Sociability in Fruit Flies: Genetic Variation, Heritability and Plasticity
Sociability, defined as individuals’ propensity to participate in non-aggressive activities with conspecifics, is a fundamental feature of behavior in many animals including humans. However, we still have a limited knowledge of the mechanisms and evolutionary biology of sociability. To enhance our understanding, we developed a new protocol to quantify sociability in fruit flies (Drosophila melanogaster). In a series of experiments with 59 F1 hybrids derived from inbred lines, we documented, first, significant genetic variation in sociability in both males and females, with broad-sense heritabilities of 0.24 and 0.21 respectively. Second, we observed little genetic correlation in sociability between the sexes. Third, we found genetic variation in social plasticity among the hybrids, with a broad-sense heritability of ~0.24. That is, genotypes differed in the degree of sociability after experiencing the same relevant social experience. Our data pave the way for further research on the mechanisms that underlie sociability as well as its ecological and evolutionary consequences.
KeywordsDrosophila melanogaster Fruit flies Genetic variation, heritability Plasticity Reaction norms Sociability, social behavior
We thank B. Bolker for statistical advice and S. Lodhi, A. Sivajohan, E. Etzler, I. Shams, S. Tao, and C. Baxter for assistance and three anonymous referees for comments.
This work was supported by the Natural Sciences and Engineering Research Council of Canada 2014–03999 to RD, Canada Foundation for Innovation, and Ontario Ministry of Research and Innovation.
Compliance with ethical standards
Conflict of interest
AM Scott, I Dworkin and R Dukas declare that they have no conflict of interest.
Human and animal rights and informed consent
This article does not contain any studies with human participants or animals performed by any of the authors.
- Abrahams BS, Geschwind DH (2008) Advances in autism genetics: on the threshold of a new neurobiology. Nat Rev Genet 9:341–355. http://www.nature.com/nrg/journal/v9/n5/suppinfo/nrg2346_S1.html
- Ashburner M (1989) Drosophila a laboratory handbook. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
- Bartholomew NR, Burdett JM, VandenBrooks JM, Quinlan MC, Call GB (2015) Impaired climbing and flight behaviour in Drosophila melanogaster following carbon dioxide anaesthesia. Sci Rep 5:15298. https://doi.org/10.1038/srep15298 http://www.nature.com/articles/srep15298#supplementary-information
- Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1–10. http://CRAN.R-project.org/package=lme4. Accessed 14 June 2017
- Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A et al (2017) Modeling zero-inflated count data with glmmtmb. bioRxiv 2017:132753Google Scholar
- Canty A, Ripley B (2017) boot: Bootstrap R (S-Plus) Functions. R package version, pp 13–20Google Scholar
- Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Benjamin Cummings, New YorkGoogle Scholar
- Fox J, Weisberg S (2011) An R companion to applied regression. SAGE Inc, Thousand OaksGoogle Scholar
- Gómez JM, Verdú M, González-Megías A, Méndez M (2016) The phylogenetic roots of human lethal violence. Nat Adv. https://doi.org/10.1038/nature19758. http://www.nature.com/nature/journal/vaop/ncurrent/abs/nature19758.html#supplementary-information
- Greenspan RJ (2004) Fly pushing: the theory and practice of Drosophila genetics. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
- Krebs CJ (1999) Ecological methodology, 2 edn. Addison-Wesley, Menlo ParkGoogle Scholar
- Mackay TFC, Richards S, Stone EA, Barbadilla A, Ayroles JF, Zhu D et al (2012) The Drosophila melanogaster genetic reference panel. Nature 482:173–178. http://www.nature.com/nature/journal/v482/n7384/abs/nature10811.html#supplementary-information
- R-Core-Team (2014) R: a language and environment for statistical computing, Vienna. http://www.R-project.org. Accessed 14 June 2017
- Silverman JL, Yang M, Lord C, Crawley JN (2010) Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci 11:490–502. http://www.nature.com/nrn/journal/v11/n7/suppinfo/nrn2851_S1.html
- Thomas JW, Cáceres M, Lowman JJ, Morehouse CB, Short ME, Baldwin EL et al (2008) The chromosomal polymorphism linked to variation in social behavior in the white-throated sparrow (Zonotrichia albicollis) is a complex rearrangement and suppressor of recombination. Genetics 179:1455CrossRefPubMedPubMedCentralGoogle Scholar
- Tuttle AH, Tansley S, Dossett K, Tohyama S, Khoutorsky A, Maldonado-Bouchard S et al (2017) Social propinquity in rodents as measured by tube cooccupancy differs between inbred and outbred genotypes. Proc Natl Acad Sci 114:5515–5520. https://doi.org/10.1073/pnas.1703477114 CrossRefPubMedPubMedCentralGoogle Scholar
- van den Berg SM, de Moor MHM, Verweij KJH, Krueger RF, Luciano M, Arias Vasquez A et al (2016) Meta-analysis of genome-wide association studies for extraversion: findings from the genetics of personality consortium. Behav Genet 46:170–182. https://doi.org/10.1007/s10519-015-9735-5 CrossRefPubMedGoogle Scholar
- Walum H, Westberg L, Henningsson S, Neiderhiser JM, Reiss D, Igl W et al (2008) Genetic variation in the vasopressin receptor 1a gene (AVPR1A) associates with pair-bonding behavior in humans. Proc Natl Acad Sci 105:14153–14156. https://doi.org/10.1073/pnas.0803081105 CrossRefPubMedPubMedCentralGoogle Scholar
- Wilson EO (1975) Sociobiology: the new synthesis. Harvard University Press, CambridgeGoogle Scholar
- Zhang B, Freeman MR, Waddell S (2010) Drosophila neurobiology: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar