Behavioral idiosyncrasy reveals genetic control of phenotypic variability
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Abstract
Significance: If we could rear genetically identical individuals from a variety of genetic backgrounds and rear them in the same environment, how much phenotypic variation between individuals of the same genotype would we see? Would different genetic backgrounds differ in their degree of variability? What would account for these differences? We used Drosophila inbred lines to address these questions focusing on variability in locomotor handedness. We show that different genotypes vary dramatically in their propensity for variability, that phenotypic variability itself, as a trait, can be heritable, and that loci affecting variability can be mapped. The genetic control of variability has received little attention in quantitative genetics despite the important role variability plays in explaining phenotypic variation between individuals.
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Our results provide insight into mechanisms underlying individual differences in navigation behavior.
“Our results also provide insight into mechanisms underlying individual differences in navigation behavior53,54.”
From Multimodal cue integration and learning in a neural representation of head direction (2025) · cites this paper as [53]
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Werkhoven, Z., Bravin, A., Skutt-Kakaria, K., Reimers, P., Pallares, L. F., Ayroles, J., & de Bivort, B. (2019) · bioRxiv · doi:10.7554/elife.64988 · Cited by 49 · see citing works
“, genetic variation (Ayroles et al., 2015), or neural state variation (Kain et al.”
BackgroundSelf-citationWerkhoven, Z., Rohrsen, C., Qin, C., Brembs, B., & de Bivort, B. (2019) · bioRxiv · doi:10.1371/journal.pone.0224243 · Cited by 47 · see citing works
“The wild-type fly lines we screened displayed population level differences in both mean preference and variability in phototactic bias [29].”
BackgroundMitchell, D., Fanson, B., Beckmann, C., & Biro, P. (2016) · Royal Society Open Science · doi:10.1098/rsos.160352 · Cited by 47
“Furthermore, rIIV in non-behavioural traits and residual intragenotypic variability have heritable components [13,15] which demonstrates rIIV could be viewed as a trait that could be selected upon.”
BackgroundanTraX, a software package for high-throughput video tracking of color-tagged insects
Gal, A., Saragosti, J., & Kronauer, D. J. C. (2020) · eLife · doi:10.7554/elife.58145 · Cited by 75 · see citing works
“…toward understanding more complex behavioral phenomena such as social interactions, individuality and inter-species interactions ( Schneider et al., 2012 ; Seeholzer et al., 2018 ; Schneider and Levine, 2014 ; Honegger and de Bivort, 2018 ; Ayroles et al., 2015 ; Akhund-Zade et al., 2019 ).”
BackgroundFrom the trajectory of heritability to the heritability of trajectories
Campbell, A., Munafò, M., Sallis, H., Pearson, R., & Smith, D. (2020) · bioRxiv · doi:10.1101/2020.06.23.167676 · Cited by 41
Gene expression variability and the analysis of large-scale RNA-seq studies with the MDSeq
Ran, D., & Daye, Z. J. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx456 · Cited by 38 · see citing works
Akhund-Zade, J., Ho, S., O’Leary, C., & de Bivort, B. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.202234 · Cited by 39 · see citing works
“Our research has identified intragenotypic variability in isogenic lines of D. melanogaster for turning bias, phototaxis and thermotaxis (Ayroles et al., 2015; Kain et al., 2012, 2015).”
BackgroundMethodInfluentialSelf-citationAdvancing behavioural genomics by considering timescale
Rittschof, C. C., & Hughes, K. A. (2018) · Nature Communications · doi:10.1038/s41467-018-02971-0 · Cited by 42 · see citing works
Co-opting evo-devo concepts for new insights into mechanisms of behavioural diversity
Hoke, K. L., Adkins–Regan, E., Bass, A. H., McCune, A. R., & Wolfner, M. F. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.190058 · Cited by 40 · see citing works
“The ability to identify the genetic underpinnings of behavioural variation, such as the natural allelic variation in the Drosophila Ten-a gene, which predicts variation in the laterality of turns within inbred fly strains (Ayroles et al., 2015), offers opportunities to show how genetic variation shapes robustness and…”
BackgroundMicroenvironmental Gene Expression Plasticity Among IndividualDrosophila melanogaster
Lin, Y., Chen, Z., Oliver, B., & Harbison, S. T. (2016) · G3 Genes Genomes Genetics · doi:10.1534/g3.116.035444 · Cited by 37 · see citing works
“…can be found in (Lin et al. 2016) and in the Gene Expression Omnibus (GEO) entry (GSE60314) (see “DGRP_Number,” “Sex,” Environment,” “Fly_Number,” and “Fly_Plate_Location” in the GSE60314_GEO_run_summary.xlsx file, GEO entry GSE60314, for the order of genotypes, sexes, and replicate environments).”
