The faster-X effect: integrating theory and data
Open accessAbstract
Population genetics theory predicts that X (or Z) chromosomes could play disproportionate roles in speciation and evolutionary divergence, and recent genome-wide analyses have identified situations in which X or Z-linked divergence exceeds that on the autosomes (the so-called 'faster-X effect'). Here, we summarize the current state of both the theory and data surrounding the study of faster-X evolution. Our survey indicates that the faster-X effect is pervasive across a taxonomically diverse array of evolutionary lineages. These patterns could be informative of the dominance or recessivity of beneficial mutations and the nature of genetic variation acted upon by natural selection. We also identify several aspects of disagreement between these empirical results and the population genetic models used to interpret them. However, there are clearly delineated aspects of the problem for which additional modeling and collection of genomic data will address these discrepancies and provide novel insights into the population genetics of adaptation.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Half of the false negatives may be related to faster X chromosome evolution.
“Manual investigation of misclassifications showed that false positives mostly represent partial or full gene duplications (actual co-orthologous loci) and that half of the false negatives may be related to faster X chromosome evolution (17) (fig. S5–S6).”
From Integrating gene annotation with orthology inference at scale (2023) · cites this paper as [17]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
An integrated map of genetic variation from 1,092 human genomes
The 1000 Genomes Project Consortium (2012) · Nature · doi:10.1038/nature11632 · Cited by 7,711 · see citing works
On the rate of molecular evolution
Kimura, M., & Ohta, T. (1971) · Journal of Molecular Evolution · doi:10.1007/bf01659390 · Cited by 195 · see citing works
Flagged first, then by citations
Research works printed but not linked: 76
- [1]Begun DJ Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans PLoS Biol 2007 5 e310 17988176 PMC2062478
- [2]Sella G Pervasive natural selection in the Drosophila genome? PLoS Genet 2009 5 0 PMC2684638 19503600
- [4]Mackay TFC The Drosophila melanogaster genetic reference panel Nature 2012 482 173 178 22318601 PMC3683990
- [5]Gossmann TI The effect of variation in the effective population size on the rate of adaptive molecular evolution in eukaryotes Genome Biol. Evol 2012 4 658 667 22436998 PMC3381672
- [6]Haldane JBS A mathematical theory of natural and artificial selection, Part V: selection and mutation Proc. Camb. Philos. Soc 1927 28 838 844
- [7]Vicoso B Charlesworth B Evolution on the X chromosome: unusual patterns and processes Nat. Rev. Genet 2006 7 645 653 16847464
- [9]Orr HA Betancourt AJ Haldane’s sieve and adaptation from the standing genetic variation Genetics 2001 157 875 884 11157004 PMC1461537
- [10]Kirkpatrick M Hall DW Male-biased mutation, sex linkage, and the rate of adaptive evolution Evolution 2004 58 437 440 15068360
- [11]Vicoso B Charlesworth B effective population size and the faster-X effect: an extended model Evolution 2009 63 2413 26 19473388
- [12]Mank JE Effective population size and the faster-X effect: empirical results and their interpretation Evolution 2010 64 663 674 19796145
- [13]Orr HA The population genetics of beneficial mutations Philos. Trans. R. Soc. Lond., B, Biol. Sci 2010 365 1195 1201 20308094 PMC2871816
- [14]Connallon T Impact of genetic architecture on the relative rates of X versus autosomal adaptive substitution Mol. Biol. Evol 2012 29 1933 1942 22319138 PMC3408067
- [16]Kimura M Ohta T Theoretical aspects of population genetics 1971 Princeton University Press 5162676
- [17]Ellegren H Characteristics, causes and evolutionary consequences of male-biased mutation Proc. R. Soc. Lond., B, Biol. Sci 2007 274 1 10 PMC1679872 17134994
- [18]Xu K Lineage-specific variation in slow- and fast-X evolution in primates Evolution 2012 66 1751 1761 22671544
- [19]Weissman DB Barton NH Limits to the rate of adaptive substitution in sexual populations PLoS Genet 2012 8 e1002740 22685419 PMC3369949
- [21]Stern DL Orgogozo V Is genetic evolution predictable? Science 2009 323 746 751 19197055 PMC3184636
- [22]Christin PA Causes and evolutionary significance of genetic convergence Trends Genet 2010 26 400 405 20685006
- [23]Mank JE Some inconvenient truths about sex chromosome dosage compensation and the potential role of sexual conflict Evolution 2011 65 2133 2144 21790564
- [24]Meisel RP Disentangling the relationship between sex-biased gene expression and X-linkage Genome Res 2012 22 1255 1265 22499666 PMC3396367
- [25]Sellis D Heterozygote advantage as a natural consequence of adaptation in diploids Proc. Natl. Acad. Sci. U.S.A 2011 108 20666 20671 22143780 PMC3251125
- [26]McDonald JH Kreitman M Adaptive protein evolution at the Adh locus in Drosophila Nature 1991 351 652 654 1904993
- [27]Eyre-Walker A The genomic rate of adaptive evolution Trends Ecol. Evol 2006 21 569 575 16820244
- [28]Fay JC Weighing the evidence for adaptation at the molecular level Trends Genet 2011 27 343 349 21775012 PMC3185218
- [29]Betancourt AJ A test for faster X evolution in Drosophila Mol. Biol. Evol 2002 19 1816 1819 12270910
- [30]Counterman BA Using comparative genomic data to test for fast-X evolution Evolution 2004 58 656 660 15119449
- [31]Musters H A genomic comparison of faster-sex, faster-X, and faster-male evolution between Drosophila melanogaster and Drosophila pseudoobscura J. Mol. Evol 2006 62 693 700 16612543
- [32]Thornton K X chromosomes and autosomes evolve at similar rates in Drosophila: no evidence for faster-X protein evolution Genome Res 2006 16 498 504 16520459 PMC1457026
- [33]Singh ND Contrasting the e cacy of selection on the X and autosomes in Drosophila Mol. Biol. Evol 2008 25 454 467 18083702
- [34]Vicoso B A multispecies approach for comparing sequence evolution of X-linked and autosomal sites in Drosophila Genet. Res 2008 90 421 431 19061532
- [35]Grath S Parsch J Rate of amino acid substitution is influenced by the degree and conservation of male-biased transcription over 50 million years of Drosophila evolution Genome Biol. Evol 2012 4 346 359 22321769 PMC3318448
- [36]Zhou Q Bachtrog D Sex-specific adaptation drives early sex chromosome evolution in Drosophila Science 2012 337 341 345 22822149 PMC4107656
- [37]Thornton K Long M Rapid divergence of gene duplicates on the Drosophila melanogaster X chromosome Mol. Biol. Evol 2002 19 918 925 12032248
- [38]Bhutkar A Chromosomal rearrangement inferred from comparisons of 12 Drosophila genomes Genetics 2008 179 1657 1680 18622036 PMC2475759
- [39]Hu TT A second-generation assembly of the Drosophila simulans genome provides new insights into patterns of lineage-specific divergence Genome Res 2013 23 89 98 22936249 PMC3530686
- [40]Lu J Wu CI Weak selection revealed by the whole-genome comparison of the X chromosome and autosomes of human and chimpanzee Proc. Natl. Acad. Sci. U.S.A 2005 102 4063 4067 15728731 PMC554819
- [41]Nielsen R A scan for positively selected genes in the genomes of humans and chimpanzees PLoS Biol 2005 3 e170 15869325 PMC1088278
- [42]Hvilsom C Extensive X-linked adaptive evolution in central chimpanzees Proc. Natl. Acad. Sci. U.S.A 2012 109 2054 2059 22308321 PMC3277544
- [43]Baines JF Harr B Reduced X-linked diversity in derived populations of house mice Genetics 2007 175 1911 1921 17287527 PMC1855135
- [44]Borge T Contrasting patterns of polymorphism and divergence on the Z chromosome and autosomes in two Ficedula flycatcher species Genetics 2005 171 1861 1873 15956661 PMC1456110
- [45]Mank JE Fast-X on the Z: rapid evolution of sex-linked genes in birds Genome Res 2007 17 618 624 17416747 PMC1855182
- [46]Ellegren H Genomic evidence for a large-Z effect Proc. R. Soc. Lond., B, Biol. Sci 2009 276 361 366 PMC2674357 18826931
- [47]Sackton TB Positive selection drives faster-Z evolution in silkmoths in review arXiv, 1304.7670 PMC4122604 24826901 · arXiv
- [48]Mank JE Faster-Z evolution is predominantly due to genetic drift Mol. Biol. Evol 2010 27 661 670 19926635
- [49]Jaquiery J Accelerated evolution of sex chromosomes in aphids, an X0 system Mol. Biol. Evol 2012 29 837 847 21998277
- [50]Presgraves DC Recombination enhances protein adaptation in Drosophila melanogaster Curr. Biol 2005 15 1651 1656 16169487
- [51]Connallon T Adaptive protein evolution of X-linked and autosomal genes in Drosophila: implications for faster-X hypotheses Mol. Biol. Evol 2007 24 2566 2572 17884828
- [52]Baines JF Effects of X-linkage and sex-biased gene expression on the rate of adaptive protein evolution in Drosophila Mol. Biol. Evol 2008 25 1639 1650 18477586 PMC2727381
- [53]Presgraves DC Sex chromosomes and speciation in Drosophila Trends Genet 2008 24 336 343 18514967 PMC2819171
- [54]Langley CH Genomic variation in natural populations of Drosophila melanogaster Genetics 2012 192 533 598 22673804 PMC3454882
- [55]Thornton K Long M Excess of amino acid substitutions relative to polymorphism between X-linked duplications in Drosophila melanogaster Mol. Biol. Evol 2005 22 273 284 15483321
- [56]Carneiro M Evidence for widespread positive and purifying selection across the european rabbit (Oryctolagus cuniculus) genome Mol. Biol. Evol 2012 29 1837 1849 22319161 PMC3375474
- [57]Ellegren H The genomic landscape of species divergence in Ficedula flycatchers Nature 2012 491 756 760 23103876
- [58]Hogner S Increased divergence but reduced variation on the Z chromosome relative to autosomes in Ficedula flycatchers: differential introgression or the faster-Z effect? Ecol. Evol 2012 2 379 396 22423331 PMC3298950
- [59]Müller L Inter- and intraspecific variation in Drosophila genes with sex-biased expression Int. J. Evol. Biol 2012 2012 963976 22315698 PMC3270394
- [60]Torgerson DG Singh RS Sex-linked mammalian sperm proteins evolve faster than autosomal ones Mol. Biol. Evol 2003 20 1705 1709 12832636
- [61]Torgerson DG Singh RS Enhanced adaptive evolution of sperm-expressed genes on the mammalian X chromosome Heredity 2006 96 39 44 16175195
- [62]Khaitovich P Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees Science 2005 309 1850 1854 16141373
- [63]Stevenson B Rapid evolution of cancer/testis genes on the X chromosome BMC Genomics 2007 8 129 17521433 PMC1890293
- [64]Guo X Rapid evolution of mammalian X-linked testis microR-NAs BMC Genomics 2009 10 97 19257908 PMC2660371
- [65]Sin HS Human postmeiotic sex chromatin and its impact on sex chromosome evolution Genome Res 2012 22 827 836 22375025 PMC3337429
- [66]Connallon T Clark AG Association between sex-biased gene expression and mutations with sex-specific phenotypic consequences in Drosophila Genome Biol Evol 2011 3 151 155 21292631 PMC3048362
- [67]Charlesworth B Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation Nat. Rev. Genet 2009 10 195 205 19204717
- [68]Betancourt AJ A pseudohitchhiking model of X vs. autosomal diversity Genetics 2004 168 2261 2269 15611190 PMC1448734
