The genetic basis of variation in sexual aggression: Evolution versus social plasticity.
Drosophila melanogaster
RNAseq
artificial selection
forced copulation
gene expression
plasticity
sexual aggression
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
05 2022
05 2022
Historique:
revised:
04
02
2022
received:
21
10
2021
accepted:
07
02
2022
pubmed:
22
3
2022
medline:
18
5
2022
entrez:
21
3
2022
Statut:
ppublish
Résumé
Male sexual aggression towards females is a form of sexual conflict that can result in increased fitness for males through forced copulations (FCs) or coercive matings at the cost of female lifetime fitness. We used male fruit flies (Drosophila melanogaster) as a model system to uncover the genomic contributions to variation in FC, both due to standing variation in a wild population, and due to plastic changes associated with variation in social experience. We used RNAseq to analyse whole-transcriptome differential expression (DE) in male head tissue associated with evolved changes in FC from lineages previously selected for high and low FC rate and in male flies with varying FC rates due to social experience. We identified hundreds of genes associated with evolved and plastic variation in FC, however only a small proportion (27 genes) showed consistent DE due to both modes of variation. We confirmed this trend of low concordance in gene expression effects across broader sets of genes significant in either the evolved or plastic analyses using multivariate approaches. The gene ontology terms neuropeptide hormone activity and serotonin receptor activity were significantly enriched in the set of significant genes. Of seven genes chosen for RNAi knockdown validation tests, knockdown of four genes showed the expected effect on FC behaviours. Taken together, our results provide important information about the apparently independent genetic architectures that underlie natural variation in sexual aggression due to evolution and plasticity.
Substances chimiques
Plastics
0
Banques de données
RefSeq
['PRJNA816348']
Dryad
['10.5061/dryad.zs7h44jbr']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2865-2881Informations de copyright
© 2022 John Wiley & Sons Ltd.
Références
Agrawal, P., Kao, D., Chung, P., & Looger, L. L. (2020). The neuropeptide Drosulfakinin regulates social isolation-induced aggression in Drosophila. Journal of Experimental Biology, 223(2), jeb207407. https://doi.org/10.1242/jeb.207407
Alaux, C., Sinha, S., Hasadsri, L., Hunt, G. J., Guzmán-Novoa, E., DeGrandi-Hoffman, G., Uribe-Rubio, J. L., Southey, B. R., Rodriguez-Zas, S., & Robinson, G. E. (2009). Honey bee aggression supports a link between gene regulation and behavioral evolution. Proceedings of the National Academy of Sciences of the United States of America, 106(36), 15400-15405. https://doi.org/10.1073/pnas.0907043106
Alekseyenko, O. V., Chan, Y. B., De La Paz Fernandez, M., Bülow, T., Pankratz, M. J., & Kravitz, E. A. (2014). Single serotonergic neurons that modulate aggression in Drosophila. Current Biology, 24(22), 2700-2707. https://doi.org/10.1016/j.cub.2014.09.051
Alekseyenko, O. V., Chan, Y. B., Okaty, B. W., Chang, Y. J., Dymecki, S. M., & Kravitz, E. A. (2019). Serotonergic modulation of aggression in Drosophila Involves GABAergic and cholinergic opposing pathways. Current Biology, 29(13), 2145-2156.e5. https://doi.org/10.1016/j.cub.2019.05.070
Alexa, A., & Rahnenführer, J. (2016). Gene set enrichment analysis with topGO. https://bioconductor.org/packages/release/bioc/vignettes/topGO/inst/doc/topGO.pdf
Andrews, S. (2019). FastQC: A quality control tool for high throughput sequence data. https://www.bioinformatics.babraham.ac.uk/projects/fastqc/
Angoa-Pérez, M., & Kuhn, D. M. (2015). Neuroanatomical dichotomy of sexual behaviors in rodents. Behavioural Pharmacology, 26(6), 595-606. https://doi.org/10.1097/FBP.0000000000000157
Arnqvist, G., & Rowe, L. (2005). Sexual conflict. Princeton University Press.
