The evolution of sex-biased genes and sex-biased gene expression
Abstract
Differences between males and females in the optimal phenotype that is favoured by selection can be resolved by the evolution of differential gene expression in the two sexes. Microarray experiments have shown that such sex-biased gene expression is widespread across organisms and genomes. Sex-biased genes show unusually rapid sequence evolution, are often labile in their pattern of expression, and are non-randomly distributed in the genome. Here we discuss the characteristics and expression of sex-biased genes, and the selective forces that shape this previously unappreciated source of phenotypic diversity. Sex-biased gene expression has implications beyond just evolutionary biology, including for medical genetics.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Cites
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
Altschul, S. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.17.3389 · Cited by 73,302 · see citing works
Genome sequencing in microfabricated high-density picolitre reactors
Margulies, M., Egholm, M., Altman, W. E., Attiya, S., Bader, J. S., Bemben, L. A., Berka, J., Braverman, M. S., Chen, Y.-J., Chen, Z., et al. (2005) · Nature · doi:10.1038/nature03959 · Cited by 7,693 · see citing works
Serial Analysis of Gene Expression
Velculescu, V. E., Zhang, L., Vogelstein, B., & Kinzler, K. W. (1995) · Science · doi:10.1126/science.270.5235.484 · Cited by 3,713 · see citing works
X-inactivation profile reveals extensive variability in X-linked gene expression in females
Carrel, L., & Willard, H. F. (2005) · Nature · doi:10.1038/nature03479 · Cited by 2,097 · see citing works
Arnqvist, G., & Rowe, L. (2005) · Princeton University Press eBooks · doi:10.1515/9781400850600 · Cited by 1,622 · see citing works
Bennetzen, J. L., & Hall, B. D. (1982) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)81068-2 · Cited by 1,584 · see citing works
Ikemura, T. (1981) · Journal of Molecular Biology · doi:10.1016/0022-2836(81)90003-6 · Cited by 1,423 · see citing works
The rapid evolution of reproductive proteins
Swanson, W. J., & Vacquier, V. D. (2002) · Nature Reviews Genetics · doi:10.1038/nrg733 · Cited by 1,316 · see citing works
Sexually antagonistic male adaptation triggered by experimental arrest of female evolution
Rice, W. R. (1996) · Nature · doi:10.1038/381232a0 · Cited by 1,074 · see citing works
The Relative Rates of Evolution of Sex Chromosomes and Autosomes
Charlesworth, B., Coyne, J. A., & Barton, N. (1987) · The American Naturalist · doi:10.1086/284701 · Cited by 1,068 · see citing works
SEX CHROMOSOMES AND THE EVOLUTION OF SEXUAL DIMORPHISM
Rice, W. R. (1984) · Evolution · doi:10.1111/j.1558-5646.1984.tb00346.x · Cited by 1,046 · see citing works
A Scan for Positively Selected Genes in the Genomes of Humans and Chimpanzees
Nielsen, R., Bustamante, C. D., Clark, A. G., Glanowski, S., Sackton, T. B., Hubisz, M. J., Fledel-Alon, A., Tanenbaum, D. M., Civello, D., White, T. J., et al. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030170 · Cited by 998 · see citing works
Codon catalog usage is a genome strategy modulated for gene expressivity
Grantham, R. L., Gautier, C., Gouy, M., Jacobzone, M., & Mercier, R. (1981) · Nucleic Acids Research · doi:10.1093/nar/9.1.213-b · Cited by 939 · see citing works
Tissue-specific expression and regulation of sexually dimorphic genes in mice
Yang, X., Schadt, E. E., Wang, S., Wang, H., Arnold, A. P., Ingram-Drake, L., Drake, T. A., & Lusis, A. J. (2006) · Genome Research · doi:10.1101/gr.5217506 · Cited by 922 · see citing works
Resolving the paradox of sex and recombination
Otto, S. P., & Lenormand, T. (2002) · Nature Reviews Genetics · doi:10.1038/nrg761 · Cited by 830 · see citing works
Duret, L., & Mouchiroud, D. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.8.4482 · Cited by 808 · see citing works
Bentley, D. (2006) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2006.10.009 · Cited by 805 · see citing works
An abundance of X-linked genes expressed in spermatogonia
Wang, P. J., McCarrey, J. R., Yang, F., & Page, D. C. (2001) · Nature Genetics · doi:10.1038/86927 · Cited by 784 · see citing works
Sex-Dependent Gene Expression and Evolution of the Drosophila Transcriptome
Ranz, J. M., Castillo-Davis, C. I., Meiklejohn, C. D., & Hartl, D. L. (2003) · Science · doi:10.1126/science.1085881 · Cited by 617 · see citing works
Ikemura, T. (1982) · Journal of Molecular Biology · doi:10.1016/0022-2836(82)90250-9 · Cited by 605 · see citing works
Chippindale, A. K., Gibson, J. R., & Rice, W. R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.4.1671 · Cited by 599 · see citing works
Parallel Patterns of Evolution in the Genomes and Transcriptomes of Humans and Chimpanzees
Khaitovich, P., Hellmann, I., Enard, W., Nowick, K., Leinweber, M., Franz, H., Weiß, G., Lachmann, M., & Pääbo, S. (2005) · Science · doi:10.1126/science.1108296 · Cited by 590 · see citing works
