144
Views
0
CrossRef citations to date
0
Altmetric
Review Articles

Learning to collaborate: bringing together behavior and quantitative genomics

ORCID Icon, ORCID Icon & ORCID Icon
Pages 28-35 | Received 25 Oct 2019, Accepted 25 Dec 2019, Published online: 10 Jan 2020

References

  • Anreiter, I., & Sokolowski, M.B. (2019). The foraging gene and its behavioral effects: Pleiotropy and plasticity. Annual Review of Genetics, 53, 373–392. doi:10.1146/annurev-genet-112618-043536
  • Aylor, D.L., Valdar, W., Foulds-Mathes, W., Buus, R.J., Verdugo, R.A., Baric, R.S., … Churchill, G.A. (2011). Genetic analysis of complex traits in the emerging Collaborative Cross. Genome Research, 21, 1213–1222. doi:10.1101/gr.111310.110
  • Baldwin-Brown, J.G., Long, A.D., & Thornton, K.R. (2014). The power to detect quantitative trait loci using resequenced, experimentally evolved populations of diploid, sexual organisms. Molecular Biology and Evolution, 31, 1040–1055. doi:10.1093/molbev/msu048
  • Bauzer, L.G.S.R., Souza, N.A., Ward, R.D., Kyriacou, C.P., & Peixoto, A.A. (2002). The period gene and genetic differentiation between three Brazilian populations of Lutzomyia longipalpis. Insect Molecular Biology, 11, 315–323. doi:10.1046/j.1365-2583.2002.00340.x
  • Boyle, E.A., Li, Y.I., & Pritchard, J.K. (2017). An expanded view of complex traits: from polygenic to omnigenic. Cell, 169, 1177–1186. doi:10.1016/j.cell.2017.05.038
  • Busto, G.U., Cervantes-Sandoval, I., & Davis, R.L. (2010). Olfactory learning in Drosophila. Physiology, 25, 338–346. doi:10.1152/physiol.00026.2010
  • de Koning, D.-J., & McIntyre, L.M. (2017). Back to the future: Multiparent populations provide the key to unlocking the genetic basis of complex traits. Genetics, 206, 527–529. doi:10.1534/genetics.117.203265
  • De Souza, C.P.C., Hashmi, S.B., Horn, K.P., & Osmani, S.A. (2006). A point mutation in the Aspergillus nidulans sonBNup98 nuclear pore complex gene causes conditional DNA damage sensitivity. Genetics, 174, 1881–1893. doi:10.1534/genetics.106.063438
  • Dolan, M.-J., Frechter, S., Bates, A.S., Dan, C., Huoviala, P., Roberts, R.J., … Jefferis, G.S. (2019). Neurogenetic dissection of the Drosophila lateral horn reveals major outputs, diverse behavioural functions, and interactions with the mushroom body. ELife, 8, 1–45. doi:10.7554/eLife.43079
  • Dudai, Y., Jan, Y.N., Byers, D., Quinn, W.G., & Benzer, S. (1976). Dunce, a mutant of Drosophila deficient in learning. Proceedings of the National Academy of Sciences of the United States of America, 73, 1684–1688. doi:10.1073/pnas.73.5.1684
  • Dudai, Y., & Zvi, S. (1985). Multiple defects in the activity of adenylate cyclase from the Drosophila memory mutant rutabaga. Journal of Neurochemistry, 45, 355–364. doi:10.1111/j.1471-4159.1985.tb03996.x
  • Ekman, F.K., Ojala, D.S., Adil, M.M., Lopez, P.A., Schaffer, D.V., & Gaj, T. (2019). CRISPR-Cas9-mediated genome editing increases lifespan and improves motor deficits in a huntington’s disease mouse model. Molecular Therapy. Nucleic Acids, 17, 829–839. doi:10.1016/j.omtn.2019.07.009
  • Galton, F. (1875). The history of twins, as a criterion of the relative powers of nature and nurture. Fraser’s Magazine, 12, 566–576.
