Genomic evidence that a sexually selected trait captures genome-wide variation and facilitates the purging of genetic load.
Journal
Nature ecology & evolution
ISSN: 2397-334X
Titre abrégé: Nat Ecol Evol
Pays: England
ID NLM: 101698577
Informations de publication
Date de publication:
09 2022
09 2022
Historique:
received:
19
10
2021
accepted:
26
05
2022
pubmed:
20
7
2022
medline:
9
9
2022
entrez:
19
7
2022
Statut:
ppublish
Résumé
The evolution of costly traits such as deer antlers and peacock trains, which drove the formation of Darwinian sexual selection theory, has been suggested to both reflect and affect patterns of genetic variance across the genome, but direct tests are missing. Here, we used an evolve and resequence approach to reveal patterns of genome-wide diversity associated with the expression of a sexually selected weapon that is dimorphic among males of the bulb mite, Rhizoglyphus robini. Populations selected for the weapon showed reduced genome-wide diversity compared to populations selected against the weapon, particularly in terms of the number of segregating non-synonymous positions, indicating enhanced purifying selection. This increased purifying selection reduced inbreeding depression, but outbred female fitness did not improve, possibly because any benefits were offset by increased sexual antagonism. Most single nucleotide polymorphisms (SNPs) that consistently diverged in response to selection were initially rare and overrepresented in exons, and enriched in regions under balancing or relaxed selection, suggesting they are probably moderately deleterious variants. These diverged SNPs were scattered across the genome, further demonstrating that selection for or against the weapon and the associated changes to the mating system can both capture and influence genome-wide variation.
Identifiants
pubmed: 35851852
doi: 10.1038/s41559-022-01816-w
pii: 10.1038/s41559-022-01816-w
doi:
Banques de données
Dryad
['10.5061/dryad.ncjsxksxg']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1330-1342Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Darwin, C. The Descent of Man and Selection in Relation to Sex (Murray, 1871).
Andersson, M. Sexual Selection (Princeton Univ. Press, 1994).
Shuker, D. M. & Kvarnemo, C. The definition of sexual selection. Behav. Ecol. 32, 781–794 (2021).
pubmed: 34695172
pmcid: 8528540
doi: 10.1093/beheco/arab055
Martínez-Ruiz, C. & Knell, R. J. Sexual selection can both increase and decrease extinction probability: reconciling demographic and evolutionary factors. J. Anim. Ecol. 86, 117–127 (2016).
pubmed: 27861841
doi: 10.1111/1365-2656.12601
Kokko, H. & Brooks, R. Sexy to die for? Sexual selection and the risk of extinction. Ann. Zool. Fennici 40, 207–219 (2003).
van Doorn, G. S., Edelaar, P. & Weissing, F. J. On the origin of species by natural and sexual selection. Science 326, 1704–1707 (2009).
pubmed: 19965377
doi: 10.1126/science.1181661
Ritchie, M. G. Sexual selection and speciation. Annu. Rev. Ecol. Evol. Syst. 38, 79–102 (2007).
doi: 10.1146/annurev.ecolsys.38.091206.095733
Lorch, P. D., Proulx, S., Rowe, L. & Day, T. Condition dependent sexual selection can accelerate adaptation. Evol. Ecol. Res. 5, 867–881 (2003).
Rowe, L. & Rundle, H. D. The alignment of natural and sexual selection. Annu. Rev. Ecol. Evol. Syst. 52, 499–517 (2021).
doi: 10.1146/annurev-ecolsys-012021-033324
Candolin, U. & Heuschele, J. Is sexual selection beneficial during adaptation to environmental change? Trends Ecol. Evol. 23, 446–452 (2008).
pubmed: 18582989
doi: 10.1016/j.tree.2008.04.008
Holman, L. & Kokko, H. The consequences of polyandry for population viability, extinction risk and conservation. Philos. Trans. R. Soc. B. Biol. Sci. 368, 20120053 (2013).
doi: 10.1098/rstb.2012.0053
Cally, J. G., Stuart-Fox, D. & Holman, L. Meta-analytic evidence that sexual selection improves population fitness. Nat. Commun. 10, 2017 (2019).
pubmed: 31043615
pmcid: 6494874
doi: 10.1038/s41467-019-10074-7
Tanaka, Y. Sexual selection enhances population extinction in a changing environment. J. Theor. Biol. 180, 197–206 (1996).
pubmed: 8759528
doi: 10.1006/jtbi.1996.0096
Winkler, L., Moiron, M., Morrow, E. H. & Janicke, T. Stronger net selection on males across animals. eLife 10, e68316 (2021).
pubmed: 34787569
pmcid: 8598160
doi: 10.7554/eLife.68316
Agrawal, A. F. Sexual selection and the maintenance of sexual reproduction. Nature 411, 692–695 (2001).
pubmed: 11395771
doi: 10.1038/35079590
Siller, S. Sexual selection and the maintenance of sex. Nature 411, 689–692 (2001).
pubmed: 11395770
doi: 10.1038/35079578
Whitlock, M. C. & Agrawal, A. F. Purging the genome with sexual selection: reducing mutation load through selection on males. Evolution 63, 569–582 (2009).
pubmed: 19154364
doi: 10.1111/j.1558-5646.2008.00558.x
Grieshop, K., Maurizio, P. L., Arnqvist, G. & Berger, D. Selection in males purges the mutation load on female fitness. Evol. Lett. 5, 328–343 (2021).
pubmed: 34367659
pmcid: 8327962
doi: 10.1002/evl3.239
Darwin, C. The Origin of Species (Oxford World’s Classics, 1859).
Rowe, L. & Houle, D. The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. B. Biol. Sci. 263, 1415–1421 (1996).
doi: 10.1098/rspb.1996.0207
Tomkins, J. L., Radwan, J., Kotiaho, J. S. & Tregenza, T. Genic capture and resolving the lek paradox. Trends Ecol. Evol. 19, 323–328 (2004).
pubmed: 16701278
doi: 10.1016/j.tree.2004.03.029
Andersson, M. Evolution of condition-dependent sex ornaments and mating preferences: sexual selection based on viability differences. Evolution 40, 804–816 (1986).
pubmed: 28556175
doi: 10.1111/j.1558-5646.1986.tb00540.x
Prokuda, A. Y. & Roff, D. A. The quantitative genetics of sexually selected traits, preferred traits and preference: a review and analysis of the data. J. Evol. Biol. 27, 2283–2296 (2014).
pubmed: 25263742
doi: 10.1111/jeb.12483
Berglund, A., Bisazza, A. & Pilastro, A. Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biol. J. Linn. Soc. 58, 385–399 (1996).
doi: 10.1111/j.1095-8312.1996.tb01442.x
Tomkins, J. L. & Hazel, W. The status of the conditional evolutionarily stable strategy. Trends Ecol. Evol. 22, 522–528 (2007).
pubmed: 17919770
doi: 10.1016/j.tree.2007.09.002
Gross, M. R. Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol. Evol. 11, 92–98 (1996).
pubmed: 21237769
doi: 10.1016/0169-5347(96)81050-0
Gross, M. R. & Repka, J. Stability with inheritance in the conditional strategy. J. Theor. Biol. 192, 445–453 (1998).
pubmed: 9782102
doi: 10.1006/jtbi.1998.0665
Taborsky, M., Oliveira, R. & Brockmann, H. in Alternative Reproductive Tactics: An Integrative Approach (eds Oliveira, R. et al.) 1–22 (Cambridge Univ. Press, 2008).
Jensen, J. D. On the unfounded enthusiasm for soft selective sweeps. Nat. Commun. 5, 527 (2014).
doi: 10.1038/ncomms6281
Connallon, T. & Clark, A. G. Balancing selection in species with separate sexes: insights from fisher’s geometric model. Genetics 197, 991–1006 (2014).
pubmed: 24812306
pmcid: 4096376
doi: 10.1534/genetics.114.165605
Johnston, S. E. et al. Life history trade-offs at a single locus maintain sexually selected genetic variation. Nature 502, 93–95 (2013).
pubmed: 23965625
doi: 10.1038/nature12489
Mérot, C., Llaurens, V., Normandeau, E., Bernatchez, L. & Wellenreuther, M. Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly. Nat. Commun. 11, 670 (2020).
pubmed: 32015341
pmcid: 6997199
doi: 10.1038/s41467-020-14479-7
Chippindale, A. K., Gibson, J. R. & Rice, W. R. Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc. Natl Acad. Sci. USA. 98, 1671–1675 (2001).
pubmed: 11172009
pmcid: 29315
doi: 10.1073/pnas.98.4.1671
Bonduriansky, R. & Chenoweth, S. F. Intralocus sexual conflict. Trends Ecol. Evol. 24, 280–288 (2009).
pubmed: 19307043
doi: 10.1016/j.tree.2008.12.005
Foerster, K. et al. Sexually antagonistic genetic variation for fitness in red deer. Nature 447, 1107–1110 (2007).
pubmed: 17597758
doi: 10.1038/nature05912
Cox, R. M. & Calsbeek, R. Sexually antagonistic selection, sexual dimorphism, and the resolution of intralocus sexual conflict. Am. Nat. 173, 176–187 (2009).
pubmed: 19138156
doi: 10.1086/595841
Pike, K. N., Tomkins, J. L. & Buzatto, B. A. Mixed evidence for the erosion of intertactical genetic correlations through intralocus tactical conflict. J. Evol. Biol. 30, 1195–1204 (2017).
pubmed: 28430382
doi: 10.1111/jeb.13093
Morris, M. R., Goedert, D., Abbott, J. K., Robinson, D. M. & Rios-Cardenas, O. in Advances in the Study of Behavior (eds Jane Brockmann, H. et al.) 45 (Elsevier Inc., 2013).
Plesnar-Bielak, A., Skrzynecka, A. M., Miler, K. & Radwan, J. Selection for alternative male reproductive tactics alters intralocus sexual conflict. Evolution 68, 2137–2144 (2014).
pubmed: 24641007
doi: 10.1111/evo.12409
Harano, T., Okada, K., Nakayama, S., Miyatake, T. & Hosken, D. J. Intralocus sexual conflict unresolved by sex-limited trait expression. Curr. Biol. 20, 2036–2039 (2010).
pubmed: 21055943
doi: 10.1016/j.cub.2010.10.023
Okada, K. et al. Natural selection increases female fitness by reversing the exaggeration of a male sexually selected trait. Nat. Commun. 12, 3420 (2021).
pubmed: 34103535
pmcid: 8187464
doi: 10.1038/s41467-021-23804-7
Radwan, J., Engqvist, L. & Reinhold, K. A paradox of genetic variance in epigamic traits: beyond ‘good genes’ view of sexual selection. Evol. Biol. 43, 267–275 (2016).
pubmed: 27217597
doi: 10.1007/s11692-015-9359-y
Zajitschek, F. & Connallon, T. Antagonistic pleiotropy in species with separate sexes, and the maintenance of genetic variation in life-history traits and fitness. Evolution. 72, 1306–1316 (2018).
pubmed: 29667189
doi: 10.1111/evo.13493
Radwan, J. Effectiveness of sexual selection in removing mutations induced with ionizing radiation. Ecol. Lett. 7, 1149–1154 (2004).
doi: 10.1111/j.1461-0248.2004.00681.x
Lumley, A. J. et al. Sexual selection protects against extinction. Nature 522, 470–473 (2015).
pubmed: 25985178
doi: 10.1038/nature14419
Almbro, M. & Simmons, L. W. Sexual selection can remove an experimentally induced mutation load. Evolution. 68, 295–300 (2014).
pubmed: 24372608
doi: 10.1111/evo.12238
Dugand, R. J., Jason Kennington, W. & Tomkins, J. L. Evolutionary divergence in competitive mating success through female mating bias for good genes. Sci. Adv. 4, eaaq0369 (2018).
pubmed: 29806021
pmcid: 5966190
doi: 10.1126/sciadv.aaq0369
Hollis, B., Fierst, J. L. & Houle, D. Sexual selection accelerates the elimination of a deleterious mutant in Drosophila melanogaster. Evolution. 63, 324–333 (2009).
pubmed: 19154371
doi: 10.1111/j.1558-5646.2008.00551.x
Dugand, R. J., Tomkins, J. L. & Kennington, W. J. Molecular evidence supports a genic capture resolution of the lek paradox. Nat. Commun. 10, 1359 (2019).
pubmed: 30911052
pmcid: 6433924
doi: 10.1038/s41467-019-09371-y
Parrett, J. M., Ghobert, V., Cullen, F. S. & Knell, R. J. Strong sexual selection fails to protect against inbreeding-driven extinction in a moth. Behav. Ecol. 32, 875–882 (2021).
doi: 10.1093/beheco/arab056
Arbuthnott, D. & Rundle, H. D. Sexual selection is ineffectual or inhibits the purging of deleterious mutations in Drosophila melanogaster. Evolution. 66, 2127–2137 (2012).
