The genomic footprint of sexual conflict.


Journal

Nature ecology & evolution
ISSN: 2397-334X
Titre abrégé: Nat Ecol Evol
Pays: England
ID NLM: 101698577

Informations de publication

Date de publication:
12 2019
Historique:
received: 07 05 2019
accepted: 15 10 2019
pubmed: 20 11 2019
medline: 18 12 2019
entrez: 20 11 2019
Statut: ppublish

Résumé

Genes with sex-biased expression show a number of unique properties and this has been seen as evidence for conflicting selection pressures in males and females, forming a genetic 'tug-of-war' between the sexes. However, we lack studies of taxa where an understanding of conflicting phenotypic selection in the sexes has been linked with studies of genomic signatures of sexual conflict. Here, we provide such a link. We used an insect where sexual conflict is unusually well understood, the seed beetle Callosobruchus maculatus, to test for molecular genetic signals of sexual conflict across genes with varying degrees of sex-bias in expression. We sequenced, assembled and annotated its genome and performed population resequencing of three divergent populations. Sex-biased genes showed increased levels of genetic diversity and bore a remarkably clear footprint of relaxed purifying selection. Yet, segregating genetic variation was also affected by balancing selection in weakly female-biased genes, while male-biased genes showed signs of overall purifying selection. Female-biased genes contributed disproportionally to shared polymorphism across populations, while male-biased genes, male seminal fluid protein genes and sex-linked genes did not. Genes showing genomic signatures consistent with sexual conflict generally matched life-history phenotypes known to experience sexually antagonistic selection in this species. Our results highlight metabolic and reproductive processes, confirming the key role of general life-history traits in sexual conflict.

Identifiants

pubmed: 31740847
doi: 10.1038/s41559-019-1041-9
pii: 10.1038/s41559-019-1041-9
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1725-1730