  • Garland, T., & Kelly, S.A. (2006). Phenotypic plasticity and experimental evolution. The Journal of Experimental Biology, 209, 2344–2361. doi:10.1242/jeb.02244
  • Garrity, P.A., Goodman, M.B., Samuel, A.D., & Sengupta, P. (2010). Running hot and cold: behavioral strategies, neural circuits, and the molecular machinery for thermotaxis in C. elegans and Drosophila. Genes & Development, 24, 2365–2382. doi:10.1101/gad.1953710
  • Gasparis, S., Przyborowski, M., Kała, M., & Nadolska-Orczyk, A. (2019). Knockout of the HvCKX1 or HvCKX3 Gene in Barley (Hordeum vulgare L.) by RNA-Guided Cas9 Nuclease affects the regulation of cytokinin metabolism and root morphology. Cells, 8, pii:E782. doi:10.3390/cells8080782
  • Gervasi, N., Tchénio, P., & Preat, T. (2010). PKA dynamics in a Drosophila learning center: coincidence detection by rutabaga adenylyl cyclase and spatial regulation by dunce phosphodiesterase. Neuron, 65, 516–529. doi:10.1016/j.neuron.2010.01.014
  • Gnan, S., Priest, A., & Kover, P.X. (2014). The genetic basis of natural variation in seed size and seed number and their trade-off using Arabidopsis thaliana MAGIC lines. Genetics, 198, 1751–1758. doi:10.1534/genetics.114.170746
  • Godenschwege, T.A., Reisch, D., Diegelmann, S., Eberle, K., Funk, N., Heisenberg, M., … Buchner, E. (2004). Flies lacking all synapsins are unexpectedly healthy but are impaired in complex behaviour. The European Journal of Neuroscience, 20, 611–622. doi:10.1111/j.1460-9568.2004.03527.x
  • Han, P.L., Levin, L.R., Reed, R.R., & Davis, R.L. (1992). Preferential expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects. Neuron, 9, 619–627. doi:10.1016/0896-6273(92)90026-A
  • Hige, T., Aso, Y., Modi, M.N., Rubin, G.M., & Turner, G.C. (2015). Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila. Neuron, 88, 985–998. doi:10.1016/j.neuron.2015.11.003
  • Highfill, C.A., Reeves, G.A., & Macdonald, S.J. (2016). Genetic analysis of variation in lifespan using a multiparental advanced intercross Drosophila mapping population. BMC Genetics, 17, 113. doi:10.1186/s12863-016-0419-9
  • Hoppe, P.E., Chau, J., Flanagan, K.A., Reedy, A.R., & Schriefer, L.A. (2010). Caenorhabditis elegans unc-82 encodes a serine/threonine kinase important for myosin filament organization in muscle during growth. Genetics, 184, 79–90. doi:10.1534/genetics.109.110189
  • Howell, G.R., Shindo, M., Murray, S., Gridley, T., Wilson, L.A., & Schimenti, J.C. (2007). Mutation of a ubiquitously expressed mouse transmembrane protein (Tapt1) causes specific skeletal homeotic transformations. Genetics, 175, 699–707. doi:10.1534/genetics.106.065177
  • Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., & Charpentier, E. (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337, 816–821. doi:10.1126/science.1225829
  • Kahsai, L., & Zars, T. (2011). Learning and memory in Drosophila: Behavior, genetics, and neural systems. In N. Atkinson (Ed.), International Review of Neurobiology (Vol. 99, pp. 139–167). Cambridge, MA: Academic Press.