A Global Profile of Germline Gene Expression in C. elegans
Reinke, V., Smith, H. E., Nance, J., Wang, J., Doren, C. V., Begley, R., Jones, S. J. M., Davis, E. B., Scherer, S., Ward, S. F., et al. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)00059-9 · Cited by 578 · see citing works
Schultz, N. D., Hamra, F. K., & Garbers, D. L. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1635054100 · Cited by 577 · see citing works
Paucity of Genes on the Drosophila X Chromosome Showing Male-Biased Expression
Parisi, M. J., Nuttall, R., Naiman, D. Q., Bouffard, G. G., Malley, J. D., Andrews, J., Eastman, S., & Oliver, B. (2003) · Science · doi:10.1126/science.1079190 · Cited by 541 · see citing works
Rapid evolution of reproductive barriers driven by sexual conflict
Sergey Gavrilets, B. (2000) · Nature · doi:10.1038/35002564 · Cited by 516 · see citing works
Dosage compensation in mammals: fine-tuning the expression of the X chromosomePreprint
Heard, É., & Distèche, C. M. (2006) · Genes & Development · doi:10.1101/gad.1422906 · Cited by 504 · see citing works
Richards, S., Liu, Y., Bettencourt, B. R., Hradecky, P., Letovsky, S., Nielsen, R., Thornton, K., Hubisz, M. J., Chen, R., Meisel, R. P., et al. (2005) · Genome Research · doi:10.1101/gr.3059305 · Cited by 498 · see citing works
Rice, W. R., & Holland, B. (1997) · Behavioral Ecology and Sociobiology · doi:10.1007/s002650050357 · Cited by 484 · see citing works
Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans
Reinke, V., Gil, I. S., Ward, S. F., & Kazmer, K. (2003) · Development · doi:10.1242/dev.00914 · Cited by 453 · see citing works
Retroposed New Genes Out of the X in DrosophilaPreprint
Betrán, E. (2002) · Genome Research · doi:10.1101/gr.6049 · Cited by 442 · see citing works
Duret, L. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(00)02041-2 · Cited by 412 · see citing works
Dosage balance in gene regulation: biological implications
Birchler, J. A., Riddle, N. C., Auger, D. L., & Veitia, R. A. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.02.010 · Cited by 371 · see citing works
Birchler, J. A., Bhadra, U., Bhadra, M. P., & Auger, D. L. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0262 · Cited by 355 · see citing works
Dosage compensation is less effective in birds than in mammals
Itoh, Y., Melamed, E., Yang, X., Kampf, K., Wang, S. S.-M., Yehya, N., van Nas, A., Replogle, K. L., Band, M. R., Clayton, D. F., et al. (2007) · Journal of Biology · doi:10.1186/jbiol53 · Cited by 354 · see citing works
Codon Usage Bias and tRNA Abundance in Drosophila
Moriyama, E., & Powell, J. (1997) · Journal of Molecular Evolution · doi:10.1007/pl00006256 · Cited by 341 · see citing works
Levine, M. T., Jones, C. D., Kern, A. D., Lindfors, H. A., & Begun, D. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509809103 · Cited by 339 · see citing works
Khil, P. P., Smirnova, N. A., Romanienko, P. J., & Camerini‐Otero, R. D. (2004) · Nature Genetics · doi:10.1038/ng1368 · Cited by 316 · see citing works
Global analysis of X-chromosome dosage compensation
Gupta, V., Parisi, M. J., Sturgill, D. M., Nuttall, R., Doctolero, M. H., Dudko, O. K., Malley, J. D., Eastman, P. S., & Oliver, B. (2006) · Journal of Biology · doi:10.1186/jbiol30 · Cited by 315 · see citing works
The cost of inbreeding in Arabidopsis
Bustamante, C. D., Nielsen, R., Sawyer, S. A., Olsen, K. M., Purugganan, M. D., & Hartl, D. L. (2002) · Nature · doi:10.1038/416531a · Cited by 307 · see citing works
Rapid evolution of male-biased gene expression in Drosophila
Meiklejohn, C. D., Parsch, J., Ranz, J. M., & Hartl, D. L. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1630690100 · Cited by 302 · see citing works
Chromatin Remodeling in Dosage Compensation
Lucchesi, J. C., Kelly, W. G., & Panning, B. (2005) · Annual Review of Genetics · doi:10.1146/annurev.genet.39.073003.094210 · Cited by 293 · see citing works
A Gene Expression Map for the Euchromatic Genome of Drosophila melanogaster
Štolc, V., Gauhar, Z., Mason, C. E., Halasz, G., van Batenburg, M. F., Rifkin, S. A., Hua, S., Herreman, T., Tongprasit, W., Barbano, P. E., et al. (2004) · Science · doi:10.1126/science.1101312 · Cited by 290 · see citing works
Sexual dimorphism in mammalian gene expression
Rinn, J. L., & Snyder, M. P. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.03.005 · Cited by 285 · see citing works
Genomic and functional evolution of the Drosophila melanogaster sperm proteome
Dorus, S., Busby, S. A., Gerike, U., Shabanowitz, J., Hunt, D. F., & Karr, T. L. (2006) · Nature Genetics · doi:10.1038/ng1915 · Cited by 277 · see citing works
Swanson, W. J., Wong, A., Wolfner, M. F., & Aquadro, C. F. (2004) · Genetics · doi:10.1534/genetics.104.030478 · Cited by 237 · see citing works
