Conservation of social effects (Ψ) between two species of Drosophila despite reversal of sexual dimorphism

Abstract

Indirect genetic effects (IGEs) describe the effect of the genes of social partners on the phenotype of a focal individual. Here, we measure indirect genetic effects using the “coefficient of interaction” (Ψ) to test whether Ψ evolved between Drosophila melanogaster and D. simulans. We compare Ψ for locomotion between ethanol and nonethanol environments in both species, but only D. melanogaster utilizes ethanol ecologically. We find that while sexual dimorphism for locomotion has been reversed in D. simulans, there has been no evolution of social effects between these two species. What did evolve was the interaction between genotype-specific Ψ and the environment, as D. melanogaster varies unpredictably between environments and D. simulans does not. In this system, this suggests evolutionary lability of sexual dimorphism but a conservation of social effects, which brings forth interesting questions about the role of the social environment in sexual selection.

REFERENCES Bailey, J. K., Genung, M. A., Ware, I., Gorman, C., Van Nuland, M. E., Long, H., et al. (2013). Indirect genetic effects: an evolutionary mechanism linking feedbacks, genotypic diversity and coadaptation in a climate change context. Funct Ecol, 28, 87–95. http://dx.doi.org/10.1111/1365-2435.12154. Bailey, N. W., & Hoskins, J. L. (2014). Detecting cryptic indirect genetic effects. Evolution, 68, 1871–1882. https://doi.org/10.1111/evo.2014.68.issue-7 Bailey, N. W., & Zuk, M. (2012). Socially flexible female choice differs among populations of the Pacific field cricket: Geographical variation in the interaction coefficient psi (Ψ). Genetics, 279, 3589–3596. http://dx.doi.org/10.1098/rspb.2012.0631 Bateman, A. J. (1948). Intra-sexual selection in Drosophila. Heredity, 2, 349–368. https://doi.org/10.1038/hdy.1948.21 Bijma, P. (2014). The quantitative genetics of indirect genetic effects: A selective review of modelling issues. Heredity, 112, 61–69. https://doi.org/10.1038/hdy.2013.15 Bleakley, B. H., & Brodie, E. D. (2009). Indirect genetic effects influence antipredator behavior in guppies: Estimates of the coefficient of interaction psi and the inheritance of reciprocity. Evolution, 63, 1796–1806. https://doi.org/10.1111/evo.2009.63.issue-7 Brakefield, P. M. (2003). Artificial selection and the development of ecologically relevant phenotypes. Ecology, 84, 1661–1671. https://doi.org/10.1890/0012-9658(2003)084[1661:ASATDO]2.0.CO;2 Brinker, T., Bijma, P., Visscher, J., Rodenburg, T. B., & Ellen, E. D. (2014). Plumage condition in laying hens: Genetic parameters for direct and indirect effects in two purebred layer lines. Genetics, Selection, Evolution, 46, 33. https://doi.org/10.1186/1297-9686-46-33 Camerlink, I., Turner, S. P., Bijma, P., & Bolhuis, J. E. (2013). Indirect genetic effects and housing conditions in relation to aggressive behaviour in pigs. PLoS ONE, 8, e65136. https://doi.org/10.1371/journal.pone.0065136 Camerlink, I., Ursinus, W. W., Bijma, P., Kemp, B., & Bolhuis, J. E. (2015). Indirect genetic effects for growth rate in domestic pigs alter aggressive and manipulative biting behaviour. Behavior Genetics, 45, 117–126. https://doi.org/10.1007/s10519-014-9671-9 Campo, D., Lehmann, K., Fjeldsted, C., Souaiaia, T., Kao, J., & Nuzhdin, S. V. (2013). Whole-genome sequencing of two North American Drosophila melanogaster populations reveals genetic differentiation and positive selection. Molecular Ecology, 22, 5084–5097. https://doi.org/10.1111/mec.12468 Chakir, M., Peridy, O., Capy, P., Pla, E., & David, J. R. (1993). Adaptation to alcoholic fermentation in Drosophila: A parallel selection imposed by environmental ethanol and acetic acid. Proceedings of the National Academy of Sciences of the United States of America, 90, 3621–3625. https://doi.org/10.1073/pnas.90.8.3621 Chakraborty, M., & Fry, J. D. (2016). Evidence that environmental heterogeneity maintains a detoxifying enzyme polymorphism in Drosophila melanogaster. Current Biology, 26, 219–223. https://doi.org/10.1016/j.cub.2015.11.049 Chapman, T., Liddle, L. F., Kalb, J. M., & Wolfner, M. F. (1995). Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature, 373, 241–244. https://doi.org/10.1038/373241a0 Chenoweth, S. F., Rundle, H. D., & Blows, M. W. (2010). Experimental evidence for the evolution of indirect genetic effects: Changes in the interaction effect coefficient, psi, due to sexual selection. Evolution, 64, 1849–1856. https://doi.org/10.1111/j.1558-5646.2010.00952.x Cho, W., Heberlein, U., & Wolf, F. W. (2004). Habituation of an odorant-induced startle response in Drosophila. Genes, Brain, and Behavior, 3, 127–137. https://doi.org/10.1111/gbb.2004.3.issue-3 Cobb, M., Burnet, B., & Connolly, K. (1986). The structure of courtship in the Drosophila melanogaster species sub-group. Behaviour, 97, 182–211. https://doi.org/10.1163/156853986X00379 Cobb, M., Connolly, K., & Burnet, B. (1985). Courtship behaviour in the melanogaster species sub-group of Drosophila. Behaviour, 95, 203–230. https://doi.org/10.1163/156853985X00136 Cobb, M., Connolly, K., & Burnet, B. (1987). The relationship between locomotor activity and courtship in the melanogaster species sub-group of Drosophila. Animal Behavior, 35, 705–713. https://doi.org/10.1016/S0003-3472(87)80106-9 Colomb, J., & Brembs, B. (2014). Sub-strains of Drosophila Canton-S differ markedly in their locomotor behavior. F1000Research, 3, 176. https://doi.org/10.12688/f1000research.4263.1 David, J., & Bocquet, C. (1976). Compared toxicities of different alcohols for two Drosophila sibling species: D. melanogaster and D. simulans. Comparative Biochemistry and Physiology. C: Comparative Pharmacology, 54, 71–74. https://doi.org/10.1016/0306-4492(76)90066-6 Dickinson, W. J., Rowan, R. G., & Brennan, M. D. (1984). Regulatory gene evolution: Adaptive differences in expression of alcohol dehydrogenase in Drosophila melanogaster and Drosophila simulans. Heredity, 52(Pt 2), 215–225. https://doi.org/10.1038/hdy.1984.23 Dingemanse, N. J., & Araya-Ajoy, Y. G. (2015). Interacting personalities: Behavioural ecology meets quantitative genetics. Trends in Ecology & Evolution, 30, 88–97. https://doi.org/10.1016/j.tree.2014.12.002 Dorado, G., & Barbancho, M. (1984). Differential responses in Drosophila melanogaster to environmental ethanol: Modification of fitness components at the Adh locus. Heredity, 53, 309–320. https://doi.org/10.1038/hdy.1984.90 Ferguson, C. T. J., O'Neill, T. L., Audsley, N., & Isaac, R. E. (2015). The sexually dimorphic behaviour of adult Drosophila suzukii: Elevated female locomotor activity and loss of siesta is a post-mating response. Journal of Experimental Biology, 218, 3855–3861. https://doi.org/10.1242/jeb.125468 Fiumera, A. C., & Dumont, B. L. (2006). Natural variation in male-induced “cost-of-mating”and allele-specific association with male reproductive genes in Drosophila melanogaster. Philosophical Transactions of the Royal Society of London. Series B, Biological sciences, 361, 355–361. https://doi.org/10.1098/rstb.2005.1791 Friberg, U., & Arnqvist, G. (2003). Fitness effects of female mate choice: Preferred males are detrimental for Drosophila melanogaster females. Journal of Evolutionary Biology, 16, 797–811. https://doi.org/10.1046/j.1420-9101.2003.00597.x Fry, J. D. (2014). Mechanisms of naturally evolved ethanol resistance in Drosophila melanogaster. Journal of Experimental Biology, 217, 