- [69]Vicoso B Charlesworth B Recombination rates may a ect the ratio of X to autosomal noncoding polymorphism in African populations of Drosophila melanogaster Genetics 2009 181 1699 1701 19189953 PMC2666533
- [70]Charlesworth B The role of background selection in shaping patterns of molecular evolution and variation: evidence from variability on the Drosophila X chromosome Genetics 2012 191 233 246 22377629 PMC3338263
- [71]Hermisson J Pennings PS Soft sweeps: molecular population genetics of adaptation from standing genetic variation Genetics 2005 169 2335 2352 15716498 PMC1449620
- [72]Brawand D The evolution of gene expression levels in mammalian organs Nature 2011 478 343 348 22012392
- [73]Kayserili MA An excess of gene expression divergence on the X chromosome in Drosophila embryos: implications for the faster-X hypothesis PLoS Genet 2012 8 e1003200 23300473 PMC3531489
- [74]Llopart A The rapid evolution of X-linked male-biased gene expression and the large-X effect in Drosophila yakuba, D. santomea, and their hybirds Mol. Biol. Evol 2012 29 3873 3886 22844069
- [75]Meisel RP Faster-X evolution of gene expression in Drosophila PLoS Genet 2012 8 e1003013 23071459 PMC3469423
- [76]Meiklejohn CD Rapid evolution of male-biased gene expression in Drosophila Proc. Natl. Acad. Sci. U.S.A 2003 100 9894 9899 12907700 PMC188344
- [77]Charlesworth J Eyre-Walker A The McDonald-Kreitman test and slightly deleterious mutations Mol. Biol. Evol 2008 25 1007 1015 18195052
- [78]Campos JL Codon usage bias and effective population sizes on the X chromosome versus the autosomes in Drosophila melanogaster Mol. Biol. Evol 2013 30 811 823 23204387 PMC3603305
- [79]Messer PW Petrov DA The McDonald-Kreitman test and its extensions under frequent adaptation: problems and solutions in review arXiv, 1211.0060 · arXiv
- [80]Meiklejohn CD Tao Y Genetic conflict and sex chromosome evolution Trends Ecol. Evol 2010 25 215 223 19931208 PMC2843792
Cited by
Sorted by citations
The Strength of Selection against Neanderthal Introgression
Juric, I., Aeschbacher, S., & Coop, G. (2016) · PLOS Genetics · doi:10.1371/journal.pgen.1006340 · Cited by 309 · see citing works
Integrating gene annotation with orthology inference at scale
Kirilenko, B. M., Munegowda, C., Osipova, E., Jebb, D., Sharma, V., Blumer, M., Morales, A. E., Ahmed, A.-W., Kontopoulos, D.-G., Hilgers, L., et al. (2023) · Science · doi:10.1126/science.abn3107 · Cited by 209 · see citing works
- Authors
- Meisel, R. P., & Connallon, T.
- Affiliations
- Cornell University (US)
- Corresponding author
- Meisel, Richard P.
- Venue
- Trends in Genetics
- Publisher
- Elsevier BV
- Published
- 2013-09
- Volume
- 29
- Issue
- 9
- Pages
- 537-544
- ISSN
- 0168-9525 (ISSN-L)
- PMC
- PMC3755111
- OpenAlex
- W2171269638
- Cited by
- 238
- References
- 2
- Citations by year
- 2026: 17 · 2025: 14 · 2024: 25 · 2023: 15 · 2022: 44 · 2021: 18 · 2020: 11 · 2019: 12 · 2018: 25 · 2017: 11 · 2016: 17 · 2015: 18 · 2014: 10 · 2013: 1
- FWCI
- 1.86
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Trends in Genetics (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of General Medical Sciences (R01GM064590)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Keywords
- X chromosome, Z chromosome, sex chromosomes, speciation, evolutionary divergence, autosomes, natural selection, population genetic models
- MeSH terms
- Adaptation, Physiological, Animals, Pan troglodytes, Drosophila, Genetics, Population, Humans, Models, Genetic, Mutation, Selection, Genetic, Genetic Variation, X Chromosome, Evolution, Molecular, Empirical Research, Genetic Loci, Genetic Association Studies
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