Baxter, C. M., & Dukas, R. (2017). Life history of aggression: Effects of age and sexual experience on male aggression towards males and females. Animal Behaviour, 123, 11-20. https://doi.org/10.1016/j.anbehav.2016.10.022
Baxter, C. M., Yan, J. L., & Dukas, R. (2019). Genetic variation in sexual aggression and the factors that determine forced copulation success. Animal Behaviour, 158, 261-267. https://doi.org/10.1016/j.anbehav.2019.09.015
Becnel, J., Johnson, O., Luo, J., Nässel, D. R., & Nichols, C. D. (2011). The serotonin 5-HT7Dro receptor is expressed in the brain of Drosophila, and is essential for normal courtship and mating. PLoS One, 6(6), e20800. https://doi.org/10.1371/journal.pone.0020800
Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30(15), 2114-2120. https://doi.org/10.1093/bioinformatics/btu170
Brooks, M. E., Kristensen, K., van Benthem, K. J., Magnusson, A., Berg, C. W., Nielsen, A., Skaug, H. J., Mächler, M., & Bolker, B. M. (2017). glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R Journal, 9(2), 378-400. https://doi.org/10.32614/RJ-2017-066
Chapman, T. (2006). Evolutionary conflicts of interest between males and females. Current Biology, 16(17), R744-R754. https://doi.org/10.1016/j.cub.2006.08.020
Chapman, T., Liddle, L. F., Kalb, J. M., Wolfner, M. F., & Partridge, L. (1995). Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature, 373(6511), 241-244.
Crean, C. S., & Gilburn, A. S. (1998). Sexual selection as a side-effect of sexual conflict in the seaweed fly, Coelopa ursina (Diptera: Coelopidae). Animal Behaviour, 56(6), 1405-1410. https://doi.org/10.1006/anbe.1998.0932
Cushing, B. S., Levine, K., & Cushing, N. L. (2005). Neonatal manipulations of oxytocin affect reproductive behavior and reproductive success of adult female prairie voles (Microtus ochrogaster). Hormones and Behavior, 47(1), 22-28.
Dierick, H. A., & Greenspan, R. J. (2006). Molecular analysis of flies selected for aggressive behavior. Nature Genetics, 38(9), 1023-1031. https://doi.org/10.1038/ng1864
Dierick, H. A., & Greenspan, R. J. (2007). Serotonin and neuropeptide F have opposite modulatory effects on fly aggression. Nature Genetics, 39(5), 678-682. https://doi.org/10.1038/ng2029
Dukas, R., & Jongsma, K. (2012). Costs to females and benefits to males from forced copulations in fruit flies. Animal Behaviour, 84(5), 1177-1182. https://doi.org/10.1016/j.anbehav.2012.08.021
Dukas, R., Yan, J. L., Scott, A. M., Sivaratnam, S., & Baxter, C. M. (2020). Artificial selection on sexual aggression: Correlated traits and possible trade-offs. Evolution, 74(6), 1112-1123. https://doi.org/10.1111/evo.13993
Dunn, P. K., & Smyth, G. K. (2005). Series evaluation of Tweedie exponential dispersion model densities. Statistics and Computing, 15(4), 267-280. https://doi.org/10.1007/s11222-005-4070-y
Edwards, A. C., Rollmann, S. M., Morgan, T. J., & Mackay, T. F. C. (2006). Quantitative genomics of aggressive behavior in Drosophila melanogaster. PLoS Genetics, 2(9), 1386-1395. https://doi.org/10.1371/journal.pgen.0020154
Ellis, L. L., & Carney, G. E. (2010). Mating alters gene expression patterns in Drosophila melanogaster male heads. BMC Genomics, 11(1), 558. https://doi.org/10.1186/1471-2164-11-558
Ellis, L. L., & Carney, G. E. (2011). Socially-responsive gene expression in male Drosophila melanogaster is influenced by the sex of the interacting partner. Genetics, 187(1), 157-169.
Elphick, M. R., Mirabeau, O., & Larhammar, D. (2018). Evolution of neuropeptide signalling systems. Journal of Experimental Biology, 221(3), jeb15109. https://doi.org/10.1242/jeb.151092
Farr, J. A., Travis, J., & Trexler, J. C. (1986). Behavioural allometry and interdemic variation in sexual behaviour of the sailfin molly, Poecilia latipinna (Pisces: Poeciliidae). Animal Behaviour, 34(2), 497-509. https://doi.org/10.1016/S0003-3472(86)80118-X
Fox, J., & Weisberg, S. (2019). An R companion to applied regression (third). Sage.
