FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / J Mol Evol / Mammalian male mutation bias: impacts of generation time and...
Journal of molecular evolution2006; 63(4); 537-544; doi: 10.1007/s00239-005-0308-8

Mammalian male mutation bias: impacts of generation time and regional variation in substitution rates.

Abstract: In mammals, males undergo a greater number of germline cell divisions compared with females. Thus, the male germline accumulates more DNA replication errors, which result in male mutation bias-a higher mutation rate for males than for females. The phenomenon of male mutation bias has been investigated mostly for rodents and primates, however, it has not been studied in detail for other mammalian orders. Here we sequenced and analyzed five introns of three genes (DBX/DBY, UTX/UTY, and ZFX/ZFY) homologous between X and Y chromosomes in several species of perissodactyls (horses and rhinos) and of primates. Male mutation bias was evident: substitution rate was higher for a Y chromosome intron than for its X chromosome homologue for all five intron pairs studied. Substitution rates varied regionally among introns sequenced on the same chromosome and this variation influenced male mutation bias inferred from each intron pair. Interestingly, we observed a positive correlation in substitution rates between homologous X and homologous Y introns as well as between orthologous primate and perissodactyl introns. The male-to-female mutation rate ratio estimated from concatenated sequences of five perissodactyl introns was 3.88 (95% CI = 2.90-6.07). Using the data generated here and estimates available in the literature, we compared male mutation bias among several mammalian orders. We conclude that male mutation bias is significantly higher for organisms with long generation times (primates, perissodactyls, and felids) than for organisms with short generation times (e.g., rodents) since the former undergo a greater number of male germline cell divisions.
Get Full Text
Publication Date: 2006-09-04 PubMed ID: 16955237DOI: 10.1007/s00239-005-0308-8Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • N.I.H.
  • Extramural
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research paper investigates the phenomenon of higher mutation rates in male mammals than females, known as male mutation bias, particularly among species with longer generation times such as primates, horses and rhinos. Derived from sequencing and analyzing introns of genes, this study reinforces the view that longer-generation species accumulate more DNA replication errors due to more number of male germline cell divisions, thus leading to a higher male mutation bias.

Objective and Methodology

  • The researchers’ primary goal was to understand the occurrence and degree of male mutation bias in various mammalian species, focusing mainly on perissodactyls and primates, given the limited information available for these species on the subject.
  • They sequenced and analyzed five introns of three genes homologous between X and Y chromosomes in the two aforementioned species.
  • The intron pairs’ substitution rates were studied, revealing higher rates for Y chromosome intron than its X chromosome counterpart.

Findings and Observations

  • The analysis revealed a clear male mutation bias: the substitution rate was consistently higher for a Y chromosome intron – associated with male lineage – than for its X chromosome counterpart.
  • Substitution rates varied regionally among introns sequenced on the same chromosome, meaning that different parts of the same chromosome mutated at different rates. This varying rate, in turn, influenced the degree of male mutation bias recorded.
  • A significant positive correlation was observed in substitution rates between homologous X and Y introns and also between orthologous primate and perissodactyl introns. This implies a consistent pattern of increased rates of genetic sequence change in both species groups and sexes.

Conclusions and Implications

  • The research estimated a male-to-female mutation rate ratio of 3.88 for perissodactyls, offering a quantitative measure of male mutation bias in this group.
  • By analyzing the data generated and comparing it with other literature, researchers confirmed a higher degree of male mutation bias in species that have longer generation times – such as primates, perissodactyls, and felines – due to the increased number of male germline cell divisions, and consequently, more cumulative DNA replication errors.
  • These findings not only fill a knowledge gap about male mutation bias in perissodactyls and primates but also offer potential explanations for differences in mutation rates among mammals based on their life history traits.

Cite This Article

APA
Goetting-Minesky MP, Makova KD. (2006). Mammalian male mutation bias: impacts of generation time and regional variation in substitution rates. J Mol Evol, 63(4), 537-544. https://doi.org/10.1007/s00239-005-0308-8

Publication

Journal of molecular evolution
ISSN: 0022-2844
NlmUniqueID: 0360051
Country: Germany
Language: English
Volume: 63
Issue: 4
Pages: 537-544

Researcher Affiliations

Goetting-Minesky, M Paula
  • Department of Biology, Center for Comparative Genomics and Bioinformatics, 518A Mueller Lab, Penn State University, University Park, PA 16803, USA.
Makova, Kateryna D

    MeSH Terms

    • Aging / physiology
    • Animals
    • Base Sequence
    • Genetic Variation
    • Humans
    • Introns / genetics
    • Male
    • Mutation / genetics
    • Phylogeny
    • Reproduction / physiology
    • Sex Characteristics
    • Time Factors

    Grant Funding

    • R01-GM072264 / NIGMS NIH HHS

    References

    This article includes 39 references
    1. Ptak SE, Roeder AD, Stephens M, Gilad Y, Pääbo S, Przeworski M. Absence of the TAP2 human recombination hotspot in chimpanzees.. PLoS Biol 2004 Jun;2(6):e155.
      pubmed: 15208713doi: 10.1371/journal.pbio.0020155google scholar: lookup
    2. Gaffney DJ, Keightley PD. The scale of mutational variation in the murid genome.. Genome Res 2005 Aug;15(8):1086-94.
      pubmed: 16024822doi: 10.1101/gr.3895005google scholar: lookup
    3. Goodman M, Grossman LI, Wildman DE. Moving primate genomics beyond the chimpanzee genome.. Trends Genet 2005 Sep;21(9):511-7.
      pubmed: 16009448doi: 10.1016/j.tig.2005.06.012google scholar: lookup
    4. Huang W, Chang BH, Gu X, Hewett-Emmett D, Li W. Sex differences in mutation rate in higher primates estimated from AMG intron sequences.. J Mol Evol 1997 Apr;44(4):463-5.
      pubmed: 9089087doi: 10.1007/pl00006166google scholar: lookup
    5. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees.. Mol Biol Evol 1987 Jul;4(4):406-25.
      pubmed: 3447015doi: 10.1093/oxfordjournals.molbev.a040454google scholar: lookup
    6. Lawson LJ, Hewitt GM. Comparison of substitution rates in ZFX and ZFY introns of sheep and goat related species supports the hypothesis of male-biased mutation rates.. J Mol Evol 2002 Jan;54(1):54-61.
      pubmed: 11734898doi: 10.1007/s00239-001-0017-xgoogle scholar: lookup
    7. Taylor J, Tyekucheva S, Zody M, Chiaromonte F, Makova KD. Strong and weak male mutation bias at different sites in the primate genomes: insights from the human-chimpanzee comparison.. Mol Biol Evol 2006 Mar;23(3):565-73.
      pubmed: 16280537doi: 10.1093/molbev/msj060google scholar: lookup
    8. Gibbs RA, Weinstock GM, Metzker ML, Muzny DM, Sodergren EJ, Scherer S, Scott G, Steffen D, Worley KC, Burch PE, Okwuonu G, Hines S, Lewis L, DeRamo C, Delgado O, Dugan-Rocha S, Miner G, Morgan M, Hawes A, Gill R, Celera, Holt RA, Adams MD, Amanatides PG, Baden-Tillson H, Barnstead M, Chin S, Evans CA, Ferriera S, Fosler C, Glodek A, Gu Z, Jennings D, Kraft CL, Nguyen T, Pfannkoch CM, Sitter C, Sutton GG, Venter JC, Woodage T, Smith D, Lee HM, Gustafson E, Cahill P, Kana A, Doucette-Stamm L, Weinstock K, Fechtel K, Weiss RB, Dunn DM, Green ED, Blakesley RW, Bouffard