pubmed: 22759290
doi: 10.1111/j.1558-5646.2012.01584.x
Holland, B. & Rice, W. R. Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proc. Natl Acad. Sci. USA. 96, 5083–5088 (1999).
pubmed: 10220422
pmcid: 21820
doi: 10.1073/pnas.96.9.5083
Rundle, H. D., Chenoweth, S. F. & Blows, M. W. The roles of natural and sexual selection during adaptation to a novel environment. Evolution 60, 2218–2225 (2006).
pubmed: 17236415
doi: 10.1111/j.0014-3820.2006.tb01859.x
Chenoweth, S. F., Appleton, N. C., Allen, S. L. & Rundle, H. D. Genomic evidence that sexual selection impedes adaptation to a novel environment. Curr. Biol. 25, 1860–1866 (2015).
pubmed: 26119752
doi: 10.1016/j.cub.2015.05.034
Holland, B. Sexual selection fails to promote adaptation to a new environment. Evolution. 56, 721–730 (2002).
pubmed: 12038530
doi: 10.1111/j.0014-3820.2002.tb01383.x
Berger, D. et al. Intralocus sexual conflict and the tragedy of the commons in seed beetles. Am. Nat. 188, E98–E112 (2016).
pubmed: 27622882
doi: 10.1086/687963
Sayadi, A. et al. The genomic footprint of sexual conflict. Nat. Ecol. Evol. 3, 1725–1730 (2019).
pubmed: 31740847
doi: 10.1038/s41559-019-1041-9
Ruzicka, F. et al. Genome-wide sexually antagonistic variants reveal long-standing constraints on sexual dimorphism in fruit flies. PLoS Biol. 17, e3000244 (2019).
pubmed: 31022179
pmcid: 6504117
doi: 10.1371/journal.pbio.3000244
Radwan, J., Czyz, M., Konior, M. & Kołodziejczyk, M. Aggressiveness in two male morphs of the bulb mite Rhizoglyphus robini. Ethology 106, 53–62 (2000).
doi: 10.1046/j.1439-0310.2000.00498.x
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
doi: 10.1038/nrg3803
Ellegren, H. The different levels of genetic diversity in sex chromosomes and autosomes. Trends Genet. 25, 278–284 (2009).
pubmed: 19481288
doi: 10.1016/j.tig.2009.04.005
Charlesworth, B., Coyne, J. A. & Barton, N. H. The relative rates of evolution of sex chromosomes and autosomes. Am. Nat. 130, 113–146 (1987).
doi: 10.1086/284701
Wiberg, R. A. W., Veltsos, P., Snook, R. R. & Ritchie, M. G. Experimental evolution supports signatures of sexual selection in genomic divergence. Evol. Lett. 5, 214–229 (2021).
pubmed: 34136270
pmcid: 8190450
doi: 10.1002/evl3.220
Wright, S. Evolution in mendelian populations. Genetics 16, 97–159 (1931).
pubmed: 17246615
pmcid: 1201091
doi: 10.1093/genetics/16.2.97
Smallegange, I. M. Complex environmental effects on the expression of alternative reproductive phenotypes in the bulb mite. Evol. Ecol. 25, 857–873 (2011).
doi: 10.1007/s10682-010-9446-6
Radwan, J. Male morph determination in two species of acarid mites. Heredity. 74, 669–673 (1995).
doi: 10.1038/hdy.1995.91
Łukasiewicz, A., Niśkiewicz, M. & Radwan, J. Sexually selected male weapon is associated with lower inbreeding load but higher sex load in the bulb mite. Evolution. 74, 1851–1855 (2020).
pubmed: 32519389
pmcid: 7496443
doi: 10.1111/evo.14033
Charlesworth, D. & Willis, J. H. The genetics of inbreeding depression. Nat. Rev. Genet. 10, 783–796 (2009).
pubmed: 19834483
doi: 10.1038/nrg2664
Radwan, J. & Klimas, M. Male dimorphism in the bulb mite, Rhizoglyphus robini: fighters survive better. Ethol. Ecol. Evol. 13, 69–79 (2001).
doi: 10.1080/08927014.2001.9522788
Wiberg, R. A. W., Gaggiotti, O. E., Morrissey, M. B. & Ritchie, M. G. Identifying consistent allele frequency differences in studies of stratified populations. Methods Ecol. Evol. 8, 1899–1909 (2017).