Fraser, B. A., Janowitz, I., Thairu, M., Travis, J., & Hughes, K. A. (2014). Phenotypic and genomic plasticity of alternative male reproductive tactics in sailfin mollies. Proceedings of the Royal Society B: Biological Sciences, 281(1781), 23-25.
Friard, O., & Gamba, M. (2016). BORIS: A free, versatile open-source event-logging software for video/audio coding and live observations. Methods in Ecology and Evolution, 7(11), 1324-1330.
Fricke, C., Bretman, A., & Chapman, T. (2010). Sexual conflict. In D. F. Westneat, & C. W. Fox (Eds.), Evolutionary behavioral ecology (pp. 400-4015). Oxford University Press.
Gammie, S. C., Auger, A. P., Jessen, H. M., Vanzo, R. J., Awad, T. A., & Stevenson, S. A. (2007). Altered gene expression in mice selected for high maternal aggression. Genes, Brain and Behavior, 6(5), 432-443. https://doi.org/10.1111/j.1601-183X.2006.00271.x
Hartig, F. (2020). DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models. https://cran.r-project.org/web/packages/DHARMa/vignettes/DHARMa.html
He, L., Davila-Velderrain, J., Sumida, T. S., Hafler, D. A., Kellis, M., & Kulminski, A. M. (2021). NEBULA is a fast negative binomial mixed model for differential or co-expression analysis of large-scale multi-subject single-cell data. Communications Biology, 4(1), 1-17. https://doi.org/10.1038/s42003-021-02146-6
Huey, R. B., Hertz, P. E., & Sinervo, B. (2003). Behavioral drive versus behavioral inertia in evolution: A null model approach. American Naturalist, 161(3), 357-366. https://doi.org/10.1086/346135
Immonen, E., Sayadi, A., Bayram, H., & Arnqvist, G. (2017). Mating changes sexually dimorphic gene expression in the seed beetle Callosobruchus maculatus. Genome Biology and Evolution, 9(3), 677-699. https://doi.org/10.1093/gbe/evx029
Iuso, A., Sibon, O. C. M., Gorza, M., Heim, K., Organisti, C., Meitinger, T., & Prokisch, H. (2014). Impairment of Drosophila orthologs of the human orphan protein C19orf12 induces bang sensitivity and neurodegeneration. PLoS One, 9(2), e89439. https://doi.org/10.1371/journal.pone.0089439
Jékely, G., Melzer, S., Beets, I., Kadow, I. C. G., Koene, J., Haddad, S., & Holden-Dye, L. (2018). The long and the short of it-A perspective on peptidergic regulation of circuits and behaviour. Journal of Experimental Biology, 221(3), jeb.166710. https://doi.org/10.1242/jeb.166710
Johns, J. L., Roberts, J. A., Clark, D. L., & Uetz, G. W. (2009). Love bites: Male fang use during coercive mating in wolf spiders. Behavioral Ecology and Sociobiology, 64(1), 13-18. https://doi.org/10.1007/s00265-009-0812-8
Kramer, K. M., Choe, C., Carter, C. S., & Cushing, B. S. (2006). Developmental effects of oxytocin on neural activation and neuropeptide release in response to social stimuli. Hormones and Behavior, 49(2), 206-214. https://doi.org/10.1016/j.yhbeh.2005.07.001
Kuruvilla, F. G., Park, P. J., & Schreiber, S. L. (2002). Vector algebra in the analysis of genome-wide expression data. Genome Biology, 3(3), 1-11.
Lenth, R. V. (2021). emmeans: Estimated Marginal Means, aka Least-Squares Means (1.7.0). https://cran.r-project.org/package=emmeans
Madani, R., Poirier, R., Wolfer, D. P., Welzl, H., Groscurth, P., Lipp, H., Lu, B., Mouedden, M. E., Mercken, M., Nitsch, R. M., & Mohajeri, M. H. (2006). Lack of neprilysin suffices to generate murine amyloid-like deposits in the brain and behavioral deficit in vivo. Journal of Neuroscience Research, 84(8), 1871-1878. https://doi.org/10.1002/jnr.21074
Mäkinen, H., Papakostas, S., Vøllestad, L. A., Leder, E. H., & Primmer, C. R. (2016). Plastic and evolutionary gene expression responses are correlated in European grayling (Thymallus thymallus) subpopulations adapted to different thermal environments. Journal of Heredity, 107(1), 82-89.
Markow, T. A. (1987). Behavioral and sensory basis of courtship success in Drosophila melanogaster. Proceedings of the National Academy of Sciences, 84(17), 6200-6204. https://doi.org/10.1073/pnas.84.17.6200
Markow, T. A. (2000). Forced matings in natural populations of Drosophila. American Naturalist, 156(1), 100-103.
McKay, J. P., Nightingale, B., & Pollock, J. A. (2008). Helmsman is expressed in both trachea and photoreceptor development: Partial inactivation alters tracheal morphology and visually guided behavior. Journal of Neurogenetics, 22(2), 117-137.
McKinney, F., Derrickson, S. R., & Mineau, P. (1983). Forced copulation in waterfowl. Behaviour, 86(3), 250-294.
McKinney, F., & Evarts, S. (1998). Sexual coercion in waterfowl and other birds. Ornithological Monographs, 49, 163-195. https://doi.org/10.2307/40166723
McLean, C. A., Chan, R., Dickerson, A. L., Moussalli, A., & Stuart-Fox, D. (2016). Social interactions generate mutually reinforcing selection for male aggression in Lake Eyre dragons. Behavioral Ecology, 27(4), 1149-1157. https://doi.org/10.1093/beheco/arw028
Muller, M. N., & Wrangham, R. W. (Eds.). (2009). Sexual coercion in primates and humans. Harvard University Press.
Nässel, D. (2014). Neuropeptides regulating Drosophila behavior. In J. Dubnau (Ed.), Behavioral genetics of the fly (Drosophila melanogaster) (pp. 20-36). Cambridge University Press.
Nässel, D. R., & Larhammar, D. (2013). Neuropeptides and peptide hormones. In C. G. Galizia, & P.-M. Lledo (Eds.), Neurosciences-From molecule to behavior: A university textbook (pp. 213-237). Springer.
Olsson, M. (2017). Forced copulation and costly female resistance behavior in the Lake Eyre Dragon. Ctenophorus Maculosus, 51(1), 19-24.
Oostra, V., Saastamoinen, M., Zwaan, B. J., & Wheat, C. W. (2018). Strong phenotypic plasticity limits potential for evolutionary responses to climate change. Nature Communications, 9(1), 1005. https://doi.org/10.1038/s41467-018-03384-9
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A., & Kingsford, C. (2017). Salmon provides fast and bias-aware quantification of transcript expression. Nature Methods, 14(4), 417-419. https://doi.org/10.1038/nmeth.4197
Perry, J. C., & Rowe, L. (2012). Sexual conflict and antagonistic coevolution across water strider populations. Evolution, 66(2), 544-557. https://doi.org/10.1111/j.1558-5646.2011.01464.x
Price, T. D., Qvarnström, A., & Irwin, D. E. (2003). The role of phenotypic plasticity in driving genetic evolution. Proceedings of the Royal Society B: Biological Sciences, 270(1523), 1433-1440.
R Core Team. (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.r-project.org/
Radersma, R., Noble, D. W. A., & Uller, T. (2020). Plasticity leaves a phenotypic signature during local adaptation. Evolution Letters, 4(4), 360-370. https://doi.org/10.1002/evl3.185
Ries, A. S., Hermanns, T., Poeck, B., & Strauss, R. (2017). Serotonin modulates a depression-like state in Drosophila responsive to lithium treatment. Nature Communications, 8, 1-11. https://doi.org/10.1038/ncomms15738
Ritchie, M. E., Phipson, B., Wu, D., Hu, Y., Law, C. W., Shi, W., & Smyth, G. K. (2015). limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Research, 43(7), e47. https://doi.org/10.1093/nar/gkv007
Robinson, B. W., & Dukas, R. (1999). The influence of phenotypic modifications on evolution: The Baldwin effect and modern perspectives. Oikos, 85(3), 582-589. https://doi.org/10.2307/3546709
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010). edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26(1), 139-140. https://doi.org/10.1093/bioinformatics/btp616
Saisawang, C., Wongsantichon, J., & Ketterman, A. J. (2012). A preliminary characterization of the cytosolic glutathione transferase proteome from Drosophila melanogaster. Biochemical Journal, 422(1), 181-190.
Scheiner, S. M., & Levis, N. A. (2021). The loss of phenotypic plasticity via natural selection: genetic assimilation. In D. W. Pfennig (Ed.), Phenotypic plasticity and evolution: Causes, consequences, controversies (pp. 161-181). CRC Press.
Schoofs, L., De Loof, A., & Van Hiel, M. B. (2017). Neuropeptides as regulators of behavior in insects. Annual Review of Entomology, 62, 35-52. https://doi.org/10.1146/annurev-ento-031616-035500
Scoville, A. G., & Pfrender, M. E. (2010). Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proceedings of the National Academy of Sciences of the United States of America, 107(9), 4260-4263. https://doi.org/10.1073/pnas.0912748107
Seeley, C., & Dukas, R. (2011). Teneral matings in fruit flies: Male coercion and female response. Animal Behaviour, 81(3), 595-601. https://doi.org/10.1016/j.anbehav.2010.12.003
Shine, R., Langkilde, T., & Mason, R. T. (2003). Cryptic forcible insemination: Male snakes exploit female physiology, anatomy, and behavior to obtain coercive matings. American Naturalist, 162(5), 653-667. https://doi.org/10.1086/378749
Shultzaberger, R. K., Johnson, S. J., Wagner, J., Ha, K., Markow, T. A., & Greenspan, R. J. (2019). Conservation of the behavioral and transcriptional response to social experience among Drosophilids. Genes, Brain and Behavior, 18(1), 1-13.
Smuts, B. B., & Smuts, R. W. (1993). Male aggression and sexual coercion of females in nonhuman primates and other mammals: Evidence and theoretical implications. Advances in the Study of Behavior, 22, 1-63.
Soneson, C., Love, M. I., & Robinson, M. D. (2015). Differential analyses for RNA-seq: Transcript-level estimates improve gene-level inferences. F1000Research, 4(2), 1521. https://doi.org/10.12688/f1000research.7563.1
Taghert, P. H., & Nitabach, M. N. (2012). Peptide neuromodulation in invertebrate model systems. Neuron, 76(1), 82-97. https://doi.org/10.1016/j.neuron.2012.08.035
Thornhill, R. (1980). Rape in Panorpa scorpionflies and a general rape hypothesis. Animal Behaviour, 28(1), 52-59.
Tierney, A. J. (2020). Feeding, hunger, satiety and serotonin in invertebrates. Proceedings of the Royal Society B: Biological Sciences, 287(1932).
Waddington, C. H. (1942). Canalization of development and the inheritance of acquired characters. Nature, 150(3811), 563-565.
Wang, L., Dankert, H., Perona, P., & Anderson, D. J. (2008). A common genetic target for environmental and heritable influences on aggressiveness in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 105(15), 5657-5663.
Wigby, S., & Chapman, T. (2005). Sex peptide causes mating costs in female Drosophila melanogaster. Current Biology, 15(4), 316-321. https://doi.org/10.1016/j.cub.2005.01.051
Zhang, W., Reeves, G. R., & Tautz, D. (2021). Testing implications of the omnigenic model for the genetic analysis of loci identified through genome-wide association. Current Biology, 31(5), 1092-1098.e6. https://doi.org/10.1016/j.cub.2020.12.023
Zhu, A., Ibrahim, J. G., & Love, M. I. (2019). Heavy-tailed prior distributions for sequence count data: Removing the noise and preserving large differences. Bioinformatics, 35(12), 2084-2092. https://doi.org/10.1093/bioinformatics/bty895
Zinna, R., Emlen, D., Lavine, L. C., Johns, A., Gotoh, H., Niimi, T., & Dworkin, I. (2018). Sexual dimorphism and heightened conditional expression in a sexually selected weapon in the Asian rhinoceros beetle. Molecular Ecology, 27(24), 5049-5072. https://doi.org/10.1111/mec.14907
Zirin, J., Hu, Y., Liu, L., Yang-Zhou, D., Colbeth, R., Yan, D., Ewen-Campen, B., Tao, R., Vogt, E., VanNest, S., Cavers, C., Villalta, C., Comjean, A., Sun, J., Wang, X., Jia, Y., Zhu, R., Peng, P., Yu, J., … Perrimon, N. (2020). Large-scale transgenic Drosophila resource collections for loss- and gain-of-function studies. Genetics, 214(4), 755-767.