Sex differences in deleterious mutational effects in Drosophila melanogaster: combining quantitative and population genetic insights.


Journal

Genetics
ISSN: 1943-2631
Titre abrégé: Genetics
Pays: United States
ID NLM: 0374636

Informations de publication

Date de publication:
05 11 2021
Historique:
received: 05 02 2021
accepted: 25 08 2021
entrez: 5 11 2021
pubmed: 6 11 2021
medline: 23 2 2022
Statut: ppublish

Résumé

Fitness effects of deleterious mutations can differ between females and males due to: (i) sex differences in the strength of purifying selection; and (ii) sex differences in ploidy. Although sex differences in fitness effects have important broader implications (e.g., for the evolution of sex and lifespan), few studies have quantified their scope. Those that have belong to one of two distinct empirical traditions: (i) quantitative genetics, which focusses on multi-locus genetic variances in each sex, but is largely agnostic about their genetic basis; and (ii) molecular population genetics, which focusses on comparing autosomal and X-linked polymorphism, but is poorly suited for inferring contemporary sex differences. Here, we combine both traditions to present a comprehensive analysis of female and male adult reproductive fitness among 202 outbred, laboratory-adapted, hemiclonal genomes of Drosophila melanogaster. While we find no clear evidence for sex differences in the strength of purifying selection, sex differences in ploidy generate multiple signals of enhanced purifying selection for X-linked loci. These signals are present in quantitative genetic metrics-i.e., a disproportionate contribution of the X to male (but not female) fitness variation-and population genetic metrics-i.e., steeper regressions of an allele's average fitness effect on its frequency, and proportionally less nonsynonymous polymorphism on the X than autosomes. Fitting our data to models for both sets of metrics, we infer that deleterious alleles are partially recessive. Given the often-large gap between quantitative and population genetic estimates of evolutionary parameters, our study showcases the benefits of combining genomic and fitness data when estimating such parameters.

Identifiants

pubmed: 34740242
pii: 6362879
doi: 10.1093/genetics/iyab143
pmc: PMC8570791
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© The Author(s) 2021. Published by Oxford University Press on behalf of Genetics Society of America. All rights reserved. For permissions, please email: journals.permissions@oup.com.