pubmed: 29263778
pmcid: 5726381
doi: 10.1111/2041-210X.12810
Llaurens, V., Whibley, A. & Joron, M. Genetic architecture and balancing selection: the life and death of differentiated variants. Mol. Ecol. 26, 2430–2448 (2017).
pubmed: 28173627
doi: 10.1111/mec.14051
Joag, R. et al. Transcriptomics of intralocus sexual conflict: Gene expression patterns in females change in response to selection on a male secondary sexual trait in the bulb mite. Genome Biol. Evol. 8, 2351–2357 (2016).
pubmed: 27401174
pmcid: 5010903
doi: 10.1093/gbe/evw169
Connallon, T. & Clark, A. G. A general population genetic framework for antagonistic selection that accounts for demography and recurrent mutation. Genetics 190, 1477–1489 (2012).
pubmed: 22298707
pmcid: 3316657
doi: 10.1534/genetics.111.137117
Küpper, C. et al. A supergene determines highly divergent male reproductive morphs in the ruff. Nat. Genet. 48, 79–83 (2015).
pubmed: 26569125
pmcid: 5218575
doi: 10.1038/ng.3443
Hendrickx, F. et al. A masculinizing supergene underlies an exaggerated male reproductive morph in a spider. Nat. Ecol. Evol. 6, 195–206 (2022).
pubmed: 34949821
doi: 10.1038/s41559-021-01626-6
Kirkpatrick, M. & Ryan, M. J. The evolution of mating preferences and the paradox of the lek. Nature 350, 33–38 (1991).
doi: 10.1038/350033a0
Houle, D. How should we explain variation in the genetic variance of traits? Genetica 102–103, 241–253 (1998).
pubmed: 9720283
doi: 10.1023/A:1017034925212
Parrett, J. M. & Knell, R. J. The effect of sexual selection on adaptation and extinction under increasing temperatures. Proc. R. Soc. B. Biol. Sci. 285, 20180303 (2018).
doi: 10.1098/rspb.2018.0303
Parrett, J. M., Mann, D. J., Chung, A. Y. C., Slade, E. M. & Knell, R. J. Sexual selection predicts the persistence of populations within altered environments. Ecol. Lett. 22, 1629–1637 (2019).
pubmed: 31353816
doi: 10.1111/ele.13358
Plesnar-Bielak, A., Skrzynecka, A. M., Prokop, Z. M. & Radwan, J. Mating system affects population performance and extinction risk under environmental challenge. Proc. R. Soc. B. Biol. Sci. 279, 4661–4667 (2012).
doi: 10.1098/rspb.2012.1867
Jarzebowska, M. & Radwan, J. Sexual selection counteracts extinction of small populations of the bulb mites. Evolution. 64, 1283–1289 (2010).
pubmed: 19930452
Godwin, J. L., Lumley, A. J., Michalczyk, Ł., Martin, O. Y. & Gage, M. J. G. Mating patterns influence vulnerability to the extinction vortex. Glob. Chang. Biol. 26, 4226–4239 (2020).
pubmed: 32558066
doi: 10.1111/gcb.15186
Yun, L. et al. Competition for mates and the improvement of nonsexual fitness. Proc. Natl Acad. Sci. USA 115, 6762–6767 (2018).
pubmed: 29891650
pmcid: 6042133
doi: 10.1073/pnas.1805435115
Martins, M. J. F., Puckett, T. M., Lockwood, R., Swaddle, J. P. & Hunt, G. High male sexual investment as a driver of extinction in fossil ostracods. Nature 556, 366–369 (2018).
pubmed: 29643505
doi: 10.1038/s41586-018-0020-7
Doherty, P. F. et al. Sexual selection affects local extinction and turnover in bird communities. Proc. Natl Acad. Sci. USA 100, 5858–5862 (2003).
pubmed: 12682284
pmcid: 156291
doi: 10.1073/pnas.0836953100
Sorci, G., Møller, A. P. & Clobert, J. Plumage dichromatism of birds predicts introduction success in New Zealand. J. Anim. Ecol. 67, 263–269 (1998).
doi: 10.1046/j.1365-2656.1998.00199.x
Grieshop, K., Berger, D. & Arnqvist, G. Male-benefit sexually antagonistic genotypes show elevated vulnerability to inbreeding. BMC Evol. Biol. 17, 134 (2017).
pubmed: 28606137
pmcid: 5469140
doi: 10.1186/s12862-017-0981-4
Radwan, J. & Siva-Jothy, M. T. The function of post-insemination mate association in the bulb mite, Rhizoglyphus robini. Anim. Behav. 52, 651–657 (1996).
doi: 10.1006/anbe.1996.0209
Radwan, J. Sperm precedence in the bulb mite, Rhiziglyphus robini: context-dependent variation. Ethol. Ecol. Evol. 9, 373–383 (1997).
doi: 10.1080/08927014.1997.9522879
Radwan, J. & Bogacz, I. Comparison of life-history traits of the two male morphs of the bulb mite, Rhizoglyphus robini. Exp. Appl. Acarol. 24, 115–121 (2000).
pubmed: 11108391
doi: 10.1023/A:1006492903270
Roff, D. A. Evolutionary Quantitative Genetics (Chapman and Hall, 1997).
Knell, R. J. On the analysis of non-linear allometries. Ecol. Entomol. 34, 1–11 (2009).
doi: 10.1111/j.1365-2311.2008.01022.x
Tilszer, M., Antoszczyk, K., Sałek, N., Zajac, E. & Radwan, J. Evolution under relaxed sexual conflict in the bulb mite Rhizoglyphus robini. Evolution 60, 1868–1873 (2006).
pubmed: 17089971
doi: 10.1111/j.0014-3820.2006.tb00530.x
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020); https://www.R-project.org/
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (2016).
Bates, D., Mächler, M., Bolker, B. M. & Walker, S. C. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
doi: 10.18637/jss.v067.i01
Therneau, T. M. coxme: mixed effects Cox models (2020); https://CRAN.R-project.org/package=coxme
Sterck, L., Billiau, K., Abeel, T., Rouzé, P. & Van De Peer, Y. ORCAE: online resource for community annotation of eukaryotes. Nat. Methods 9, 1041 (2012).
pubmed: 23132114
doi: 10.1038/nmeth.2242
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at arXiv https://doi.org/10.48550/arXiv.1303.3997 (2013).
Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943
pmcid: 2723002
doi: 10.1093/bioinformatics/btp352
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
doi: 10.1371/journal.pone.0015925
Kofler, R., Pandey, R. V. & Schlötterer, C. PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinformatics 27, 3435–3436 (2011).
pubmed: 22025480
pmcid: 3232374
doi: 10.1093/bioinformatics/btr589
Storey, J. D. A direct approach to false discovery rates. J. R. Stat. Soc. Ser.B. Stat. Methodol. 64, 479–498 (2002).
doi: 10.1111/1467-9868.00346
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
pubmed: 20110278
pmcid: 2832824
doi: 10.1093/bioinformatics/btq033
D. Turner, S. qqman: an R package for visualizing GWAS results using Q-Q and Manhattan plots. J. Open Source Softw. 3, 731 (2018).
doi: 10.21105/joss.00731
Oliver, J. H. Cytogenetics of mites and ticks. Annu. Rev. Entomol. 22, 407–429 (1977).
pubmed: 319744
doi: 10.1146/annurev.en.22.010177.002203
Taus, T., Futschik, A. & Schlötterer, C. Quantifying selection with pool-seq time series data. Mol. Biol. Evol. 34, 3023–3034 (2017).
pubmed: 28961717
pmcid: 5850601
doi: 10.1093/molbev/msx225
Smallegange, I. M. & Coulson, T. The stochastic demography of two coexisting male morphs. Ecology 92, 755–764 (2011).
pubmed: 21608483
doi: 10.1890/09-2069.1
Plesnar-Bielak, A., Skwierzyńska, A. M., Hlebowicz, K. & Radwan, J. Relative costs and benefits of alternative reproductive phenotypes at different temperatures—genotype-by-environment interactions in a sexually selected trait. BMC Evol. Biol. 18, 109 (2018).
pubmed: 29996775
pmcid: 6042425
doi: 10.1186/s12862-018-1226-x
Bleay, C., Comendant, T. & Sinervo, B. An experimental test of frequency-dependent selection on male mating strategy in the field. Proc. R. Soc. B Biol. Sci. 274, 2019–2025 (2007).
doi: 10.1098/rspb.2007.0361
Skrzynecka, A. M. & Radwan, J. Experimental evolution reveals balancing selection underlying coexistence of alternative male reproductive phenotypes. Evolution 70, 2611–2615 (2016).
pubmed: 27530807
doi: 10.1111/evo.13038