BackgroundInfluentialWord learning dogs (Canis familiaris) provide an animal model for studying exceptional performance
Fugazza, C., Dror, S., Sommese, A., Temesi, A., & Miklósi, Á. (2021) · Scientific Reports · doi:10.1038/s41598-021-93581-2 · Cited by 36 · see citing works
Environmental variation partitioned into separate heritable components
Ørsted, M., Rohde, P. D., Hoffmann, A., Sørensen, P., & Kristensen, T. (2018) · Evolution; international journal of organic evolution · doi:10.1111/evo.13391 · Cited by 36
Statistical tests for detecting variance effects in quantitative trait studies
Dumitrascu, B., Darnell, G., Ayroles, J. F., & Engelhardt, B. E. (2018) · Bioinformatics · doi:10.1093/bioinformatics/bty565 · Cited by 35 · see citing works
Self-citationStochastic and Conditional Regulation of Nematode Mouth-Form Dimorphisms
Susoy, V., & Sommer, R. (2016) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2016.00023 · Cited by 31 · see citing works
Nagel, K., Lenz, H., Kastenholz, B., Gilmer, F., Averesch, A., Putz, A., Heinz, K., Fischbach, A., Scharr, H., Fiorani, F., et al. (2020) · Plant Methods · doi:10.1186/s13007-020-00631-3 · Cited by 30 · see citing works
“Therefore, the observed intra-genotypic variability could rather be caused by unintentional micro-environmental perturbations and stochasticity (randomness) in root development [4, 27].”
BackgroundVersace, E., Caffini, M., Werkhoven, Z., & de Bivort, B. (2019) · Scientific Reports · doi:10.1038/s41598-020-61410-7 · Cited by 29 · see citing works
Precise Quantification of Behavioral Individuality From 80 Million Decisions Across 183,000 Flies
de Bivort, B., Buchanan, S. M., Skutt-Kakaria, K., Gajda, E., Ayroles, J., O’Leary, C., Reimers, P., Akhund-Zade, J., Senft, R. A., Maloney, R., et al. (2021) · bioRxiv · doi:10.3389/fnbeh.2022.836626 · Cited by 28 · see citing works
Self-citationAlisch, T., Crall, J. D., Kao, A. B., Zucker, D., & de Bivort, B. L. (2018) · eLife · doi:10.7554/elife.37166 · Cited by 38 · see citing works
Measuring the repertoire of age-related behavioral changes in Drosophila melanogaster
Overman, K. E., Choi, D. M., Leung, K., Shaevitz, J., & Berman, G. J. (2021) · bioRxiv · doi:10.1371/journal.pcbi.1009867 · Cited by 27 · see citing works
“[20] Ayroles JF, Buchanan SM, O’Leary C, Skutt-Kakaria”
Honeybee communication during collective defence is shaped by predation
López-Incera, A., Nouvian, M., Ried, K., Müller, T., & Briegel, H. (2020) · BMC Biology · doi:10.1186/s12915-021-01028-x · Cited by 27 · see citing works
“In this case, selection should act on the mechanisms controlling this individual variability, to ensure that an appropriate distribution of thresholds is maintained across generations [31].”
BackgroundThe road less traveled: from genotype to phenotype in flies and humans
Anholt, R. R. H., & Mackay, T. F. C. (2017) · Mammalian Genome · doi:10.1007/s00335-017-9722-7 · Cited by 25 · see citing works
Resolving the Complex Genetic Basis of Phenotypic Variation and Variability of Cellular Growth
Ziv, N., Shuster, B., Siegal, M. L., & Gresham, D. (2017) · Genetics · doi:10.1534/genetics.116.195180 · Cited by 25
“Bauer, C. R., S. Li, and M. L. Siegal, 2015 Essential gene disruptions reveal complex relationships between phenotypic robustness, pleiotropy, and fitness.”
BackgroundSell-Kubiak, E., Knol, E., & Lopes, M. (2022) · Genetics Selection Evolution · doi:10.1186/s12711-021-00692-5 · Cited by 23 · see citing works
“[56] Drosophila melanogaster Locomotor handedness”
Behavior Individuality: A Focus on Drosophila melanogaster
Mollá-Albaladejo, R., & Sánchez‐Alcañiz, J. A. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.719038 · Cited by 30 · see citing works
A sibling method for identifying vQTLs
Conley, D., Johnson, R., Domingue, B. W., Dawes, C. T., Boardman, J., & Siegal, M. L. (2018) · PLoS ONE · doi:10.1371/journal.pone.0194541 · Cited by 21 · see citing works
Idiosyncratic learning performance in flies
Smith, M. A.-Y., Honegger, K. S., Turner, G. C., & de Bivort, B. L. (2022) · Biology Letters · doi:10.1098/rsbl.2021.0424 · Cited by 39 · see citing works
Environmental and Molecular Modulation of Motor Individuality in Larval Zebrafish
Hageter, J., Waalkes, M., Starkey, J., Copeland, H., Price, H., Bays, L. D., Showman, C., Laverty, S. M., Bergeron, S. A., & Horstick, E. J. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.777778 · Cited by 23 · see citing works
“…use same-direction turns, and the magnitude of this bias is modulated by genetic background, activity in the central complex, and exposure to environmental enrichment as well as social experiences (Ayroles et al., 2015; Buchanan et al., 2015; Akhund-Zade et al., 2019; Versace et al., 2020).”
BackgroundBayesian updating during development predicts genotypic differences in plasticity
Stamps, J. A., Biro, P. A., Mitchell, D. J., & Saltz, J. B. (2018) · Evolution · doi:10.1111/evo.13585 · Cited by 24 · see citing works
Modelling the co-evolution of indirect genetic effects and inherited variability
Marjanovic, J., Mulder, H., Rönnegård, L., & Bijma, P. (2018) · Heredity · doi:10.1038/s41437-018-0068-z · Cited by 21
“2008), and locomotor behavior in fruit flies (Ayroles et al. 2015).”
On the relationship between epistasis and genetic variance-heterogeneity
Forsberg, S., & Carlborg, Ö. (2017) · bioRxiv · doi:10.1101/119727 · Cited by 21
“A growing body of evidence suggests that phenotypic variability can be genetically controlled (Rönnegård and Valdar, 2011; Shen et al., 2012; Ayroles et al., 2015).”
BackgroundA neural correlate of individual odor preference in DrosophilaPreprint
Churgin, M. A., Lavrentovich, D., Smith, M. A., Gao, R.-X., Boyden, E., & de Bivort, B. (2021) · bioRxiv · doi:10.1101/2021.12.24.474127 · Cited by 20 · see citing works
“The high-level functions of the AL that represent a baseline, working condition were: (1) firing rates for ORNs, LNs, and PNs matching the literature (listed in Table 318,38–40, (2) a more uniform distribution of PN firing rates during odor stimuli compared to ORN firing rates, (3) greater separation of representation…”
BackgroundWhy behavioral neuroscience still needs diversity?: A curious case of a persistent need.
Mathuru, A., Libersat, F., Vyas, A., & Teseo, S. (2020) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.06.021 · Cited by 20 · see citing works
A neural circuit basis for context-modulation of individual locomotor behaviorPreprint
Skutt-Kakaria, K., Reimers, P., Currier, T. A., Werkhoven, Z., & de Bivort, B. L. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/797126 · Cited by 22 · see citing works
“Handed locomotor biases at the individual level have been found to be stable over time in numerous species including humans (Lebovich et al., 2019) and flies (Ayroles et al., 2015; Buchanan et al., 2015; Linneweber et al., 2019).”
BackgroundMethodInfluentialSelf-citationComplex dynamics and the development of behavioural individuality
Fisher, D. N., Brachmann, M., & Burant, J. (2018) · doi:10.1016/j.anbehav.2018.02.015 · Cited by 20
“Groothuis and Trillmich (2011) point out both how similar genetic information can lead to different behaviours (e.g., Ayroles et al., 2015), while different genes can produce the same behaviours through canalisation (Siegal & Bergman, 2002).”
BackgroundThalamic Regulation of a Visual Critical Period and Motor Behavior
Hageter, J., Starkey, J., & Horstick, E. J. (2022) · Cell Reports · doi:10.1016/j.celrep.2023.112287 · Cited by 26 · see citing works
“96,97 Alternatively, in our CP assay, the “occluded” eye likely receives some visual input.”
BackgroundHussain, W., Campbell, M. T., Jarquín, D., Walia, H., & Morota, G. (2020) · The Plant Genome · doi:10.1002/tpg2.20011 · Cited by 20 · see citing works
“…associated with diverse phenotypes, including the tendency to left-right turning and bristles (Mackay and Lyman, 2005) and locomotor handedness (Ayroles et al., 2015) in Drosophila; coat color (Nachman et al., 2003), circadian activity, and exploratory behavior (Corty et al., 2018) in mice;…”
BackgroundNegron, Y. L. S., Hansen, N. F., & Harbison, S. T. (2018) · G3 Genes Genomes Genetics · doi:10.1534/g3.118.200503 · Cited by 19 · see citing works
Collective Behavior: Social Digging in Drosophila Larvae.
Louis, M., & de Polavieja, G. D. (2017) · Current Biology · doi:10.1016/j.cub.2017.08.023 · Cited by 19
“Adult flies have different ‘personalities’ [17] and the same level of idiosyncrasy is expected for larvae.”
BackgroundNeuromodulation and Individuality
Maloney, R. T. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.777873 · Cited by 23 · see citing works
Genotype Influences Day-to-Day Variability in Sleep in Drosophila melanogaster
Wu, K. J., Kumar, S., Negron, Y. L. S., & Harbison, S. T. (2018) · Sleep · doi:10.1093/sleep/zsx205 · Cited by 16 · see citing works
Wei, W., Bowes, J., Plant, D., Viatte, S., Yarwood, A., Massey, J., Worthington, J., & Eyre, S. (2016) · Scientific Reports · doi:10.1038/srep25014 · Cited by 17 · see citing works
Cleal, M., Fontana, B. D., Hillman, C., & Parker, M. O. (2023) · Behavioural Processes · doi:10.1016/j.beproc.2023.104943 · Cited by 15 · see citing works
Krams, I. A., Krama, T., Krams, R., Trakimas, G., Popovs, S., Jõers, P., Munkevics, M., Elferts, D., Rantala, M. J., Makņa, J., et al. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.659331 · Cited by 24 · see citing works
“A genetic basis for variability has been found in several other Drosophila behaviors including locomotor bias (Ayroles et al., 2015) and odor preference (Honegger et al.”
BackgroundQTL Mapping on a Background of Variance Heterogeneity
Corty, R., & Valdar, W. (2018) · G3: Genes, Genomes, Genetics · doi:10.1534/g3.118.200790 · Cited by 15
The study of animal behaviour as a physical science
Brown, A. E. X., & de Bivort, B. (2017) · bioRxiv · doi:10.1101/220855 · Cited by 15
“As an example, tracking the centroids of many flies in parallel exploring simple arenas has permitted the measurement of individual behaviour from tens of thousands of individuals across hours and days 36,37 .”
A neurodevelopmental origin of behavioral individuality
Linneweber, G., Andriatsilavo, M., Dutta, S., Hellbruegge, L., Liu, G., Ejsmont, R., Fenk, L., Straw, A., Wernet, M. F., Hiesinger, P., et al. (2019) · bioRxiv · doi:10.1101/540880 · Cited by 14
Cross-species Analyses of Intra-species Behavioral Differences in Mammals and Fish
Demin, K. A., Lakstygal, A. M., Volgin, A. D., de Abreu, M. S., Genário, R., Alpyshov, E. T., Serikuly, N., Wang, D., Wang, J., Yan, D., et al. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2019.12.035 · Cited by 14 · see citing works
“4 Common in various species, individual behavioral differences [39-44] are often affected by age, sex, size, social status and learned adaptive strategies [19, 45, 46].”
BackgroundCorty, R., Kumar, V., Tarantino, L., Takahashi, J., & Valdar, W. (2018) · G3: Genes, Genomes, Genetics · doi:10.1534/g3.118.200194 · Cited by 13 · see citing works
The Novel Concept of "Behavioural Instability" and Its Potential Applications
Pertoldi, C., Bahrndorff, S., Novicic, Z. K., & Rohde, P. D. (2016) · Symmetry · doi:10.3390/sym8110135 · Cited by 13
“Similarly, several genome-wide association studies (GWAS) studies are trying to associate genetic variation with variation in behavioral traits [35].”
BackgroundRohde, P. D., Madsen, L. S., Arvidson, S. M. N., Loeschcke, V., Demontis, D., & Kristensen, T. (2016) · Fly · doi:10.1080/19336934.2016.1158365 · Cited by 13 · see citing works
“, intragenotypic, such variation does exist.(17,18) The Y-maze assay”
BackgroundMultimodal cue integration and learning in a neural representation of head direction
Basnak, M. A., Kutschireiter, A., Okubo, T. S., Chen, A., Gorelik, P., Drugowitsch, J., & Wilson, R. I. (2025) · Nature Neuroscience · doi:10.1038/s41593-024-01823-z · Cited by 13 · see citing works
Variation and Variability in Drosophila Grooming Behavior
Mueller, J. M., Zhang, N., Carlson, J., & Simpson, J. (2020) · bioRxiv · doi:10.1101/2020.08.15.252627 · Cited by 12
Genetic variants and underlying mechanisms influencing variance heterogeneity in maize.
Li, H., Wang, M., Li, W.-J., He, L., Zhou, Y., Zhu, J.-T., Che, R., Warburton, M., Yang, X.-H., & Yan, J.-B. (2020) · The Plant Journal · doi:10.1111/tpj.14786 · Cited by 12
“The last two could contribute to genetic variance heterogeneity as described in previous literatures (Shen et al., 2012, Ayroles et al., 2015, Ek et al., 2018).”
BackgroundanTraX: high throughput video tracking of color-tagged insects
Gal, A., Saragosti, J., & Kronauer, D. (2020) · bioRxiv · doi:10.1101/2020.04.29.068478 · Cited by 12
“Such experiments are of increasing interest, as the study of behavior in classical model systems like Drosophila fruit flies is shifting toward understanding more complex behavioral phenomena such as social interactions, individuality and interspecies interactions [12,42–46].”
Backgroundvqtl: An R Package for Mean-Variance QTL Mapping
Corty, R., & Valdar, W. (2017) · G3: Genes, Genomes, Genetics · doi:10.1101/149377 · Cited by 12
“Nonetheless, although detection of vQTL has started to enter the main-stream of genetic analysis (Yang et al. 2012; Hulse and Cai 2013; Ayroles et al. 2015; Forsberg et al. 2015; Wei et al. 2016; Wang and Payseur 2017; Wei et al. 2017), statistical tools for this purpose remain heterogeneous.”
BackgroundShedding Light on Inter-Individual Variability of Olfactory Circuits in Drosophila
Rihani, K., & Sachse, S. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.835680 · Cited by 16 · see citing works
“, 2020), while the degree of variability in locomotor handedness is itself genetically determined and thus heritable (Ayroles et al., 2015; Buchanan et al., 2015).”
BackgroundWild flies hedge their thermal preference bets in response to seasonal fluctuations
Akhund-Zade, J., Yoon, D., Bangerter, A., Polizos, N. T., Campbell, M., Soloshenko, A., Zhang, T., Wice, E., Albright, A., Narayanan, A. K., et al. (2020) · bioRxiv · doi:10.1101/2020.09.16.300731 · Cited by 10
Self-citationAnimal Behavior: A Neural Basis of Individuality.
Takagi, S., & Benton, R. (2020) · Current Biology · doi:10.1016/j.cub.2020.04.052 · Cited by 10 · see citing works
Genetics of Genome-Wide Recombination Rate Evolution in Mice from an Isolated Island
Wang, R. J., & Payseur, B. A. (2017) · Genetics · doi:10.1534/genetics.117.202382 · Cited by 11 · see citing works
Genetic architecture of natural variation of cardiac performance from flies to humans
Saha, S., Spinelli, L., Castro-Mondragon, J., Kervadec, A., Lynott, M., Kremmer, L., Röder, L., Krifa, S., Torres, M., Brun, C., et al. (2021) · bioRxiv · doi:10.1101/2021.06.08.447524 · Cited by 9
Petrazzini, M. E. M., Pecunioso, A., Dadda, M., & Agrillo, C. (2020) · Symmetry · doi:10.3390/sym12081294 · Cited by 9
Zhang, W.-Y., Reeves, G., & Tautz, D. (2019) · Molecular Ecology · doi:10.1111/mec.15341 · Cited by 9
“Given the relatively small number of DGRP lines (n = 198 in our study), false positive or negative discovery associations may exist from our GWA and LD analysis, while still identifying candidate genes for further experimental follow-up (Ayroles et al., 2015; Turner & Miller, 2012).”
BackgroundGenetic control of variability in subcortical and intracranial volumes
Córdova‐Palomera, A., van der Meer, D., Kaufmann, T., Bettella, F., Wang, Y., Alnæs, D., Doan, N. T., Agartz, I., Bertolino, A., Buitelaar, J. K., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-0664-1 · Cited by 17 · see citing works
Kielland, Ø. N., Bech, C., & Einum, S. (2017) · Ecology and Evolution · doi:10.1002/ece3.3556 · Cited by 9
“…our results, multiple studies show heritability in within- genotype phenotypic variation or demonstrate that evolution of DI is indeed plausible (Ayroles et al., 2015; Breno, Bots, & Van Dongen, 2013; Carter & Houle, 2011; Hansen et al., 2006; Leamy, 1997; Pélabon et al., 2010; Polak & Starmer,…”
ResultA Bayesian test to identify variance effectsPreprint
Dumitrascu, B., Darnell, G., Ayroles, J. F., & Engelhardt, B. E. (2015) · arXiv (Cornell University) · doi:10.48550/arxiv.1512.01616 · Cited by 6 · see citing works
“These studies include diverse quantitative phenotypes, including left-right turning tendency in the fruit fly Drosophila melanogaster [6], coat color in the rock pocket mice Chaetodipus intermedius [8], and thermotolerance [9] and flowering time [10] in the plant Arabidopsis thaliana.”
BackgroundMethodSelf-citationA predisposed motor bias shapes individuality in vocal learning
Toji, N., Sawai, A., Wang, H., Ji, Y., Sugioka, R., Go, Y., & Wada, K. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2308837121 · Cited by 7 · see citing works
A reductionist paradigm for high-throughput behavioural fingerprinting in Drosophila melanogaster
Jones, H., Willis, J. A., Firth, L. C., Giachello, C. N., & Gilestro, G. F. (2023) · eLife · doi:10.7554/elife.86695 · Cited by 8 · see citing works
“…in part compatible with high-throughput approaches ( Wiltschko et al., 2020 ), especially when employed on small invertebrate animal models ( McDermott-Rouse et al., 2021 ; Ayroles et al., 2015 ; Branson et al., 2009 ; Kabra et al., 2013 ) or when aided by robotic handling ( Alisch et al., 2018 ).”
Background
- Authors
- Ayroles, J. F., Buchanan, S. M., O’Leary, C., Skutt-Kakaria, K., Grenier, J. K., Clark, A. G., Hartl, D. L., & de Bivort, B. L.
- Affiliations
- Harvard University (US)
- Cornell University (US)
- Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138;
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2015-05-07
- Volume
- 112
- Issue
- 21
- Pages
- 6706-6711
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4450409
- OpenAlex
- W2112316313
- Cited by
- 218
- References
- 54
- Citations by year
- 2026: 22 · 2025: 22 · 2024: 20 · 2023: 20 · 2022: 18 · 2021: 20 · 2020: 22 · 2019: 13 · 2018: 24 · 2017: 15 · 2016: 14 · 2015: 8
- FWCI
- 9.49
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- arXiv (Cornell University) (submittedVersion)
- arXiv (Cornell University) (cc-by)
- Funders
- Division of Intramural Research, National Institute of Allergy and Infectious Diseases (AI064950)
- Society of Fellows, Harvard University (N/A)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Hemispheric Asymmetry in Neuroscience
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
- Keywords
- phenotypic variability, central complex, brain gene expression, genotype-phenotype correlation, alternative alleles
- MeSH terms
- Animals, Behavior, Animal, Brain, Drosophila melanogaster, Female, Inbreeding, Locomotion, Male, Phenotype, Receptors, Cell Surface, Genetic Variation, Genes, Insect, Drosophila Proteins, Animals, Genetically Modified, RNA Interference, Quantitative Trait Loci, Genome-Wide Association Study, Gene Knockdown Techniques
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