  • Keele, G.R., Crouse, W.L., Kelada, S.N.P., & Valdar, W. (2019). Determinants of QTL mapping power in the realized collaborative cross. G3 (Bethesda), 9, 1707–1727. doi:10.1534/g3.119.400194
  • King, E.G., Macdonald, S.J., & Long, A.D. (2012). Properties and power of the Drosophila synthetic population resource for the routine dissection of complex traits. Genetics, 191, 935–949. doi:10.1534/genetics.112.138537
  • King, E.G., Merkes, C.M., McNeil, C.L., Hoofer, S.R., Sen, S., Broman, K.W., … Macdonald, S.J. (2012). Genetic dissection of a model complex trait using the Drosophila synthetic population resource. Genome Research, 22, 1558–1566. doi:10.1101/gr.134031.111
  • King, E.G., Sanderson, B.J., McNeil, C.L., Long, A.D., & Macdonald, S.J. (2014). Genetic dissection of the Drosophila melanogaster female head transcriptome reveals widespread allelic heterogeneity. PLoS Genetics, 10, e1004322. doi:10.1371/journal.pgen.1004322
  • Kitamoto, T. (2001). Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. Journal of Neurobiology, 47, 81–92. doi:10.1002/neu.1018
  • Kofler, R., & Schlotterer, C. (2014). A guide for the design of evolve and resequencing studies. Molecular Biology and Evolution, 31, 474–483. doi:10.1093/molbev/mst221
  • König, C., Khalili, A., Niewalda, T., Gao, S., & Gerber, B. (2019). An optogenetic analogue of second-order reinforcement in Drosophila. Biology Letters, 15, 20190084. doi:10.1098/rsbl.2019.0084
  • Krashes, M.J., & Waddell, S. (2008). Rapid consolidation to a radish and protein synthesis-dependent long-term memory after single-session appetitive olfactory conditioning in Drosophila. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 28, 3103–3113. doi:10.1523/JNEUROSCI.5333-07.2008
  • LaFerriere, H., Guarnieri, D.J., Sitaraman, D., Diegelmann, S., Heberlein, U., & Zars, T. (2008). Genetic dissociation of ethanol sensitivity and memory formation in Drosophila melanogaster. Genetics, 178, 1895–1902. doi:10.1534/genetics.107.084582
  • LaFerriere, H., Ostrowski, D., Guarnieri, D.J., & Zars, T. (2011). The arouser EPS8L3 gene is critical for normal memory in Drosophila. PloS One, 6, e22867doi:10.1371/journal.pone.0022867
  • LaFerriere, H., Speichinger, K., Stromhaug, A., & Zars, T. (2011). The radish gene reveals a memory component with variable temporal properties. PloS One, 6, e24557. doi:10.1371/journal.pone.0024557
  • Lentsch, E., Li, L., Pfeffer, S., Ekici, A.B., Taher, L., Pilarsky, C., & Grützmann, R. (2019). CRISPR/Cas9-Mediated Knock-Out of KrasG12D Mutated Pancreatic Cancer Cell Lines. International Journal of Molecular Sciences, 20, 5706. doi:10.3390/ijms20225706
  • Lesuisse, E., Knight, S.A.B., Courel, M., Santos, R., Camadro, J.-M., & Dancis, A. (2005). Genome-wide screen for genes with effects on distinct iron uptake activities in Saccharomyces cerevisiae. Genetics, 169, 107–122. doi:10.1534/genetics.104.035873
  • Levin, L.R., Han, P.-L., Hwang, P.M., Feinstein, P.G., Davis, R.L., & Reed, R.R. (1992). The Drosophila learning and memory gene rutabaga encodes a Ca2 + calmodulin-responsive adenylyl cyclase. Cell, 68, 479–489. doi:10.1016/0092-8674(92)90185-F
  • Liu, Y., Ramos-Womack, M., Han, C., Reilly, P., Brackett, K.L., Rogers, W., … Rebeiz, M. (2019). Changes throughout a genetic network mask the contribution of hox gene evolution. Current Biology: CB, 29, 2157–2166.e6. doi:10.1016/j.cub.2019.05.074
  • Livingstone, M.S., Sziber, P.P., & Quinn, W.G. (1984). Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant. Cell, 37, 205–215. doi:10.1016/0092-8674(84)90316-7
  • Lofdahl, K.L., Holliday, M., & Hirsch, J. (1992). Selection for conditionability in Drosophila melanogaster. Journal of Comparative Psychology, 106, 172–183. doi:10.1037//0735-7036.106.2.172
  • Long, A.D., & Langley, C.H. (1999). The power of association studies to detect the contribution of candidate genetic loci to variation in complex traits. Genome Research, 9, 720–731.
  • Mackay, T.F.C. (2001). The genetic architecture of quantitative traits. Annual Review of Genetics, 35, 303–339. doi:10.1146/annurev.genet.35.102401.090633
  • Manolio, T.A., Collins, F.S., Cox, N.J., Goldstein, D.B., Hindorff, L.A., Hunter, D.J., … Visscher, P.M. (2009). Finding the missing heritability of complex diseases. Nature, 461, 747–753. doi:10.1038/nature08494
  • Marella, S., Fischler, W., Kong, P., Asgarian, S., Rueckert, E., & Scott, K. (2006). Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron, 49, 285–295. doi:10.1016/j.neuron.2005.11.037
  • McGuire, S.E., Roman, G., & Davis, R.L. (2004). Gene expression systems in Drosophila: a synthesis of time and space. Trends Genet, 20, 384–391. doi:10.1016/j.tig.2004.06.012
  • McGuire, T.R., & Hirsch, J. (1977). Behavior-genetic analysis of Phormia regina: conditioning, reliable individual differences, and selection. Proceedings of the National Academy of Sciences of the United States of America, 74, 5193–5197. doi:10.1073/pnas.74.11.5193
  • Mery, F., Belay, A.T., So, A.K.-C., Sokolowski, M.B., & Kawecki, T.J. (2007). Natural polymorphism affecting learning and memory in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 104, 13051–13055. doi:10.1073/pnas.0702923104
  • Mery, F., Pont, J., Preat, T., & Kawecki, T.J. (2007). Experimental evolution of olfactory memory in Drosophila melanogaster. Physiological and Biochemical Zoology: PBZ, 80, 399–405. doi:10.1086/518014
  • Ostrowski, D., Kahsai, L., Kramer, E.F., Knutson, P., & Zars, T. (2015). Place memory retention in Drosophila. Neurobiology of Learning and Memory, 123, 217–224. doi:10.1016/j.nlm.2015.06.015
  • Owald, D., Lin, S., & Waddell, S. (2015). Light, heat, action: neural control of fruit fly behaviour. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 370, 20140211. doi:10.1098/rstb.2014.0211
  • Papassotiropoulos, A., Henke, K., Stefanova, E., Aerni, A., Müller, A., Demougin, P., … de Quervain, D.J.-F. (2011). A genome-wide survey of human short-term memory. Molecular Psychiatry, 16, 184–192. doi:10.1038/mp.2009.133
  • Pascual, A., & Préat, T. (2001). Localization of long-term memory within the Drosophila mushroom body. Science, 294, 1115–1117. doi:10.1126/science.1064200
  • Pearce, J.M. (2008). Animal Learning & Cognition: An Introduction. London: Psychology Press.
  • Perrimon, N., Ni, J.-Q., & Perkins, L. (2010). In vivo RNAi: today and tomorrow. Cold Spring Harbor Perspectives in Biology, 2, a003640. doi:10.1101/cshperspect.a003640
  • Pfeiffer, B.D., Ngo, T.-T.B., Hibbard, K.L., Murphy, C., Jenett, A., Truman, J.W., & Rubin, G.M. (2010). Refinement of tools for targeted gene expression in Drosophila. Genetics, 186, 735–755. doi:10.1534/genetics.110.119917
  • Pitman, J.L., DasGupta, S., Krashes, M.J., Leung, B., Perrat, P.N., & Waddell, S. (2009). There are many ways to train a fly. Fly, 3, 3–9. doi:10.4161/fly.3.1.7726
  • Prolo, L.M., Li, A., Owen, S.F., Parker, J.J., Foshay, K., Nitta, R.T., … Grant, G.A. (2019). Targeted genomic CRISPR-Cas9 screen identifies MAP4K4 as essential for glioblastoma invasion. Scientific Reports, 9, 14020. doi:10.1038/s41598-019-50160-w
  • Ran, F.A., Hsu, P.D., Wright, J., Agarwala, V., Scott, D.A., & Zhang, F. (2013). Genome engineering using the CRISPR-Cas9 system. Nature Protocols, 8, 2281–2308. doi:10.1038/nprot.2013.143
  • Rockman, M.V. (2012). The QTN program and the alleles that matter for evolution: all that’s gold does not glitter. International Journal of Organic Evolution, 66, 1–17. doi:10.1111/j.1558-5646.2011.01486.x
  • Schultzhaus, J.N., Saleem, S., Iftikhar, H., & Carney, G.E. (2017). The role of the Drosophila lateral horn in olfactory information processing and behavioral response. Journal of Insect Physiology, 98, 29–37. doi:10.1016/j.jinsphys.2016.11.007
  • Schwaerzel, M., Heisenberg, M., & Zars, T. (2002). Extinction antagonizes olfactory memory at the subcellular level. Neuron, 35, 951–960. doi:10.1016/S0896-6273(02)00832-2
  • Sitaraman, D., Aso, Y., Rubin, G.M., & Nitabach, M.N. (2015). Control of sleep by dopaminergic inputs to the Drosophila mushroom body. Frontiers in Neural Circuits, 9, 73. doi:10.3389/fncir.2015.00084
  • Sitaraman, D., Kramer, E.F., Kahsai, L., Ostrowski, D., & Zars, T. (2017). Discrete serotonin systems mediate memory enhancement and escape latencies after unpredicted aversive experience in Drosophila place memory. Frontiers in Systems Neuroscience, 11, 92. doi:10.3389/fnsys.2017.00092
  • Sitaraman, D., Zars, M., LaFerriere, H., Chen, Y.-C., Sable-Smith, A., Kitamoto, T., … Zars, T. (2008). Serotonin is necessary for place memory in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 105, 5579–5584. doi:10.1073/pnas.0710168105
  • Sitaraman, D., Zars, M., & Zars, T. (2010). Place memory formation in Drosophila is independent of proper octopamine signaling. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 196, 299–305. doi:10.1007/s00359-010-0517-5
  • Slate, J. (2004). Quantitative trait locus mapping in natural populations: progress, caveats and future directions. Molecular Ecology, 14, 363–379. doi:10.1111/j.1365-294X.2004.02378.x
  • Stanley, P.D., Ng’oma, E., O’Day, S., & King, E.G. (2017). Genetic dissection of nutrition-induced plasticity in insulin/insulin-like growth factor signaling and median life span in a Drosophila multiparent population. Genetics, 206, 587–602. doi:10.1534/genetics.116.197780
  • Stern, D.L. (2014). Identification of loci that cause phenotypic variation in diverse species with the reciprocal hemizygosity test. Trends in Genetics: TIG, 30, 547–554. doi:10.1016/j.tig.2014.09.006
  • Tauber, E., Zordan, M., Sandrelli, F., Pegoraro, M., Osterwalder, N., Breda, C., … Costa, R. (2007). Natural selection favors a newly derived timeless allele in drosophila melanogaster. Science, 316, 1895–1898. doi:10.1126/science.1138412
  • Tolman, E.C. (1924). The inheritance of maze-learning ability in rats. Journal of Comparative Psychology, 4, 1–18. doi:10.1037/h0071979
  • Tully, T., & Quinn, W.G. (1985). Classical conditioning and retention in normal and mutant Drosophila melanogaster. Journal of Comparative Physiology A, 157, 263–277. doi:10.1007/BF01350033
  • Tumkaya, T., Ott, S., & Claridge-Chang, A. (2018). A systematic review of Drosophila short-term-memory genetics: Meta-analysis reveals robust reproducibility. Neuroscience and Biobehavioral Reviews, 95, 361–382. doi:10.1016/j.neubiorev.2018.07.016
  • Turner, T.L. (2014). Fine-mapping natural alleles: quantitative complementation to the rescue. Molecular Ecology, 23, 2377–2382. doi:10.1111/mec.12719
  • von Philipsborn, A.C., Liu, T., Yu, J.Y., Masser, C., Bidaye, S.S., & Dickson, B.J. (2011). Neuronal control of Drosophila courtship song. Neuron, 69, 509–522. doi:10.1016/j.neuron.2011.01.011
  • Williams-Simon, P.A., Posey, C., Mitchell, S., Ng’oma, E., Mrkvicka, J.A., … King, E.G. (2019). Multiple genetic loci affect place learning and memory performance in Drosophila melanogaster. Genes, Brain, and Behavior, 18, 708.
  • Wustmann, G., Rein, K., Wolf, R., & Heisenberg, M. (1996). A new paradigm for operant conditioning of Drosophila melanogaster. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology, 179, 429–436. doi:10.1007/bf00194996
  • Yarali, A., & Gerber, B. (2010). A neurogenetic dissociation between punishment-, reward-, and relief-learning in Drosophila. Frontiers in Behavioral Neuroscience, 4, 189. doi:10.3389/fnbeh.2010.00189
  • Zars, T., Fischer, M., Schulz, R., & Heisenberg, M. (2000). Localization of a short-term memory in Drosophila. Science, 288, 672–675. doi:10.1126/science.288.5466.672
  • Zars, T., Wolf, R., Davis, R., & Heisenberg, M. (2000). Tissue-specific expression of a type I adenylyl cyclase rescues the rutabaga mutant memory defect: in search of the engram. Learning & Memory, 7, 18–31. doi:10.1101/lm.7.1.18
  • Zhang, W., Guy Reeves, R., & Tautz, D. (2019). Testing the Omnigenic Model for a Behavioral Trait in Drosophila melanogaster. BioRxiv, doi:10.1101/639955

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.