GG, De Jong PJ, Osoegawa K, Zhu B, Marra M, Schein J, Bosdet I, Fjell C, Jones S, Krzywinski M, Mathewson C, Siddiqui A, Wye N, McPherson J, Zhao S, Fraser CM, Shetty J, Shatsman S, Geer K, Chen Y, Abramzon S, Nierman WC, Havlak PH, Chen R, Durbin KJ, Egan A, Ren Y, Song XZ, Li B, Liu Y, Qin X, Cawley S, Worley KC, Cooney AJ, D'Souza LM, Martin K, Wu JQ, Gonzalez-Garay ML, Jackson AR, Kalafus KJ, McLeod MP, Milosavljevic A, Virk D, Volkov A, Wheeler DA, Zhang Z, Bailey JA, Eichler EE, Tuzun E, Birney E, Mongin E, Ureta-Vidal A, Woodwark C, Zdobnov E, Bork P, Suyama M, Torrents D, Alexandersson M, Trask BJ, Young JM, Huang H, Wang H, Xing H, Daniels S, Gietzen D, Schmidt J, Stevens K, Vitt U, Wingrove J, Camara F, Mar Albà M, Abril JF, Guigo R, Smit A, Dubchak I, Rubin EM, Couronne O, Poliakov A, Hübner N, Ganten D, Goesele C, Hummel O, Kreitler T, Lee YA, Monti J, Schulz H, Zimdahl H, Himmelbauer H, Lehrach H, Jacob HJ, Bromberg S, Gullings-Handley J, Jensen-Seaman MI, Kwitek AE, Lazar J, Pasko D, Tonellato PJ, Twigger S, Ponting CP, Duarte JM, Rice S, Goodstadt L, Beatson SA, Emes RD, Winter EE, Webber C, Brandt P, Nyakatura G, Adetobi M, Chiaromonte F, Elnitski L, Eswara P, Hardison RC, Hou M, Kolbe D, Makova K, Miller W, Nekrutenko A, Riemer C, Schwartz S, Taylor J, Yang S, Zhang Y, Lindpaintner K, Andrews TD, Caccamo M, Clamp M, Clarke L, Curwen V, Durbin R, Eyras E, Searle SM, Cooper GM, Batzoglou S, Brudno M, Sidow A, Stone EA, Venter JC, Payseur BA, Bourque G, López-Otín C, Puente XS, Chakrabarti K, Chatterji S, Dewey C, Pachter L, Bray N, Yap VB, Caspi A, Tesler G, Pevzner PA, Haussler D, Roskin KM, Baertsch R, Clawson H, Furey TS, Hinrichs AS, Karolchik D, Kent WJ, Rosenbloom KR, Trumbower H, Weirauch M, Cooper DN, Stenson PD, Ma B, Brent M, Arumugam M, Shteynberg D, Copley RR, Taylor MS, Riethman H, Mudunuri U, Peterson J, Guyer M, Felsenfeld A, Old S, Mockrin S, Collins F. Genome sequence of the Brown Norway rat yields insights into mammalian evolution.. Nature 2004 Apr 1;428(6982):493-521.
      pubmed: 15057822doi: 10.1038/nature02426google scholar: lookup
    9. Whittle CA, Johnston MO. Male-driven evolution of mitochondrial and chloroplastidial DNA sequences in plants.. Mol Biol Evol 2002 Jun;19(6):938-49.
      pubmed: 12032250doi: 10.1093/oxfordjournals.molbev.a004151google scholar: lookup
    10. Li WH. Distribution of nucleotide differences between two randomly chosen cistrons in a finite population.. Genetics 1977 Feb;85(2):331-7.
      pubmed: 863231doi: 10.1093/genetics/85.2.331google scholar: lookup
    11. Makova KD, Li WH. Strong male-driven evolution of DNA sequences in humans and apes.. Nature 2002 Apr 11;416(6881):624-6.
      pubmed: 11948348doi: 10.1038/416624agoogle scholar: lookup
    12. Raudsepp T, Santani A, Wallner B, Kata SR, Ren C, Zhang HB, Womack JE, Skow LC, Chowdhary BP. A detailed physical map of the horse Y chromosome.. Proc Natl Acad Sci U S A 2004 Jun 22;101(25):9321-6.
      pubmed: 15197257doi: 10.1073/pnas.0403011101google scholar: lookup
    13. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees.. Mol Biol Evol 1993 May;10(3):512-26.
      pubmed: 8336541doi: 10.1093/oxfordjournals.molbev.a040023google scholar: lookup
    14. Lahn BT, Page DC. Four evolutionary strata on the human X chromosome.. Science 1999 Oct 29;286(5441):964-7.
      pubmed: 10542153doi: 10.1126/science.286.5441.964google scholar: lookup
    15. Makova KD, Yang S, Chiaromonte F. Insertions and deletions are male biased too: a whole-genome analysis in rodents.. Genome Res 2004 Apr;14(4):567-73.
      pubmed: 15059997doi: 10.1101/gr.1971104google scholar: lookup
    16. Shimmin LC, Chang BH, Li WH. Male-driven evolution of DNA sequences.. Nature 1993 Apr 22;362(6422):745-7.
      pubmed: 8469284doi: 10.1038/362745a0google scholar: lookup
    17. Pecon Slattery J, O'Brien SJ. Patterns of Y and X chromosome DNA sequence divergence during the Felidae radiation.. Genetics 1998 Mar;148(3):1245-55.
      pubmed: 9539439doi: 10.1093/genetics/148.3.1245google scholar: lookup
    18. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, Repping S, Pyntikova T, Ali J, Bieri T, Chinwalla A, Delehaunty A, Delehaunty K, Du H, Fewell G, Fulton L, Fulton R, Graves T, Hou SF, Latrielle P, Leonard S, Mardis E, Maupin R, McPherson J, Miner T, Nash W, Nguyen C, Ozersky P, Pepin K, Rock S, Rohlfing T, Scott K, Schultz B, Strong C, Tin-Wollam A, Yang SP, Waterston RH, Wilson RK, Rozen S, Page DC. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes.. Nature 2003 Jun 19;423(6942):825-37.
      pubmed: 12815422doi: 10.1038/nature01722google scholar: lookup
    19. Laird CD, McConaughy BL, McCarthy BJ. Rate of fixation of nucleotide substitutions in evolution.. Nature 1969 Oct 11;224(5215):149-54.
      pubmed: 5343515doi: 10.1038/224149a0google scholar: lookup
    20. Filatov DA, Charlesworth D. Substitution rates in the X- and Y-linked genes of the plants, Silene latifolia and S. dioica.. Mol Biol Evol 2002 Jun;19(6):898-907.
      pubmed: 12032246doi: 10.1093/oxfordjournals.molbev.a004147google scholar: lookup
    21. Chang BH, Shimmin LC, Shyue SK, Hewett-Emmett D, Li WH. Weak male-driven molecular evolution in rodents.. Proc Natl Acad Sci U S A 1994 Jan 18;91(2):827-31.
      pubmed: 8290607doi: 10.1073/pnas.91.2.827google scholar: lookup
    22. Chang BH, Li WH. Estimating the intensity of male-driven evolution in rodents by using X-linked and Y-linked Ube 1 genes and pseudogenes.. J Mol Evol 1995 Jan;40(1):70-7.
      pubmed: 7714913doi: 10.1007/BF00166597google scholar: lookup
    23. Raudsepp T, Kata SR, Piumi F, Swinburne J, Womack JE, Skow LC, Chowdhary BP. Conservation of gene order between horse and human X chromosomes as evidenced through radiation hybrid mapping.. Genomics 2002 Mar;79(3):451-7.
      pubmed: 11863376doi: 10.1006/geno.2002.6723google scholar: lookup
    24. Norman JE, Ashley MV. Phylogenetics of Perissodactyla and tests of the molecular clock.. J Mol Evol 2000 Jan;50(1):11-21.
      pubmed: 10654255doi: 10.1007/s002399910002google scholar: lookup
    25. Hellborg L, Ellegren H. Y chromosome conserved anchored tagged sequences (YCATS) for the analysis of mammalian male-specific DNA.. Mol Ecol 2003 Jan;12(1):283-91.
      pubmed: 12492896doi: 10.1046/j.1365-294x.2003.01702.xgoogle scholar: lookup
    26. Ellegren H, Fridolfsson AK. Male-driven evolution of DNA sequences in birds.. Nat Genet 1997 Oct;17(2):182-4.
      pubmed: 9326938doi: 10.1038/ng1097-182google scholar: lookup
    27. Hardison RC, Roskin KM, Yang S, Diekhans M, Kent WJ, Weber R, Elnitski L, Li J, O'Connor M, Kolbe D, Schwartz S, Furey TS, Whelan S, Goldman N, Smit A, Miller W, Chiaromonte F, Haussler D. Covariation in frequencies of substitution, deletion, transposition, and recombination during eutherian evolution.. Genome Res 2003 Jan;13(1):13-26.
      pubmed: 12529302doi: 10.1101/gr.844103google scholar: lookup
    28. Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood.. Comput Appl Biosci 1997 Oct;13(5):555-6.
      pubmed: 9367129doi: 10.1093/bioinformatics/13.5.555google scholar: lookup
    29. Lercher MJ, Williams EJ, Hurst LD. Local similarity in evolutionary rates extends over whole chromosomes in human-rodent and mouse-rat comparisons: implications for understanding the mechanistic basis of the male mutation bias.. Mol Biol Evol 2001 Nov;18(11):2032-9.
      pubmed: 11606699doi: 10.1093/oxfordjournals.molbev.a003744google scholar: lookup
    30. Kumar S, Tamura K, Nei M. MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment.. Brief Bioinform 2004 Jun;5(2):150-63.
      pubmed: 15260895doi: 10.1093/bib/5.2.150google scholar: lookup
    31. Li WH, Yi S, Makova K. Male-driven evolution.. Curr Opin Genet Dev 2002 Dec;12(6):650-6.
      pubmed: 12433577doi: 10.1016/s0959-437x(02)00354-4google scholar: lookup
    32. Bartosch-Härlid A, Berlin S, Smith NG, Møller AP, Ellegren H. Life history and the male mutation bias.. Evolution 2003 Oct;57(10):2398-406.
      pubmed: 14628927doi: 10.1554/03-036google scholar: lookup
    33. Springer MS, Murphy WJ, Eizirik E, O'Brien SJ. Placental mammal diversification and the Cretaceous-Tertiary boundary.. Proc Natl Acad Sci U S A 2003 Feb 4;100(3):1056-61.
      pubmed: 12552136doi: 10.1073/pnas.0334222100google scholar: lookup
    34. Ellegren H, Fridolfsson AK. Sex-specific mutation rates in salmonid fish.. J Mol Evol 2003 Apr;56(4):458-63.
      pubmed: 12664165doi: 10.1007/s00239-002-2416-zgoogle scholar: lookup
    35. Hellmann I, Prüfer K, Ji H, Zody MC, Pääbo S, Ptak SE. Why do human diversity levels vary at a megabase scale?. Genome Res 2005 Sep;15(9):1222-31.
      pubmed: 16140990doi: 10.1101/gr.3461105google scholar: lookup
    36. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.. Nucleic Acids Res 1994 Nov 11;22(22):4673-80.
      pubmed: 7984417doi: 10.1093/nar/22.22.4673google scholar: lookup
    37. Miyata T, Hayashida H, Kuma K, Mitsuyasu K, Yasunaga T. Male-driven molecular evolution: a model and nucleotide sequence analysis.. Cold Spring Harb Symp Quant Biol 1987;52:863-7.
      pubmed: 3454295doi: 10.1101/sqb.1987.052.01.094google scholar: lookup
    38. Oakenfull EA, Clegg JB. Phylogenetic relationships within the genus Equus and the evolution of alpha and theta globin genes.. J Mol Evol 1998 Dec;47(6):772-83.
      pubmed: 9847419doi: 10.1007/pl00006436google scholar: lookup
    39. Makova KD, Patton JC. Increased yield of tri- and tetranucleotide heterospecific microsatellites from unenriched small-insert libraries.. Biotechniques 1998 Jan;24(1):38, 40, 42-3.
      pubmed: 9454948doi: 10.2144/98241bm06google scholar: lookup

