid evolution of sex-linked genes in birds.
J. E. Mank, E. Axelsson, and H. Ellegren (2007)
Genome Res. 17, 618-624
   Abstract »    Full Text »    PDF »
Inaugural Article: Prevalence of positive selection among nearly neutral amino acid replacements in Drosophila.
S. A. Sawyer, J. Parsch, Z. Zhang, and D. L. Hartl (2007)
PNAS 104, 6504-6510
   Abstract »    Full Text »    PDF »
Effects of genome-wide heterozygosity on a range of biomedically relevant human quantitative traits.
H. Campbell, A. D. Carothers, I. Rudan, C. Hayward, Z. Biloglav, L. Barac, M. Pericic, B. Janicijevic, N. Smolej-Narancic, O. Polasek, et al. (2007)
Hum. Mol. Genet. 16, 233-241
   Abstract »    Full Text »    PDF »
Characteristics, causes and evolutionary consequences of male-biased mutation.
H. Ellegren (2007)
Proc R Soc B 274, 1-10
   Abstract »    Full Text »    PDF »
Contrasting evolution of expression differences in the testis between species and subspecies of the house mouse.
C. Voolstra, D. Tautz, P. Farbrother, L. Eichinger, and B. Harr (2007)
Genome Res. 17, 42-49
   Abstract »    Full Text »    PDF »
Impact of Transcriptional Properties on Essentiality and Evolutionary Rate.
J. K. Choi, S. C. Kim, J. Seo, S. Kim, and J. Bhak (2007)
Genetics 175, 199-206
   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 »
Sebida: a database for the functional and evolutionary analysis of genes with sex-biased expression.
F. Gnad and J. Parsch (2006)
Bioinformatics 22, 2577-2579
   Abstract »    Full Text »    PDF »
The Nature of Genetic Influences on Behavior: Lessons From "Simpler" Organisms.
K. S. Kendler and R. J. Greenspan (2006)
Am J Psychiatry 163, 1683-1694
   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 »
No Accelerated Rate of Protein Evolution in Male-Biased Drosophila pseudoobscura Genes.
M. Metta, R. Gudavalli, J.-M. Gibert, and C. Schlotterer (2006)
Genetics 174, 411-420
   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 »
Low Rates of Expression Profile Divergence in Highly Expressed Genes and Tissue-Specific Genes During Mammalian Evolution.
B.-Y. Liao and J. Zhang (2006)
Mol. Biol. Evol. 23, 1119-1128
   Abstract »    Full Text »    PDF »
Adaptive Protein Evolution and Regulatory Divergence in Drosophila.
J. M. Good, C. A. Hayden, and T. J. Wheeler (2006)
Mol. Biol. Evol. 23, 1101-1103
   Abstract »    Full Text »    PDF »
A data-driven clustering method for time course gene expression data.
P. Ma, C. I. Castillo-Davis, W. Zhong, and J. S. Liu (2006)
Nucleic Acids Res. 34, 1261-1269
   Abstract »    Full Text »    PDF »
Evolutionary Conservation of Expression Profiles Between Human and Mouse Orthologous Genes.
B.-Y. Liao and J. Zhang (2006)
Mol. Biol. Evol. 23, 530-540
   Abstract »    Full Text »    PDF »
A new method to remove hybridization bias for interspecies comparison of global gene expression profiles uncovers an association between mRNA sequence divergence and differential gene expression in Xenopus.
M. A. Sartor, A. M. Zorn, J. A. Schwanekamp, D. Halbleib, S. Karyala, M. L. Howell, G. E. Dean, M. Medvedovic, and C. R. Tomlinson (2006)
Nucleic Acids Res. 34, 185-200
   Abstract »    Full Text »    PDF »
Genomewide Nonadditive Gene Regulation in Arabidopsis Allotetraploids.
J. Wang, L. Tian, H.-S. Lee, N. E. Wei, H. Jiang, B. Watson, A. Madlung, T. C. Osborn, R. W. Doerge, L. Comai, et al. (2006)
Genetics 172, 507-517
   Abstract »    Full Text »    PDF »
Drosophila melanogaster: A case study of a model genomic sequence and its consequences.
M. Ashburner and C. M. Bergman (2005)
Genome Res. 15, 1661-1667
   Abstract »    Full Text »    PDF »
Genetic Analysis of Variation in Gene Expression in Arabidopsis thaliana.
M. Vuylsteke, F. van Eeuwijk, P. Van Hummelen, M. Kuiper, and M. Zabeau (2005)
Genetics 171, 1267-1275
   Abstract »    Full Text »    PDF »
Molecular Population Genetics of Accessory Gland Protein Genes and Testis-Expressed Genes in Drosophila mojavensis and D. arizonae.
B. J. Wagstaff and D. J. Begun (2005)
Genetics 171, 1083-1101
   Abstract »    Full Text »    PDF »
Positive Correlation Between Evolutionary Rate and Recombination Rate in Drosophila Genes with Male-Biased Expression.
Z. Zhang and J. Parsch (2005)
Mol. Biol. Evol. 22, 1945-1947
   Abstract »    Full Text »    PDF »
Rapid Evolution of Genomic Acp Complement in the melanogaster Subgroup of Drosophila.