3996–4003. https://doi.org/10.1242/jeb.110510 Fry, J. D., Bahnck, C. M., Mikucki, M., Phadnis, N., & Slattery, W. C. (2004). Dietary ethanol mediates selection on Aldehyde dehydrogenase activity in Drosophila melanogaster. Integrative and Comparative Biology, 44, 275–283. https://doi.org/10.1093/icb/44.4.275 Fry, J. D., Donlon, K., & Saweikis, M. (2008). A worldwide polymorphism in aldehyde dehydrogenase in Drosophila melanogaster: Evidence for selection mediated by dietary ethanol. Evolution, 62, 66–75. https://doi.org/10.1111/j.1558-5646.2007.00288.x Garcin, F., Cote, J., Lau You Hin, G., Chawla, S., & Radouco-Thomas, S. (1986). Ethanol metabolizing system in Drosophila. Aldehyde dehydrogenase: Functional aspects in adult and during development. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 10, 167–176. http://dx.doi.org/10.1016/0278-5846(86)90071-0 Gibson, J. B., May, T. W., & Wilks, A. V. (1981). Genetic variation at the alcohol dehydrogenase locus in Drosophila melanogaster in relation to environmental variation: Ethanol levels in breeding sites and allozyme frequencies. Oecologia, 51, 191–198. https://doi.org/10.1007/BF00540600 Gibson, J. B., & Wilks, A. V. (1988). The alcohol dehydrogenase polymorphism of Drosophila melanogaster in relation to environmental ethanol, ethanol tolerance and alcohol dehydrogenase activity. Heredity, 60(Pt 3), 403–414. https://doi.org/10.1038/hdy.1988.58 Grosjean, Y., Rytz, R., Farine, J.-P., Abuin, L., Cortot, J., Jefferis, G. S. X. E., & Benton, R. (2011). An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature, 478, 236–240. https://doi.org/10.1038/nature10428 Hodges, T. K., Laskowski, K. L., Squadrito, G. L., De Luca, M., & Leips, J. (2013). Defense traits of larval Drosophila melanogaster exhibit genetically based trade-offs against different species of parasitoids. Evolution, 67, 749–760. https://doi.org/10.1111/evo.2013.67.issue-3 Hoffmann, A. A., & McKechnie, S. W. (1991). Heritable variation in resource utilization and response in a winery population of Drosophila melanogaster. Evolution, 45, 1000–1015. https://doi.org/10.1111/j.1558-5646.1991.tb04366.x Husak, J. F., & Fox, S. F. (2008). Sexual selection on locomotor performance. Evolutionary Ecology Research, 10, 213–228. Joshi, A., & Thompson, J. N. (1997). Adaptation and specialization in a two-resource environment in Drosophila species. Evolution, 51, 846–855. https://doi.org/10.1111/evo.1997.51.issue-3 Kazancıoğlu, E., Klug, H., & Alonzo, S. H. (2012). The evolution of social interactions changes predictions about interacting phenotypes. Evolution, 66, 2056–2064. https://doi.org/10.1111/evo.2012.66.issue-7 Kent, C., Azanchi, R., Smith, B., Formosa, A., & Levine, J. D. (2008). Social context influences chemical communication in D. melanogaster males. Current Biology, 18, 1384–1389. https://doi.org/10.1016/j.cub.2008.07.088 Kerver, W., & Rotman, G. (1987). Development of ethanol tolerance in relation to the alcohol dehydrogenase locus in Drosophila melanogaster. II. The influence of phenotypic adaptation and maternal. Heredity, 58, 239–248. https://doi.org/10.1038/hdy.1987.38 Kuijper, B., Stewart, A. D., & Rice, W. R. (2006). The cost of mating rises nonlinearly with copulation frequency in a laboratory population of Drosophila melanogaster. Journal of Evolutionary Biology, 19, 1795–1802. https://doi.org/10.1111/jeb.2006.19.issue-6 Lailvaux, S. P., Alexander, G. J., & Whiting, M. J. (2003). Sex-based differences and similarities in locomotor performance, thermal preferences, and escape behaviour in the lizard Platysaurus intermedius wilhelmi. Physiological and Biochemical Zoology, 76, 511–521. https://doi.org/10.1086/376423 Lefèvre, T., de Roode, J. C., Kacsoh, B. Z., & Schlenke, T. A. (2012). Defence strategies against a