    Citations

    This article has been cited 20 times.
    1. Waldvogel AM, Pfenninger M. Temperature dependence of spontaneous mutation rates. Genome Res 2021 Sep;31(9):1582-1589.
      doi: 10.1101/gr.275168.120pubmed: 34301628google scholar: lookup
    2. Campbell CR, Tiley GP, Poelstra JW, Hunnicutt KE, Larsen PA, Lee HJ, Thorne JL, Dos Reis M, Yoder AD. Pedigree-based and phylogenetic methods support surprising patterns of mutation rate and spectrum in the gray mouse lemur. Heredity (Edinb) 2021 Aug;127(2):233-244.
      doi: 10.1038/s41437-021-00446-5pubmed: 34272504google scholar: lookup
    3. Czech B, Guldbrandtsen B, Szyda J. Patterns of DNA variation between the autosomes, the X chromosome and the Y chromosome in Bos taurus genome. Sci Rep 2020 Aug 12;10(1):13641.
      doi: 10.1038/s41598-020-70380-9pubmed: 32788585google scholar: lookup
    4. Martin H, Carpentier F, Gallina S, Godé C, Schmitt E, Muyle A, Marais GAB, Touzet P. Evolution of Young Sex Chromosomes in Two Dioecious Sister Plant Species with Distinct Sex Determination Systems. Genome Biol Evol 2019 Feb 1;11(2):350-361.
      doi: 10.1093/gbe/evz001pubmed: 30649306google scholar: lookup
    5. Thybert D, Roller M, Navarro FCP, Fiddes I, Streeter I, Feig C, Martin-Galvez D, Kolmogorov M, Janoušek V, Akanni W, Aken B, Aldridge S, Chakrapani V, Chow W, Clarke L, Cummins C, Doran A, Dunn M, Goodstadt L, Howe K, Howell M, Josselin AA, Karn RC, Laukaitis CM, Jingtao L, Martin F, Muffato M, Nachtweide S, Quail MA, Sisu C, Stanke M, Stefflova K, Van Oosterhout C, Veyrunes F, Ward B, Yang F, Yazdanifar G, Zadissa A, Adams DJ, Brazma A, Gerstein M, Paten B, Pham S, Keane TM, Odom DT, Flicek P. Repeat associated mechanisms of genome evolution and function revealed by the Mus caroli and Mus pahari genomes. Genome Res 2018 Apr;28(4):448-459.
      doi: 10.1101/gr.234096.117pubmed: 29563166google scholar: lookup
    6. Ghenu AH, Bolker BM, Melnick DJ, Evans BJ. Multicopy gene family evolution on primate Y chromosomes. BMC Genomics 2016 Feb 29;17:157.
      doi: 10.1186/s12864-015-2187-8pubmed: 26925773google scholar: lookup
    7. Schlick-Steiner BC, Arthofer W, Moder K, Steiner FM. Recent insertion/deletion (reINDEL) mutations: increasing awareness to boost molecular-based research in ecology and evolution. Ecol Evol 2015 Jan;5(1):24-35.
      doi: 10.1002/ece3.1330pubmed: 25628861google scholar: lookup
    8. Yue H, Yu JB, He JW, Zhang Z, Fu WZ, Zhang H, Wang C, Hu WW, Gu JM, Hu YQ, Li M, Liu YJ, Zhang ZL. Identification of two novel mutations in the PHEX gene in Chinese patients with hypophosphatemic rickets/osteomalacia. PLoS One 2014;9(5):e97830.
      doi: 10.1371/journal.pone.0097830pubmed: 24836714google scholar: lookup
    9. Scally A, Dutheil JY, Hillier LW, Jordan GE, Goodhead I, Herrero J, Hobolth A, Lappalainen T, Mailund T, Marques-Bonet T, McCarthy S, Montgomery SH, Schwalie PC, Tang YA, Ward MC, Xue Y, Yngvadottir B, Alkan C, Andersen LN, Ayub Q, Ball EV, Beal K, Bradley BJ, Chen Y, Clee CM, Fitzgerald S, Graves TA, Gu Y, Heath P, Heger A, Karakoc E, Kolb-Kokocinski A, Laird GK, Lunter G, Meader S, Mort M, Mullikin JC, Munch K, O'Connor TD, Phillips AD, Prado-Martinez J, Rogers AS, Sajjadian S, Schmidt D, Shaw K, Simpson JT, Stenson PD, Turner DJ, Vigilant L, Vilella AJ, Whitener W, Zhu B, Cooper DN, de Jong P, Dermitzakis ET, Eichler EE, Flicek P, Goldman N, Mundy NI, Ning Z, Odom DT, Ponting CP, Quail MA, Ryder OA, Searle SM, Warren WC, Wilson RK, Schierup MH, Rogers J, Tyler-Smith C, Durbin R. Insights into hominid evolution from the gorilla genome sequence. Nature 2012 Mar 7;483(7388):169-75.