Torgerson, D. G., Kulathinal, R. J., & Singh, R. S. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004021 · Cited by 231 · see citing works
Evolutionary Strata on the Chicken Z Chromosome: Implications for Sex Chromosome Evolution
Handley, L. L., Ceplitis, H., & Ellegren, H. (2004) · Genetics · doi:10.1534/genetics.167.1.367 · Cited by 223 · see citing works
Begun, D. J., Lindfors, H. A., Kern, A. D., & Jones, C. D. (2007) · Genetics · doi:10.1534/genetics.106.069245 · Cited by 222 · see citing works
Widespread Adaptive Evolution of Drosophila Genes With Sex-Biased Expression
Pröschel, M., Zhang, Z., & Parsch, J. (2006) · Genetics · doi:10.1534/genetics.106.058008 · Cited by 200 · see citing works
Jegalian, K., & Page, D. C. (1998) · Nature · doi:10.1038/29522 · Cited by 196 · see citing works
Reproductive biology and phylogeny of birds
Jamieson, B. G. M. (2007) · Science Publishers eBooks · Cited by 190 · see citing works
Molecular Evolution of Sex-Biased Genes in Drosophila
Zhang, Z., Hambuch, T. M., & Parsch, J. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh223 · Cited by 189 · see citing works
Sexual antagonism and X inactivation – the SAXI hypothesis
Wu, C.-I., & Xu, E. Y. (2003) · Trends in Genetics · doi:10.1016/s0168-9525(03)00058-1 · Cited by 173 · see citing works
Pleiotropic Constraint Hampers the Resolution of Sexual Antagonism in Vertebrate Gene Expression
Mank, J. E., Hultin‐Rosenberg, L., Zwahlen, M., & Ellegren, H. (2007) · The American Naturalist · doi:10.1086/523954 · Cited by 172 · see citing works
Prevalence of positive selection among nearly neutral amino acid replacements in Drosophila
Sawyer, S. A., Parsch, J., Zhang, Z., & Hartl, D. L. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701572104 · Cited by 163 · see citing works
A stain upon the silence: genes escaping X inactivation
Brown, C. J., & Greally, J. M. (2003) · Trends in Genetics · doi:10.1016/s0168-9525(03)00177-x · Cited by 157 · see citing works
Male fitness increases when females are eliminated from gene pool: Implications for the Y chromosome
Rice, W. R. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.11.6217 · Cited by 157 · see citing works
Intergenomic conflict revealed by patterns of sex-biased gene expression
Connallon, T., & Knowles, L. L. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.07.006 · Cited by 156 · see citing works
An apparent excess of sex– and reproduction–related genes on the human X chromosome
Saifl, G. M., & Chandra, H. S. (1999) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1999.0623 · Cited by 152 · see citing works
Pleiotropy and the Preservation of Perfection
Waxman, D., & Peck, J. R. (1998) · Science · doi:10.1126/science.279.5354.1210 · Cited by 136 · see citing works
Begun, D. J., Lindfors, H. A., Thompson, M. E., & Holloway, A. K. (2005) · Genetics · doi:10.1534/genetics.105.050336 · Cited by 133 · see citing works
Disteche, C. M., Filippova, G. N., & Tsuchiya, K. D. (2002) · Cytogenetic and Genome Research · doi:10.1159/000071572 · Cited by 116 · see citing works
Sex-specific expression of alternative transcripts in Drosophila
McIntyre, L. M., Bono, L. M., Génissel, A., Westerman, R., Junk, D., Telonis‐Scott, M., Harshman, L., Wayne, M. L., Kopp, A., & Nuzhdin, S. V. (2006) · Genome biology · doi:10.1186/gb-2006-7-8-r79 · Cited by 114 · see citing works
Sexual and Temporal Dynamics of Molecular Evolution in C. elegans Development
Cutter, A. D., & Ward, S. F. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh267 · Cited by 113 · see citing works
Good, J. M., & Nachman, M. W. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi087 · Cited by 106 · see citing works
Sebida: a database for the functional and evolutionary analysis of genes with sex-biased expression
Gnad, F., & Parsch, J. (2006) · Bioinformatics · doi:10.1093/bioinformatics/btl422 · Cited by 105 · see citing works
Origin and Neofunctionalization of a Drosophila Paternal Effect Gene Essential for Zygote Viability
Loppin, B., Lepetit, D., Dorus, S., Couble, P., & Karr, T. L. (2005) · Current Biology · doi:10.1016/j.cub.2004.12.071 · Cited by 103 · see citing works
Betrán, E., & Long, M. (2003) · Genetics · doi:10.1093/genetics/164.3.977 · Cited by 102 · see citing works
Rapid Evolution of Genomic Acp Complement in the melanogaster Subgroup of Drosophila
Begun, D. J., & Lindfors, H. A. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi201 · Cited by 87 · see citing works
Zhang, Z., & Parsch, J. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi189 · Cited by 79 · see citing works
Patterns of Synonymous Codon Usage in Drosophila melanogaster Genes With Sex-Biased Expression
Hambuch, T. M., & Parsch, J. (2005) · Genetics · doi:10.1534/genetics.104.038109 · Cited by 76 · see citing works
Voolstra, C. R., Tautz, D., Farbrother, P., Eichinger, L., & Harr, B. (2006) · Genome Research · doi:10.1101/gr.5683806 · Cited by 75 · see citing works
Nonrandom Representation of Sex-Biased Genes on Chicken Z Chromosome
Storchová, R., & Divina, P. (2006) · Journal of Molecular Evolution · doi:10.1007/s00239-006-0022-1 · Cited by 74 · see citing works
NONRANDOM DISTRIBUTION OF GENES WITH SEX-BIASED EXPRESSION IN THE CHICKEN GENOME
Kaiser, V. B., & Ellegren, H. (2006) · Evolution · doi:10.1111/j.0014-3820.2006.tb00537.x · Cited by 74 · see citing works
Sex-dependent gene expression in early brain development of chicken embryos
Scholz, B., Kultima, K., Mattsson, A., Axelsson, J., Brunström, B., Halldin, K., Stigson, M., & Dencker, L. (2006) · BMC Neuroscience · doi:10.1186/1471-2202-7-12 · Cited by 67 · see citing works
Panhuis, T. M., & Swanson, W. J. (2006) · Genetics · doi:10.1534/genetics.105.053611 · Cited by 66 · see citing works
Using DNA microarrays to study gene expression in closely related species
Oshlack, A., Chabot, A. E., Smyth, G. K., & Gilad, Y. (2007) · Bioinformatics · doi:10.1093/bioinformatics/btm111 · Cited by 65 · see citing works
Evaluation of the CaMAL2 promoter for regulated expression of genes in Candida albicans
Backen, A. C., Broadbent, I. D., Fetherston, R., Rosamond, J., Schnell, N. F., & Stark, M. J. R. (2000) · Yeast · doi:10.1002/1097-0061(20000915)16:12 · Cited by 63 · see citing works
Oliver, B., & Parisi, M. J. (2004) · BioEssays · doi:10.1002/bies.20034 · Cited by 59 · see citing works
Molecular Evolution of the ocnus and janus Genes in the Drosophila melanogaster Species Subgroup
Parsch, J., Meiklejohn, C. D., Hauschteck‐Jungen, E., Hunziker, P., & Hartl, D. L. (2001) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003862 · Cited by 51 · see citing works
Genome-wide analysis of sex-enriched gene expression during C. elegans larval development
Thoemke, K., Yi, W., Ross, J. M., Kim, S., Reinke, V., & Zarkower, D. A. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.05.017 · Cited by 43 · see citing works
Kalamegham, R., Sturgill, D. M., Siegfried, E., & Oliver, B. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msl201 · Cited by 34 · see citing works
No Accelerated Rate of Protein Evolution in Male-Biased Drosophila pseudoobscura Genes
Metta, M., Gudavalli, R., Gibert, J., & Schlötterer, C. (2006) · Genetics · doi:10.1534/genetics.106.057414 · Cited by 33 · see citing works
Species specificity in avian sperm:perivitelline interaction
Stewart, S. G., Bausek, N., Wohlrab, F., Schneider, W. J., Horrocks, A. J., & Wishart, G. J. (2004) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpb.2004.01.027 · Cited by 31 · see citing works
Gender-specific selection on codon usage in plant genomes
Whittle, C.-A., Malik, M. R., & Krochko, J. E. (2007) · BMC Genomics · doi:10.1186/1471-2164-8-169 · Cited by 28 · see citing works
Berlin, S., & Smith, N. G. C. (2005) · BMC Evolutionary Biology · doi:10.1186/1471-2148-5-65 · Cited by 21 · see citing works
Inferring Evolutionary History through Inter- and Intraspecific DNA Sequence Comparison
Parsch, J., Meiklejohn, C. D., & Hartl, D. L. (2005) · Springer eBooks · doi:10.1007/0-387-27651-3_1 · Cited by 3 · see citing works
Flagged first, then by citations
1 of the 90 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Toward discovery science of human brain function
Biswal, B. B., Mennes, M., Zuo, X.-N., Gohel, S., Kelly, C., Smith, S. M., Beckmann, C. F., Adelstein, J. S., Buckner, R. L., Colcombe, S., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911855107 · Cited by 2,970 · see citing works
Considering how biological sex impacts immune responses and COVID-19 outcomes
Scully, E. P., Haverfield, J., Ursin, R. L., Tannenbaum, C., & Klein, S. L. (2020) · Nature reviews. Immunology · doi:10.1038/s41577-020-0348-8 · Cited by 925 · see citing works
Russell Bonduriansky, A., & Chenoweth, S. F. (2009) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2008.12.005 · Cited by 771 · see citing works
Gillies, G. E., & McArthur, S. (2010) · Pharmacological Reviews · doi:10.1124/pr.109.002071 · Cited by 733 · see citing works
Sex-specific genetic architecture of human disease
Ober, C., Loisel, D. A., & Gilad, Y. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2415 · Cited by 787 · see citing works
Arnold, A. P., & Chen, X. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.11.001 · Cited by 587 · see citing works
Genetics and Beyond – The Transcriptome of Human Monocytes and Disease Susceptibility
Zeller, T., Wild, P. S., Szymczak, S., Rotival, M., Schillert, A., Castagné, R., Maouche, S., Germain, M., Lackner, K. J., Rossmann, H., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010693 · Cited by 584 · see citing works
In Posidonia oceanica cadmium induces changes in DNA methylation and chromatin patterning
Greco, M., Chiappetta, A. A. C., Bruno, L., & Bitonti, M. B. (2011) · Journal of Experimental Botany · doi:10.1093/jxb/err313 · Cited by 533 · see citing works