parasitoid wasp in Drosophila: Fight or flight? Biology Letters, 8, 230–233. https://doi.org/10.1098/rsbl.2011.0725 Li, Y., Fink, C., El-Kholy, S., & Roeder, T. (2015). The octopamine receptor octß2R is essential for ovulation and fertilization in the fruit fly Drosophila melanogaster. Archives of Insect Biochemistry and Physiology, 88, 168–178. https://doi.org/10.1002/arch.v88.3 Long, T. A. F., & Rice, W. R. (2007). Adult locomotory activity mediates intralocus sexual conflict in a laboratory-adapted population of Drosophila melanogaster. Proceedings of the Royal Society of London B: Biological Sciences, 274, 3105–3112. https://doi.org/10.1098/rspb.2007.1140 Maklakov, A. A., & Arnqvist, G. (2009). Testing for direct and indirect effects of mate choice by manipulating female choosiness. Current Biology, 19, 1903–1906. https://doi.org/10.1016/j.cub.2009.08.058 Marie-Orleach, L., Vogt-Burri, N., Mouginot, P., Schlatter, A., Vizoso, D. B., Bailey, N. W., & Schärer, L. (2017). Indirect genetic effects and sexual conflicts: Partner genotype influences multiple morphological and behavioral reproductive traits in a flatworm. Evolution, 71, 1232–1245. https://doi.org/10.1111/evo.13218 McKechnie, S. W., & Morgan, P. (1982). Alcohol dehydrogenase polymorphism of Drosophila melanogaster: Aspects of alcohol and temperature variation in the larval environment. Australian Journal of Biological Sciences, 35, 85–93. https://doi.org/10.1071/BI9820085 McKenzie, J. A., & McKechnie, S. W. (1979). A comparative study of resource utilization in natural populations of Drosophila melanogaster and D. simulans. Oecologia, 40, 299–309. https://doi.org/10.1007/BF00345326 Mercot, H., Defaye, D., Capy, P., Pla, E., & David, J. R. (1994). Alcohol tolerance, ADH activity, and ecological niche of Drosophila species. Evolution, 3, 746–757. https://doi.org/10.1111/evo.1994.48.issue-3 Milan, N. F., Kacsoh, B. Z., & Schlenke, T. A. (2012). Alcohol consumption as self-medication against blood-borne parasites in the fruit fly. Current Biology, 22, 488–493. https://doi.org/10.1016/j.cub.2012.01.045 Moore, A. J., Brodie III, E. D., & Wolf, J. B. (1997). Interacting phenotypes and the evolutionary process: I. Direct and indirect genetic effects of social interactions. Evolution, 51, 1352–1362. https://doi.org/10.1111/evo.1997.51.issue-5 Moore, A. J., & Pizzari, T. (2005). Quantitative genetic models of sexual conflict based on interacting phenotypes. American Naturalist, 165, S88–S97. https://doi.org/10.1086/429354 Muhammed-Ali, A., & Burnet, B. (1995). Ethanol tolerance and variation at the alcohol dehydrogenase (Adh) locus of Drosophila mauritiana. Heredity, 74, 438–444. https://doi.org/10.1038/hdy.1995.61 Nuzhdin, S. V., Friesen, M. L., & McIntyre, L. M. (2012). Genotype–phenotype mapping in a post-GWAS world. Trends in Genetics, 28, 421–426. https://doi.org/10.1016/j.tig.2012.06.003 Olson-Manning, C. F., Wagner, M. R., & Mitchell-Olds, T. (2012). Adaptive evolution: Evaluating empirical support for theoretical predictions. Nature Reviews Genetics, 13, 867–877. https://doi.org/10.1038/nrg3322 Parsons, P. A. (1977). Larval reaction to alcohol as an indicator of resource utilization differences between Drosophila melanogaster and D. simulans. Oecologia, 30, 141–146. https://doi.org/10.1007/BF00345417 Parsons, P. A., & King, S. B. (1977). Ethanol: Larval discrimination between two Drosophila sibling species. Experientia, 33, 898–899. https://doi.org/10.1007/BF01951269 Parsons, P. A., & Spence, G. E. (1981). Ethanol utilization: Threshold differences among three Drosophila species. American Naturalist, 117, 568–571. https://doi.org/10.1086/283740 Partridge, L., Green, A., & Fowler, K. (1987). Effects of egg-production and of exposure to males on female