D. J. Begun and H. A. Lindfors (2005)
Mol. Biol. Evol. 22, 2010-2021
   Abstract »    Full Text »    PDF »
Cross-Species Comparison of Drosophila Male Accessory Gland Protein Genes.
J. L. Mueller, K. R. Ram, L. A. McGraw, M. C. Bloch Qazi, E. D. Siggia, A. G. Clark, C. F. Aquadro, and M. F. Wolfner (2005)
Genetics 171, 131-143
   Abstract »    Full Text »    PDF »
Rapidly Evolving Genes of Drosophila: Differing Levels of Selective Pressure in Testis, Ovary, and Head Tissues Between Sibling Species.
S. Jagadeeshan and R. S. Singh (2005)
Mol. Biol. Evol. 22, 1793-1801
   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 »
Sex-linked Correlated Responses in Female Reproductive Traits to Selection on Male Eye Span in Stalk-eyed Flies.
G. S. Wilkinson, E. G. Amitin, and P. M. Johns (2005)
Integr. Comp. Biol. 45, 500-510
   Abstract »    Full Text »    PDF »
Genetics and genomics of Drosophila mating behavior.
T. F. C. Mackay, S. L. Heinsohn, R. F. Lyman, A. J. Moehring, T. J. Morgan, and S. M. Rollmann (2005)
PNAS 102, 6622-6629
   Abstract »    Full Text »    PDF »
Genomes, phylogeny, and evolutionary systems biology.
M. Medina (2005)
PNAS 102, 6630-6635
   Abstract »    Full Text »    PDF »
Multi-species microarrays reveal the effect of sequence divergence on gene expression profiles.
Y. Gilad, S. A. Rifkin, P. Bertone, M. Gerstein, and K. P. White (2005)
Genome Res. 15, 674-680
   Abstract »    Full Text »    PDF »
Evolution of Proteins and Gene Expression Levels are Coupled in Drosophila and are Independently Associated with mRNA Abundance, Protein Length, and Number of Protein-Protein Interactions.
B. Lemos, B. R. Bettencourt, C. D. Meiklejohn, and D. L. Hartl (2005)
Mol. Biol. Evol. 22, 1345-1354
   Abstract »    Full Text »    PDF »
Mapping Multiple Quantitative Trait Loci by Bayesian Classification.
M. Zhang, K. L. Montooth, M. T. Wells, A. G. Clark, and D. Zhang (2005)
Genetics 169, 2305-2318
   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 »
Selection-driven transcriptome polymorphism in Escherichia coli/Shigella species.
T. Le Gall, P. Darlu, P. Escobar-Paramo, B. Picard, and E. Denamur (2005)
Genome Res. 15, 260-268
   Abstract »    Full Text »    PDF »
Additivity and trans-acting Effects on Gene Expression in Male Drosophila simulans.
M. L. Wayne, Y.-J. Pan, S. V. Nuzhdin, and L. M. McIntyre (2004)
Genetics 168, 1413-1420
   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 »
Molecular Evolution and Population Genetics of Duplicated Accessory Gland Protein Genes in Drosophila.
A. K. Holloway and D. J. Begun (2004)
Mol. Biol. Evol. 21, 1625-1628
   Abstract »    Full Text »    PDF »
Sex-Specific Effects of Interventions That Extend Fly Life Span.
J. M. S. Burger and D. E. L. Promislow (2004)
Sci. Aging Knowl. Environ. 2004, pe30
   Abstract »    Full Text »
Common Pattern of Evolution of Gene Expression Level and Protein Sequence in Drosophila.
S. V. Nuzhdin, M. L. Wayne, K. L. Harmon, and L. M. McIntyre (2004)
Mol. Biol. Evol. 21, 1308-1317
   Abstract »    Full Text »    PDF »
Genome-wide transcription profile of field- and laboratory-selected dichlorodiphenyltrichloroethane (DDT)-resistant Drosophila.
J. H. F. Pedra, L. M. McIntyre, M. E. Scharf, and B. R. Pittendrigh (2004)
PNAS 101, 7034-7039
   Abstract »    Full Text »    PDF »
Reduced Variation on the Chicken Z Chromosome.
H. Sundstrom, M. T. Webster, and H. Ellegren (2004)
Genetics 167, 377-385
   Abstract »    Full Text »    PDF »
A genomic analysis of Drosophila somatic sexual differentiation and its regulation.
M. N. Arbeitman, A. A. Fleming, M. L. Siegal, B. H. Null, and B. S. Baker (2004)
Development 131, 2007-2021
   Abstract »    Full Text »    PDF »
Anomalies in the Expression Profile of Interspecific Hybrids of Drosophila melanogaster and Drosophila simulans.
J. M. Ranz, K. Namgyal, G. Gibson, and D. L. Hartl (2004)
Genome Res. 14, 373-379
   Abstract »    Full Text »    PDF »
Extensive Gene Traffic on the Mammalian X Chromosome.
J. J. Emerson, H. Kaessmann, E. Betran, and M. Long (2004)
Science 303, 537-540
   Abstract »    Full Text »    PDF »
Rapid evolution of male-biased gene expression in Drosophila.
C. D. Meiklejohn, J. Parsch, J. M. Ranz, and D. L. Hartl (2003)
PNAS 100, 9894-9899
   Abstract »    Full Text »    PDF »



To Advertise     Find Products


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