Références

Parsch, J. & Ellegren, H. The evolutionary causes and consequences of sex-biased gene expression. Nat. Rev. Genet. 14, 83–87 (2013).
pubmed: 23329110
Arnqvist, G. & Rowe, L. Sexual Conflict (Princeton Univ. Press, 2005).
Dapper, A. L. & Wade, M. J. The evolution of sperm competition genes: the effect of mating system on levels of genetic variation within and between species. Evolution 70, 502–511 (2016).
pubmed: 26748568 pmcid: 4868060
Rowe, L., Chenoweth, S. F. & Agrawal, A. F. The genomics of sexual conflict. Am. Nat. 192, 274–286 (2018).
pubmed: 30016158
Kasimatis, K. R., Nelson, T. C. & Phillips, P. C. Genomic signatures of sexual conflict. J. Hered. 108, 780–790 (2017).
pubmed: 29036624 pmcid: 5892400
Mank, J. E. Population genetics of sexual conflict in the genomic era. Nat. Rev. Genet. 18, 721–730 (2017).
Connallon, T. & Clark, A. G. Balancing selection in species with separate sexes: insights from Fisher’s geometric model. Genetics 197, 991–1006 (2014).
pubmed: 4096376 pmcid: 4096376
Zhang, Y., Sturgill, D., Parisi, M., Kumar, S. & Oliver, B. Constraint and turnover in sex-biased gene expression in the genus Drosophila. Nature 450, 233–237 (2007).
pubmed: 17994089 pmcid: 2386141
Harrison, P. W. et al. Sexual selection drives evolution and rapid turnover of male gene expression. Proc. Natl Acad. Sci. USA 112, 4393–4398 (2015).
pubmed: 25831521
Wright, A. E. et al. Male biased gene expression resolves sexual conflict through the evolution of sex-specific genetic architecture. Evol. Lett. 2, 52–61 (2018).
pubmed: 30283664 pmcid: 6089503
Hotzy, C., Polak, M., Rönn, J. L. & Arnqvist, G. Phenotypic engineering unveils the function of genital morphology. Curr. Biol. 22, 2258–2261 (2012).
pubmed: 23103188
Goenaga, J., Yamane, T., Rönn, J. & Arnqvist, G. Within-species divergence in the seminal fluid proteome and its effect on male and female reproduction in a beetle. BMC Evol. Biol. 15, 266 (2015).
pubmed: 26627998 pmcid: 4667481
Berg, E. C. & Maklakov, A. A. Sexes suffer from suboptimal lifespan because of genetic conflict in a seed beetle. Proc. R. Soc. Lond. B 279, 4296–4302 (2012).
Berger, D., Berg, E. C., Widegren, V., Arnqvist, G. & Maklakov, A. A. Multivariate intralocus sexual conflict in seed beetles. Evolution 68, 3457–3469 (2014).
pubmed: 25213393
Berger, D. et al. Intralocus sexual conflict and the tragedy of the commons in seed beetles. Am. Nat. 188, E98–E112 (2016).
pubmed: 27622882
Berger, D. et al. Intralocus sexual conflict and environmental stress. Evolution 68, 2184–2196 (2014).
pubmed: 24766035
Bilde, T., Foged, A., Schilling, N. & Arnqvist, G. Postmating sexual selection favors males that sire offspring with low fitness. Science 324, 1705–1706 (2009).
pubmed: 19556506
Grieshop, K. & Arnqvist, G. Sex-specific dominance reversal of genetic variation for fitness. PLoS Biol. 16, e200681 (2018).
Immonen, E., Sayadi, A., Bayram, H. & Arnqvist, G. Mating changes sexually dimorphic gene expression in the seed beetle Callosobruchus maculatus. Genome Biol. Evol. 9, 677–699 (2017).
pubmed: 28391318 pmcid: 5381559
Dutoit, L. et al. Sex‐biased gene expression, sexual antagonism and levels of genetic diversity in the collared flycatcher (Ficedula albicollis) genome. Mol. Ecol. 27, 3572–3581 (2018).
pubmed: 30055065
Kryazhimskiy, S. & Plotkin, J. B. The population genetics of dN/dS. PLoS Genet. 4, e1000304 (2008).
pubmed: 19081788 pmcid: 2596312
Gershoni, M. & Pietrokovski, S. Reduced selection and accumulation of deleterious mutations in genes exclusively expressed in men. Nat. Comm. 5, 4438 (2014).
Rice, W. R. Sex chromosomes and the evolution of sexual dimorphism. Evolution 38, 735–742 (1984).
pubmed: 28555827
Dean, R. & Mank, J. E. The role of sex chromosomes in sexual dimorphism: discordance between molecular and phenotypic data. J. Evol. Biol. 27, 1443–1453 (2014).
pubmed: 25105198
Lucotte, E. A. et al. Detection of allelic frequency differences between the sexes in humans: a signature of sexually antagonistic selection. Genome Biol. Evol. 8, 1489–1500 (2016).
pubmed: 27189992 pmcid: 4898804
Ruzicka, F. et al. Genome-wide sexually antagonistic variants reveal longstanding constraints on sexual dimorphism in the fruitfly. PLoS Biol. 17, e3000244 (2019).
pubmed: 31022179 pmcid: 6504117
Berger, F., Ramı́rez-Hernández, M. H. & Ziegler, M. The new life of a centenarian: signalling functions of NAD(P). Trends Biochem. Sci. 29, 111–118 (2004).
pubmed: 15003268
Cheng, C. & Kirkpatrick, M. Sex-specific selection and sex-biased gene expression in humans and flies. PLoS Genet. 12, e1006170 (2016).
pubmed: 27658217 pmcid: 5033347
Griffin, R. M., Dean, R., Grace, J. L., Rydén, P. & Friberg, U. The shared genome is a pervasive constraint on the evolution of sex-biased gene expression. Mol. Biol. Evol. 30, 2168–2176 (2013).
pubmed: 23813981
Dean, R. & Mank, J. E. Tissue specificity and sex-specific regulatory variation permit the evolution of sex-biased gene expression. Am. Nat. 188, E74–E84 (2016).
pubmed: 27501094
Sirot, L. K., Wong, A., Chapman, T. & Wolfner, M. F. Sexual conflict and seminal fluid proteins: a dynamic landscape of sexual interactions. Cold Spring Harb. Perspect. Biol. 7, a017533 (2015).
pmcid: 4315932
Arnqvist, G., Vellnow, N. & Rowe, L. The effect of epistasis on sexually antagonistic genetic variation. Proc. R. Soc. Lond. B 281, 20140489 (2014).
Barson, N. J. et al. Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon. Nature 528, 405–408 (2015).
pubmed: 26536110 pmcid: 26536110
Lonn, E. et al. Balancing selection maintains polymorphisms at neurogenetic loci in field experiments. Proc. Natl Acad. Sci. USA 114, 3690–3695 (2017).
pubmed: 28325880
Rostant, W. G., Kay, C., Wedell, N. & Hosken, D. J. Sexual conflict maintains variation at an insecticide resistance locus. BMC Biol. 13, 34 (2015).
pubmed: 26032845 pmcid: 4484701
Kébé, K. et al. Global phylogeography of the insect pest Callosobruchus maculatus (Coleoptera: Bruchinae) relates to the history of its main host, Vigna unguiculata. J. Biogeo. 44, 2515–2526 (2017).
Arnqvist, G. et al. Genome size correlates with reproductive fitness in seed beetles. Proc. R. Soc. Lond. B 282, 20151421 (2015).
Sayadi, A., Immonen, E., Bayram, H. & Arnqvist, G. The de novo transcriptome and its functional annotation in the seed beetle Callosobruchus maculatus. PLoS ONE 11, e0158565 (2016).
pubmed: 27442123 pmcid: 4956038
Schlötterer, C., Tobler, R., Kofler, R. & Nolte, V. Sequencing pools of individuals—mining genome-wide polymorphism data without big funding. Nat. Rev. Genet. 15, 749–763 (2014).
pubmed: 25246196
Kofler, R. et al. PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS ONE 6, e15925 (2011).
pubmed: 21253599 pmcid: 3017084
Kelly, J. K. & Hughes, K. A. Pervasive linked selection and intermediate-frequency alleles are implicated in an evolve-and-resequencing experiment of Drosophila simulans. Genetics 211, 943–961 (2019).
pubmed: 30593495
Bayram, H., Sayadi, A., Immonen, E. & Arnqvist, G. Identification of novel ejaculate proteins in a seed beetle and division of labour across male accessory reproductive glands. Insect Biochem. Mol. Biol. 104, 50–57 (2019).
pubmed: 30529580