survival in Drosophila melanogaster. Journal of Insect Physiology, 33, 745–749. https://doi.org/10.1016/0022-1910(87)90060-6 Peeters, K., Eppink, T. T., Ellen, E. D., & Visscher, J. (2012). Indirect genetic effects for survival in domestic chickens (Gallus gallus) are magnified in crossbred genotypes and show a parent-of-origin effect. Genetics, 192, 705–713. https://doi.org/10.1534/genetics.112.142554 Perry, G. (1996). The evolution of sexual dimorphism in the lizard Anolis polylepis (Iguania): Evidence from intraspecific variation in foraging behavior and diet. Canadian Journal of Zoology, 74, 1238–1245. https://doi.org/10.1139/z96-137 Peterson, C. C., & Husak, J. F. (2006). Locomotor performance and sexual selection: Individual variation in sprint speed of collared lizards (Crotaphytus collaris). Copeia, 2, 216–224. https://doi.org/10.1643/0045-8511(2006)6[216:LPASSI]2.0.CO;2 Pitnick, S. (1991). Male size influences mate fecundity and remating interval in Drosophila melanogaster. Animal Behavior, 41, 735–745. https://doi.org/10.1016/S0003-3472(05)80340-9 Pitnick, S., & Garcia-Gonzalez, F. (2002). Harm to females increases with male body size in Drosophila melanogaster. Proceedings of the Royal Society of London B: Biological Sciences, 269, 1821–1828. https://doi.org/10.1098/rspb.2002.2090 Saltz, J. B. (2013). Genetic composition of social groups influences male aggressive behaviour and fitness in natural genotypes of Drosophila melanogaster. Genetics, 280, 20131926. https://doi.org/10.1098/rspb.2013.1926 Signor, S. A., Abbasi, M., Marjoram, P., & Nuzhdin, S. V. (2017). Indirect genetic effects mediate a conflict in locomotion among Drosophila melanogaster males and females. Evolution, 71, 1765–1775. Taylor, M. L., Wedell, N., & Hosken, D. J. (2007). Sexual selection and female fitness in Drosophila simulans. Behavioral Ecology and Sociobiology, 62, 721–728. Taylor, M. L., Wigmore, C., Hodgson, D. J., Wedell, N., & Hosken, D. J. (2008). Multiple mating increases female fitness in Drosophila simulans. Animal Behavior, 76, 963–970. https://doi.org/10.1016/j.anbehav.2008.05.015 Thomson, M. S., Jacobson, J. W., & Laurie, C. C. (1991). Comparison of alcohol dehydrogenase expression in Drosophila melanogaster and D. simulans. Molecular Biology and Evolution, 8, 31–48. Tompkins, L., Gross, A. C., Hall, J. C., Gailey, D. A., & Siegel, R. W. (1982). The role of female movement in the sexual behavior of Drosophila melanogaster. Behavior Genetics, 12, 295–307. https://doi.org/10.1007/BF01067849 Wahlsten, D. (2001). Standardizing tests of mouse behavior: Reasons, recommendations, and reality. Physiology & Behavior, 73, 695–704. https://doi.org/10.1016/S0031-9384(01)00527-3 Wigby, S., & Chapman, T. (2004). Female resistance to male harm evolves in response to manipulation of sexual conflict. Evolution, 58, 1028–1037. https://doi.org/10.1111/evo.2004.58.issue-5 Wolf, J. B., Brodie III, E. D., Cheverud, J. M., Moore, A. J., & Wade, M. J. (1998). Evolutionary consequences of indirect genetic effects. Trends in Ecology & Evolution, 13, 64–69. https://doi.org/10.1016/S0169-5347(97)01233-0 Yang, H.-P., & Nuzhdin, S. V. (2003). Fitness costs of Doc expression are insufficient to stabilize its copy number in Drosophila melanogaster. Molecular Biology and Evolution, 20, 800–804. https://doi.org/10.1093/molbev/msg087 Zhu, J., & Fry, J. D. (2015). Preference for ethanol in feeding and oviposition in temperate and tropical populations of Drosophila melanogaster. Entomologia Experimentalis et Applicata, 155, 64–70. https://doi.org/10.1111/eea.12285 Ziolo, L. K., & Parsons, P. A. (1982). Ethanol tolerance, alcohol-dehydrogenase activity and Adh allozymes in Drosophila melanogaster. Genetica, 57, 231–237. https://doi.org/10.1007/BF00056488