Sex Disparities in Cancer Mortality and Survival
Cook, M. B., McGlynn, K. A., Devesa, S. S., Freedman, N. D., & Anderson, W. F. (2011) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-11-0246 · Cited by 517 · see citing works
Systems genetics of complex traits in Drosophila melanogaster
Ayroles, J. F., Carbone, M. A., Stone, E. A., Jordan, K. W., Lyman, R. F., Magwire, M. M., Rollmann, S. M., Duncan, L. H., Lawrence, F., Anholt, R. R. H., et al. (2009) · Nature Genetics · doi:10.1038/ng.332 · Cited by 500 · see citing works
Sexual dimorphism in flowering plants
Barrett, S. C. H., & Hough, J. (2012) · Journal of Experimental Botany · doi:10.1093/jxb/ers308 · Cited by 494 · see citing works
The influence of sex and gender on the immune response
Oertelt-Prigione, S. (2012) · Autoimmunity Reviews · doi:10.1016/j.autrev.2011.11.022 · Cited by 459 · see citing works
The Natural Biotic Environment of Caenorhabditis elegans
Hinrich Schulenburg, Y., & Félix, M. (2017) · Genetics · doi:10.1534/genetics.116.195511 · Cited by 439 · see citing works
The Evolution of Sex Determination
Beukeboom, L. W., & Perrin, N. (2014) · doi:10.1093/acprof:oso/9780199657148.001.0001 · Cited by 413 · see citing works
The evolutionary causes and consequences of sex-biased gene expression
Parsch, J., & Ellegren, H. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3376 · Cited by 363 · see citing works
Genetic basis of fitness differences in natural populations
Ellegren, H., & Sheldon, B. C. (2008) · Nature · doi:10.1038/nature06737 · Cited by 349 · see citing works
Sex chromosomes and speciation in Drosophila
Presgraves, D. C. (2008) · Trends in Genetics · doi:10.1016/j.tig.2008.04.007 · Cited by 336 · see citing works
The Sexually Antagonistic Genes of Drosophila melanogaster
Innocenti, P., & Morrow, E. H. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000335 · Cited by 328 · see citing works
Stronger inflammatory/cytotoxic T-cell response in women identified by microarray analysis
Hewagama, A., Patel, D., Yarlagadda, S., Strickland, F. M., & Richardson, B. C. (2009) · Genes & Immunity · doi:10.1038/gene.2009.12 · Cited by 311 · see citing works
The biological effects of antidepressants on the molluscs and crustaceans: A review
Fong, P. P., & Ford, A. T. (2013) · Aquatic Toxicology · doi:10.1016/j.aquatox.2013.12.003 · Cited by 295 · see citing works
Constraint and turnover in sex-biased gene expression in the genus Drosophila
Zhang, Y., Sturgill, D. M., Parisi, M. J., Kumar, S., & Oliver, B. (2007) · Nature · doi:10.1038/nature06323 · Cited by 293 · see citing works
Scott, J. G., Warren, W. C., Beukeboom, L. W., Bopp, D., Clark, A. G., Giers, S. D., Hediger, M., Jones, A. K., Kasai, S., Leichter, C. A., et al. (2014) · Genome biology · doi:10.1186/s13059-014-0466-3 · Cited by 292 · see citing works
Snell‐Rood, E. C., Dyken, J. D. V., Cruickshank, T. E., Wade, M. J., & Moczek, A. P. (2009) · BioEssays · doi:10.1002/bies.200900132 · Cited by 272 · see citing works
Ovsyannikova, I. G., Haralambieva, I. H., Crooke, S. N., Poland, G. A., & Kennedy, R. B. (2020) · Immunological Reviews · doi:10.1111/imr.12897 · Cited by 258 · see citing works
The landscape of sex-differential transcriptome and its consequent selection in human adults
Gershoni, M., & Pietrokovski, S. (2017) · BMC Biology · doi:10.1186/s12915-017-0352-z · Cited by 267 · see citing works
Evolution of protein-coding genes in Drosophila
Larracuente, A. M., Sackton, T. B., Greenberg, A. J., Wong, A., Singh, N. D., Sturgill, D. M., Zhang, Y., Oliver, B., & Clark, A. G. (2008) · Trends in Genetics · doi:10.1016/j.tig.2007.12.001 · Cited by 258 · see citing works
Sex-chromosome evolution: recent progress and the influence of male and female heterogamety
Ellegren, H. (2011) · Nature Reviews Genetics · doi:10.1038/nrg2948 · Cited by 253 · see citing works
Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes
Ellegren, H., Hultin‐Rosenberg, L., Brunström, B., Dencker, L., Kultima, K., & Scholz, B. (2007) · BMC Biology · doi:10.1186/1741-7007-5-40 · Cited by 247 · see citing works
Bucky Ball Organizes Germ Plasm Assembly in Zebrafish
Bontems, F., Gautier‐Stein, A., Marlow, F. L., Lyautey, J., Gupta, T., Mullins, M. C., & Dosch, R. (2009) · Current Biology · doi:10.1016/j.cub.2009.01.038 · Cited by 245 · see citing works
Grath, S., & Parsch, J. (2016) · Annual Review of Genetics · doi:10.1146/annurev-genet-120215-035429 · Cited by 239 · see citing works
Demasculinization of X chromosomes in the Drosophila genus
Sturgill, D. M., Zhang, Y., Parisi, M. J., & Oliver, B. (2007) · Nature · doi:10.1038/nature06330 · Cited by 238 · see citing works
Speciation through evolution of sex-linked genes
Qvarnström, A., & Bailey, R. I. (2008) · Heredity · doi:10.1038/hdy.2008.93 · Cited by 235 · see citing works
Are homologies in vertebrate sex determination due to shared ancestry or to limited options?
Graves, J. A. M., & Peichel, C. L. (2010) · Genome biology · doi:10.1186/gb-2010-11-4-205 · Cited by 235 · see citing works
Bohring, A., Stamm, T., Spaich, C., Haase, C., Spree, K., Hehr, U., Hoffmann, M., Ledig, S., Sel, S., Wieacker, P., et al. (2009) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2009.06.001 · Cited by 232 · see citing works
Rapid Evolution of Sex Pheromone-Producing Enzyme Expression in Drosophila
Shirangi, T. R., Dufour, H. D., Williams, T. M., & Carroll, S. B. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000168 · Cited by 222 · see citing works
Sexual selection drives evolution and rapid turnover of male gene expression
Harrison, P. W., Wright, A. E., Zimmer, F., Dean, R., Montgomery, S. H., Pointer, M. A., & Mank, J. E. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1501339112 · Cited by 228 · see citing works
Behura, S. K., & Severson, D. W. (2012) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2012.00242.x · Cited by 221 · see citing works
Elucidating the Role of Gonadal Hormones in Sexually Dimorphic Gene Coexpression Networks
van Nas, A., GuhaThakurta, D., Wang, S. S., Yehya, N., Horvath, S., Zhang, B., Ingram-Drake, L. A., Chaudhuri, G., Schadt, E. E., Drake, T. A., et al. (2008) · Endocrinology · doi:10.1210/en.2008-0563 · Cited by 220 · see citing works
Vibranovski, M. D., Lopes, H. F., Karr, T. L., & Long, M. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000731 · Cited by 214 · see citing works
Sex differences in the brain: Implications for behavioral and biomedical research
Choleris, E., Galea, L. A. M., Sohrabji, F., & Frick, K. M. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.07.005 · Cited by 214 · see citing works
Phylogeny and Evolution of the Brown Algae
Bringloe, T. T., Starko, S., Wade, R. M., Vieira, C., Kawai, H., Clerck, O. D., Cock, J. M., Coelho, S. M., Destombe, C., Valéro, M., et al. (2020) · Critical Reviews in Plant Sciences · doi:10.1080/07352689.2020.1787679 · Cited by 204 · see citing works
EFFECTIVE POPULATION SIZE AND THE FASTER-X EFFECT: AN EXTENDED MODEL
Viçoso, B., & Charlesworth, B. (2009) · Evolution · doi:10.1111/j.1558-5646.2009.00719.x · Cited by 202 · see citing works
Sex-Biased Transcriptome Evolution in Drosophila
Assis, R., Zhou, Q., & Bachtrog, D. (2012) · Genome Biology and Evolution · doi:10.1093/gbe/evs093 · Cited by 195 · see citing works
Why estrogens matter for behavior and brain health
Galea, L. A. M., Frick, K. M., Hampson, E., Sohrabji, F., & Choleris, E. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.03.024 · Cited by 180 · see citing works
The transcriptional architecture of phenotypic dimorphism
Mank, J. E. (2017) · Nature Ecology & Evolution · doi:10.1038/s41559-016-0006 · Cited by 176 · see citing works
THE GENOMIC LOCATION OF SEXUALLY ANTAGONISTIC VARIATION: SOME CAUTIONARY COMMENTS
Fry, J. D. (2009) · Evolution · doi:10.1111/j.1558-5646.2009.00898.x · Cited by 177 · see citing works
A high resolution atlas of gene expression in the domestic sheep (Ovis aries)
Clark, E. L., Bush, S. J., McCulloch, M. E. B., Farquhar, I., Young, R. A., Lefèvre, L., Pridans, C., Tsang, H., Wu, C., Afrasiabi, C., et al. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006997 · Cited by 170 · see citing works
A Haploid System of Sex Determination in the Brown Alga Ectocarpus sp.
Ahmed, S., Cock, J. M., Pessia, E., Luthringer, R., Cormier, A., Robuchon, M., Sterck, L., Peters, A. F., Dittami, S. M., Corre, E., et al. (2014) · Current Biology · doi:10.1016/j.cub.2014.07.042 · Cited by 173 · see citing works
van Doorn, G. S. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04573.x · Cited by 173 · see citing works
Relaxed selection is a precursor to the evolution of phenotypic plasticity
Hunt, B. G., Ometto, L., Wurm, Y., Shoemaker, D., Yi, S. V., Keller, L., & Goodisman, M. A. D. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104825108 · Cited by 173 · see citing works
Pleiotropic Constraint Hampers the Resolution of Sexual Antagonism in Vertebrate Gene Expression
Mank, J. E., Hultin‐Rosenberg, L., Zwahlen, M., & Ellegren, H. (2007) · The American Naturalist · doi:10.1086/523954 · Cited by 172 · see citing works
Muyle, A., Zemp, N., Deschamps, C., Mousset, S., Widmer, A., & Marais, G. A. B. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001308 · Cited by 168 · see citing works
Sex differences in the human peripheral blood transcriptome
Jansen, R., Batista, S., Brooks, A. I., Tischfield, J. A., Willemsen, G. A. H. M., van Grootheest, G., Hottenga, J., Milaneschi, Y., Mbarek, H., Madar, V., et al. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-33 · Cited by 166 · see citing works
Chronotherapy and the molecular clock: Clinical implications in oncology☆
Innominato, P. F., Lévi, F., & Bjarnason, G. A. (2010) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2010.06.002 · Cited by 165 · see citing works
Two sexes, one genome: the evolutionary dynamics of intralocus sexual conflict
Pennell, T. M., & Morrow, E. H. (2013) · Ecology and Evolution · doi:10.1002/ece3.540 · Cited by 164 · see citing works