Auteurs

Ahmed Sayadi (A)

Animal Ecology, Department of Ecology and Genetics, Uppsala University, Uppsala, Sweden.

Alvaro Martinez Barrio (A)

Department of Cell and Molecular Biology, National Bioinformatics Infrastructure Sweden, Science for Life Laboratory, Uppsala University, Uppsala, Sweden.

Elina Immonen (E)

Evolutionary Biology, Department of Ecology and Genetics, Uppsala University, Uppsala, Sweden.

Jacques Dainat (J)

Department of Medical Biochemistry and Microbiology, National Bioinformatics Infrastructure Sweden, Science for Life Laboratory, Uppsala University, Uppsala, Sweden.

David Berger (D)

Animal Ecology, Department of Ecology and Genetics, Uppsala University, Uppsala, Sweden.

Christian Tellgren-Roth (C)

Department of Immunology, Genetics and Pathology, National Genomics Infrastructure, Science for Life Laboratory, Uppsala University, Uppsala, Sweden.

Björn Nystedt (B)

Department of Cell and Molecular Biology, National Bioinformatics Infrastructure Sweden, Science for Life Laboratory, Uppsala University, Uppsala, Sweden.

Göran Arnqvist (G)

Animal Ecology, Department of Ecology and Genetics, Uppsala University, Uppsala, Sweden. Goran.Arnqvist@ebc.uu.se.

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