      doi: 10.1038/nature10842pubmed: 22398555google scholar: lookup
    10. Wilson Sayres MA, Makova KD. Genome analyses substantiate male mutation bias in many species. Bioessays 2011 Dec;33(12):938-45.
      doi: 10.1002/bies.201100091pubmed: 22006834google scholar: lookup
    11. Goldie X, Lanfear R, Bromham L. Diversification and the rate of molecular evolution: no evidence of a link in mammals. BMC Evol Biol 2011 Oct 4;11:286.
      doi: 10.1186/1471-2148-11-286pubmed: 21967038google scholar: lookup
    12. Bromham L. The genome as a life-history character: why rate of molecular evolution varies between mammal species. Philos Trans R Soc Lond B Biol Sci 2011 Sep 12;366(1577):2503-13.
      doi: 10.1098/rstb.2011.0014pubmed: 21807731google scholar: lookup
    13. Pink CJ, Swaminathan SK, Dunham I, Rogers J, Ward A, Hurst LD. Evidence that replication-associated mutation alone does not explain between-chromosome differences in substitution rates. Genome Biol Evol 2009 Apr 30;1:13-22.
      doi: 10.1093/gbe/evp001pubmed: 20333173google scholar: lookup
    14. Labuda D, Lefebvre JF, Nadeau P, Roy-Gagnon MH. Female-to-male breeding ratio in modern humans-an analysis based on historical recombinations. Am J Hum Genet 2010 Mar 12;86(3):353-63.
      doi: 10.1016/j.ajhg.2010.01.029pubmed: 20188344google scholar: lookup
    15. Presgraves DC, Yi SV. Doubts about complex speciation between humans and chimpanzees. Trends Ecol Evol 2009 Oct;24(10):533-40.
      doi: 10.1016/j.tree.2009.04.007pubmed: 19664844google scholar: lookup
    16. Duret L. Mutation patterns in the human genome: more variable than expected. PLoS Biol 2009 Feb 3;7(2):e1000028.
      doi: 10.1371/journal.pbio.1000028pubmed: 19192948google scholar: lookup
    17. Tyekucheva S, Makova KD, Karro JE, Hardison RC, Miller W, Chiaromonte F. Human-macaque comparisons illuminate variation in neutral substitution rates. Genome Biol 2008 Apr 30;9(4):R76.
      doi: 10.1186/gb-2008-9-4-r76pubmed: 18447906google scholar: lookup
    18. Smith ER, Lee MG, Winter B, Droz NM, Eissenberg JC, Shiekhattar R, Shilatifard A. Drosophila UTX is a histone H3 Lys27 demethylase that colocalizes with the elongating form of RNA polymerase II. Mol Cell Biol 2008 Feb;28(3):1041-6.
      doi: 10.1128/MCB.01504-07pubmed: 18039863google scholar: lookup
    19. Dreszer TR, Wall GD, Haussler D, Pollard KS. Biased clustered substitutions in the human genome: the footprints of male-driven biased gene conversion. Genome Res 2007 Oct;17(10):1420-30.
      doi: 10.1101/gr.6395807pubmed: 17785536google scholar: lookup
    20. Chen H, Rushdi HE, Loor JJ, Teng Z, Liu S. Progress of sex control techniques in mammals†. Biol Reprod 2025 Nov 14;113(5):997-1012.
      doi: 10.1093/biolre/ioaf149pubmed: 40621949google scholar: lookup
    Subscribe to our newsletter
    Join 99,383 horse owners like you who receive our email updates on horse health and nutrition.