Epigenetic regulation of autosomal gene expression by sex chromosomes
Wijchers, P. J., & Festenstein, R. (2011) · Trends in Genetics · doi:10.1016/j.tig.2011.01.004 · Cited by 164 · see citing works
Comparative genomics and the study of evolution by natural selection
Ellegren, H. (2008) · Molecular Ecology · doi:10.1111/j.1365-294x.2008.03954.x · Cited by 161 · see citing works
Rosvall, K. A., Burns, C. M. B., Barske, J., Goodson, J. L., Schlinger, B. A., Sengelaub, D. R., & Ketterson, E. D. (2012) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2012.0442 · Cited by 157 · see citing works
Sex differences in the developmental origins of hypertension and cardiorenal disease
Gilbert, J. S., & Nijland, M. J. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90724.2008 · Cited by 159 · see citing works
Mouse Models for Evaluating Sex Chromosome Effects that Cause Sex Differences in Non‐Gonadal Tissues
Arnold, A. P. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01831.x · Cited by 157 · see citing works
The different levels of genetic diversity in sex chromosomes and autosomes
Ellegren, H. (2009) · Trends in Genetics · doi:10.1016/j.tig.2009.04.005 · Cited by 157 · see citing works
Sex differences in energy metabolism: natural selection, mechanisms and consequences
Mauvais‐Jarvis, F. (2023) · Nature Reviews Nephrology · doi:10.1038/s41581-023-00781-2 · Cited by 159 · see citing works
Evolution of Sex Chromosomes in Insects
Kaiser, V. B., & Bachtrog, D. (2010) · Annual Review of Genetics · doi:10.1146/annurev-genet-102209-163600 · Cited by 156 · see citing works
Ferreira, P. G., Patalano, S., Chauhan, R., ffrench‐Constant, R. H., Gabaldón, T., Guigó, R., & Sumner, S. (2013) · Genome biology · doi:10.1186/gb-2013-14-2-r20 · Cited by 155 · see citing works
Viçoso, B., Kaiser, V. B., & Bachtrog, D. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1217027110 · Cited by 152 · see citing works
Meisel, R. P. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr010 · Cited by 136 · see citing works
Disentangling the relationship between sex-biased gene expression and X-linkagePreprint
Meisel, R. P., Malone, J. H., & Clark, A. G. (2012) · Genome Research · doi:10.1101/gr.132100.111 · Cited by 143 · see citing works
SEX: DIFFERENCES IN MUTATION, RECOMBINATION, SELECTION, GENE FLOW, AND GENETIC DRIFT
Hedrick, P. W. (2007) · Evolution · doi:10.1111/j.1558-5646.2007.00250.x · Cited by 142 · see citing works
Sex gap in aging and longevity: can sex chromosomes play a role?
Marais, G. A. B., Gaillard, J., Vieira, C. P., Plotton, I., Sanlaville, D., Gueyffier, F., & Lemaître, J. (2018) · Biology of Sex Differences · doi:10.1186/s13293-018-0181-y · Cited by 141 · see citing works
Elashoff, M. R., Wingrove, J. A., Beineke, P., Daniels, S. E., Tingley, W. G., Rosenberg, S. J., Vörös, S., Kraus, W. E., Ginsburg, G. S., Schwartz, R. S., et al. (2011) · BMC Medical Genomics · doi:10.1186/1755-8794-4-26 · Cited by 139 · see citing works
Trier, C. N., Hermansen, J. S., Sætre, G., & Bailey, R. I. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004075 · Cited by 137 · see citing works
Faster-Z Evolution Is Predominantly Due to Genetic Drift
Mank, J. E., Nam, K., & Ellegren, H. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp282 · Cited by 140 · see citing works
The Genomics of Sexual Conflict
Rowe, L., Chenoweth, S. F., & Agrawal, A. F. (2018) · The American Naturalist · doi:10.1086/698198 · Cited by 136 · see citing works
Sexual Dimorphism and the Evolution of Sex-Biased Gene Expression in the Brown Alga Ectocarpus
Lipinska, A. P., Cormier, A., Luthringer, R., Peters, A. F., Corre, E., Gachon, C. M. M., Cock, J. M., & Coelho, S. M. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv049 · Cited by 135 · see citing works
Zhang, Y., Castillo-Morales, A., Jiang, M., Zhu, Y., Hu, L., Urrutia, A. O., Kong, X., & Hurst, L. D. (2013) · Molecular Biology and Evolution · doi:10.1093/molbev/mst148 · Cited by 132 · see citing works
The evolution of sex differences in disease
Morrow, E. H. (2015) · Biology of Sex Differences · doi:10.1186/s13293-015-0023-0 · Cited by 131 · see citing works
Age-dependent chromosomal distribution of male-biased genes in DrosophilaPreprint
Zhang, Y. E., Vibranovski, M. D., Krinsky, B. H., & Long, M. (2010) · Genome Research · doi:10.1101/gr.107334.110 · Cited by 130 · see citing works
Dosage Compensation in MammalsPreprint
Brockdorff, N., & Turner, B. M. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a019406 · Cited by 129 · see citing works
EVIDENCE FOR STRONG INTRALOCUS SEXUAL CONFLICT IN THE INDIAN MEAL MOTH, PLODIA INTERPUNCTELLA
Lewis, Z., Wedell, N., & Hunt, J. (2011) · Evolution · doi:10.1111/j.1558-5646.2011.01267.x · Cited by 129 · see citing works
Balancing Selection in Species with Separate Sexes: Insights from Fisher’s Geometric Model
Connallon, T., & Clark, A. G. (2014) · Genetics · doi:10.1534/genetics.114.165605 · Cited by 129 · see citing works
Freedman, J. E., Larson, M. G., Tanrıverdi, K., O’Donnell, C. J., Morin, K. M., Hakanson, A. S., Vasan, R. S., Johnson, A. D., Iafrati, M. D., & Benjamin, E. J. (2010) · Circulation · doi:10.1161/circulationaha.109.928192 · Cited by 129 · see citing works
The Ontogeny and Evolution of Sex-Biased Gene Expression in Drosophila melanogaster
Perry, J. C., Harrison, P. W., & Mank, J. E. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu072 · Cited by 128 · see citing works
Sex differences in disease genetics: evidence, evolution, and detection
Gilks, W. P., Abbott, J. K., & Morrow, E. H. (2014) · Trends in Genetics · doi:10.1016/j.tig.2014.08.006 · Cited by 123 · see citing works
Sexual selection predicts the rate and direction of colour divergence in a large avian radiation
Cooney, C. R., Varley, Z. K., Nouri, L. O., Moody, C. J., Jardine, M. D., & Thomas, G. H. (2019) · Nature Communications · doi:10.1038/s41467-019-09859-7 · Cited by 127 · see citing works
Masculinization of Gene Expression Is Associated with Exaggeration of Male Sexual Dimorphism
Pointer, M. A., Harrison, P. W., Wright, A. E., & Mank, J. E. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003697 · Cited by 127 · see citing works
Y recombination arrest and degeneration in the absence of sexual dimorphism
Lenormand, T., & Roze, D. (2022) · Science · doi:10.1126/science.abj1813 · Cited by 124 · see citing works
Sex-Specific Selection and Sex-Biased Gene Expression in Humans and Flies
Cheng, C., & Kirkpatrick, M. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006170 · Cited by 121 · see citing works
Sex differences in microRNA regulation of gene expression: no smoke, just miRs
Morgan, C. P., & Bale, T. L. (2012) · Biology of Sex Differences · doi:10.1186/2042-6410-3-22 · Cited by 118 · see citing works
The evolution of gene expression and the transcriptome–phenotype relationship
Harrison, P. W., Wright, A. E., & Mank, J. E. (2011) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2011.12.004 · Cited by 121 · see citing works
The Resolution of Sexual Antagonism by Gene Duplication
Connallon, T., & Clark, A. G. (2011) · Genetics · doi:10.1534/genetics.110.123729 · Cited by 119 · see citing works
Baines, J. F., Sawyer, S. A., Hartl, D. L., & Parsch, J. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn111 · Cited by 119 · see citing works
Hypothesis testing for network data in functional neuroimaging
Ginestet, C. E., Li, J., Balachandran, P., Rosenberg, S., & Kolaczyk, E. D. (2017) · The Annals of Applied Statistics · doi:10.1214/16-aoas1015 · Cited by 116 · see citing works
Ghiselli, F., Milani, L., Chang, P. L., Hedgecock, D., Davis, J. P., Nuzhdin, S. V., & Passamonti, M. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr248 · Cited by 115 · see citing works
Sex-Biased Gene Expression and Sexual Conflict throughout Development: Table 1.Preprint
Ingleby, F. C., Flis, I., & Morrow, E. H. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a017632 · Cited by 115 · see citing works
Connallon, T., & Clark, A. G. (2010) · Evolution · doi:10.1111/j.1558-5646.2010.01136.x · Cited by 114 · see citing works
Small, C. M., Carney, G. E., Mo, Q., Vannucci, M., & Jones, A. G. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-579 · Cited by 113 · see citing works
Olsson, M. M., Pauliny, A., Wapstra, E., Uller, T., Schwartz, T. S., & Blomqvist, D. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017473 · Cited by 109 · see citing works
Prince, E. G., Kirkland, D., & Demuth, J. P. (2010) · Genome Biology and Evolution · doi:10.1093/gbe/evq024 · Cited by 111 · see citing works
Connallon, T., & Clark, A. G. (2012) · Genetics · doi:10.1534/genetics.111.137117 · Cited by 110 · see citing works
Ontogenetic Complexity of Sexual Dimorphism and Sex-Specific Selection
Mank, J. E., Nam, K., Brunström, B., & Ellegren, H. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq042 · Cited by 110 · see citing works
- Authors
- Ellegren, H., & Parsch, J.
- Affiliations
- Uppsala University (SE)
- Ludwig-Maximilians-Universität München (DE)
- Corresponding author
- Ellegren, Hans
- Parsch, John
- Venue
- Nature Reviews Genetics
- Published
- 2007-08-07
- Volume
- 8
- Issue
- 9
- Pages
- 689-698
- ISSN
- 1471-0056 (ISSN-L)
- 1471-0064
- OpenAlex
- W2057277929
- Cited by
- 925
- References
- 90
- Citations by year
- 2026: 27 · 2025: 41 · 2024: 39 · 2023: 58 · 2022: 58 · 2021: 62 · 2020: 39 · 2019: 53 · 2018: 60 · 2017: 53 · 2016: 55 · 2015: 41 · 2014: 68 · 2013: 46 · 2012: 40
- FWCI
- 4.57
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Genetics (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Vetenskapsrådet
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Keywords
- sex-biased genes, sex-biased gene expression, sex differences, gene expression patterns, sexual dimorphism, phenotypic diversity, selection, medical genetics
- MeSH terms
- Animals, Chromosome Mapping, Codon, Female, Gene Expression Regulation, Humans, Male, Selection, Genetic, Sex Characteristics, Sex Chromosomes, Open Reading Frames, Gene Dosage, Evolution, Molecular, Genes, X-Linked, Genes, Y-Linked
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review