Références

Evolution. 2018 Mar;72(3):568-577
pubmed: 29430636
PLoS Biol. 2012;10(9):e1001388
pubmed: 22984349
Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):1671-5
pubmed: 11172009
Am Nat. 2014 Sep;184(3):326-37
pubmed: 25141142
Evolution. 2016 Apr;70(4):781-95
pubmed: 27077679
Genetics. 2012 Oct;192(2):533-98
pubmed: 22673804
J Evol Biol. 2009 Mar;22(3):637-43
pubmed: 19210593
Trends Ecol Evol. 2011 Jul;26(7):359-68
pubmed: 21507504
J Evol Biol. 2008 Jul;21(4):1046-54
pubmed: 18462311
Genetics. 1985 Dec;111(4):831-44
pubmed: 17246306
Proc Natl Acad Sci U S A. 2005 May 3;102 Suppl 1:6527-34
pubmed: 15851669
Am Nat. 2010 May;175(5):564-76
pubmed: 20331359
Evolution. 2012 Feb;66(2):558-74
pubmed: 22276548
Nucleic Acids Res. 2017 Jan 4;45(D1):D183-D189
pubmed: 27899595
Genetics. 1988 Jun;119(2):421-33
pubmed: 17246429
Proc Natl Acad Sci U S A. 2015 Dec 15;112(50):15390-5
pubmed: 26604315
Genetics. 2005 Sep;171(1):145-55
pubmed: 15965246
Heredity (Edinb). 2011 Jun;106(6):994-1002
pubmed: 21119701
Proc Biol Sci. 2018 Nov 7;285(1890):
pubmed: 30404880
Nat Genet. 2010 Nov;42(11):969-72
pubmed: 20890277
Nature. 2007 Jan 4;445(7123):82-5
pubmed: 17203060
Mol Biol Evol. 2008 Feb;25(2):454-67
pubmed: 18083702
Proc Natl Acad Sci U S A. 2017 Apr 25;114(17):4465-4470
pubmed: 28400513
Evolution. 2009 Mar;63(3):569-82
pubmed: 19154364
Genetics. 2017 May;206(1):345-361
pubmed: 28249985
Evolution. 1975 Mar;29(1):1-10
pubmed: 28563291
Nat Rev Genet. 2010 Jul;11(7):459-63
pubmed: 20548291
G3 (Bethesda). 2016 Dec 7;6(12):3903-3911
pubmed: 27678519
Biometrics. 1973 Sep;29(3):584-8
pubmed: 4806359
Nature. 2001 Jun 7;411(6838):692-5
pubmed: 11395771
Mol Biol Evol. 2019 Mar 1;36(3):500-515
pubmed: 30590559
Genetics. 2011 Feb;187(2):553-66
pubmed: 21098719
PLoS Genet. 2014 Nov 06;10(11):e1004775
pubmed: 25375361
Nat Rev Genet. 2006 Aug;7(8):645-53
pubmed: 16847464
Heredity (Edinb). 1948 Dec;2(Pt. 3):349-68
pubmed: 18103134
F1000Res. 2016 Nov 7;5:2644
pubmed: 27928499
Nature. 2012 Feb 08;482(7384):173-8
pubmed: 22318601
Evolution. 2018 Dec;72(12):2818-2824
pubmed: 30298925
Genetics. 2007 Dec;177(4):2251-61
pubmed: 18073430
Evolution. 2013 Apr;67(4):1189-95
pubmed: 23550766
Evolution. 2009 Nov;63(11):2888-95
pubmed: 19573084
PLoS Biol. 2010 Mar 16;8(3):e1000335
pubmed: 20305719
Genetics. 2004 Feb;166(2):1053-79
pubmed: 15020487
Evolution. 2017 May;71(5):1417-1424
pubmed: 28369844
Annu Rev Genet. 1977;11:49-78
pubmed: 413473
Nat Commun. 2019 Mar 25;10(1):1359
pubmed: 30911052
Proc Natl Acad Sci U S A. 2011 Nov 1;108(44):18026-31
pubmed: 22003128
Genome Biol Evol. 2013;5(10):1986-94
pubmed: 24084777
Genetics. 1986 Oct;114(2):549-66
pubmed: 17246348
Curr Biol. 2015 Jul 20;25(14):1860-6
pubmed: 26119752
Evolution. 2007 Dec;61(12):3001-6
pubmed: 17971168
Genetics. 2010 Aug;185(4):1381-96
pubmed: 20516497
Mol Biol Evol. 2014 May;31(5):1206-19
pubmed: 24526011
G3 (Bethesda). 2012 Sep;2(9):1067-75
pubmed: 22973544
Nat Genet. 2017 Jul;49(7):986-992
pubmed: 28530675
Biol Lett. 2006 Sep 22;2(3):426-30
pubmed: 17148422
J Evol Biol. 2016 Jun;29(6):1201-10
pubmed: 26991346
Genetics. 2006 Feb;172(2):1079-92
pubmed: 16299397
Proc Biol Sci. 2020 Oct 28;287(1937):20201869
pubmed: 33081608
BMC Evol Biol. 2011 Jun 06;11:156
pubmed: 21645375
Genome Res. 2012 Jul;22(7):1255-65
pubmed: 22499666
Genome Biol Evol. 2011;3:151-5
pubmed: 21292631
Proc Natl Acad Sci U S A. 2015 Feb 10;112(6):1662-9
pubmed: 25572964
Genetics. 2019 Apr;211(4):1125-1130
pubmed: 30967441
Evolution. 2017 Oct;71(10):2398-2409
pubmed: 28722119
Am J Hum Genet. 2007 Sep;81(3):559-75
pubmed: 17701901
PLoS Biol. 2019 Apr 25;17(4):e3000244
pubmed: 31022179
Bioessays. 2013 Aug;35(8):717-24
pubmed: 23733656
Nat Rev Genet. 2007 Aug;8(8):610-8
pubmed: 17637733
Genetics. 2013 Apr;193(4):1197-208
pubmed: 23341416
Evolution. 2012 Dec;66(12):3743-53
pubmed: 23206133
Mol Biol Evol. 2014 Sep;31(9):2267-82
pubmed: 24830675
Nature. 2001 Jun 7;411(6838):689-92
pubmed: 11395770
Trends Genet. 2009 Jun;25(6):278-84
pubmed: 19481288
Evolution. 2013 Dec;67(12):3662-8
pubmed: 24299417
Nat Genet. 2018 May;50(5):746-753
pubmed: 29662166
Am J Hum Genet. 2012 Dec 7;91(6):1011-21
pubmed: 23217325
Evolution. 2017 Mar;71(3):650-661
pubmed: 27943275
Proc Natl Acad Sci U S A. 2019 Feb 5;116(6):2158-2164
pubmed: 30598449
Nat Commun. 2019 Jul 8;10(1):3009
pubmed: 31285442
Nat Genet. 2010 Jul;42(7):565-9
pubmed: 20562875
Evolution. 2010 May;64(5):1510-6
pubmed: 19922443
Sci Adv. 2016 Feb 12;2(2):e1500983
pubmed: 26933680
Proc Biol Sci. 2002 Mar 7;269(1490):499-505
pubmed: 11886642
Genetics. 2011 Nov;189(3):923-37
pubmed: 21890744
Evolution. 2018 Mar;72(3):540-552
pubmed: 29336481

Auteurs

Filip Ruzicka (F)

School of Biological Sciences and Centre for Geometric Biology, Monash University, Clayton 3800, VIC, Australia.
Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK.

Tim Connallon (T)

School of Biological Sciences and Centre for Geometric Biology, Monash University, Clayton 3800, VIC, Australia.

Max Reuter (M)

Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK.
Centre for Life's Origins and Evolution, University College London, London WC1E 6BT, UK.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH