Stel je voor dat je in een vijver leeft, amper een milimeter groot, zonder ogen die scherp genoeg zijn om een predator te herkennen. Je enige waarschuwing is een zwak chemisch spoor dat door het water drijft: moleculen afgescheiden door een vis ergens in je buurt. Als reactie daarop duik je dieper, mijd je het licht en verander je je manier van zwemmen. Dit is de dagelijkse realiteit van watervlooien, kleine kreeftachtigen die het opmerkelijke vermogen hebben om hun eigen gedrag aan te passen op basis van signalen uit hun omgeving.
Voor mijn thesis onderzocht ik dit flexibele gedrag bij Daphnia magna, een veelvoorkomende watervlosoort in Vlaamse poelen en vijvers. Ik ging na hoe dieren uit 20 verschillende vijvers reageren op chemische signalen die vissen afgeven. Deze signalen waarschuven watervlooien dat er mogelijk predatoren aanwezig zijn.
Van vijver naar videotracking
In totaal testte ik 101 genetisch verschillende klonen van watervlooien op hun reactie op deze vis-signalen. Met een videotracking-opstelling volgde ik hoe de dieren zich door de waterkolom bewogen, hoe diep ze zaten, en hoe snel ze zwommen, in blootgestelde en normale condities.
Wat meteen opviel: watervlooinen uit vijvers zonder vissen vertoonden niet de verwachte reactie. In plaats van dieper te duiken bij het vis-signaal, bewogen ze net vaker omhoog. Dat suggereert dat de populaties uit vispoelen, waar dit gedrag al generaties lang loont, dit verdedigingsmechanisme sterker "onthouden" hebben dan populaties die al lang geen vis meer hebben meegemaakt.
Op zoek naar de genen achter het gedrag
Omdat watervlooien zich ongeslachtelijk kunnen voortplanten en dus klonen van zichzelf maken, zijn ze uitzonderlijk geschikt om te onderzoeken hoe verschillen in DNA, de erfelijke informatie die wordt doorgegeven van ouder op nakomeling, samenhangen met verschillen in gedrag. Elke kloon is genetisch identiek aan zichzelf maar verschilt van de andere klonen, waardoor ik gedrag en genetica netjes naast elkaar kon leggen via een studie via associatie (GWAS)
Een van de sterkste genetische signalen die daaruit naar voren kwam, wijst naar een gen dat betrokken is bij lichtperceptie. Watervlooien hebben een hele reeks van dit soort lichtgevoelige eiwitten (opsines), maar van de meeste weten wetenschappers nog altijd niet precies wat ze doen. Mijn resultaten suggereren dat een van deze eiwitten mee bepaalt of een dier dicht bij het oppervlak blijft, of net dieper de waterkolom in trekt.Dit is een nieuwe aanwijzing van een mogelijke functie van deze eiwitten in Daphnia.
Niet alleen de positie in de waterkolom, maar ook de zwemsnelheid van de dieren bleek onder genetishce controle te staan. Een aparte GWAS-analyse op de verandering in zwemsnelheid na blootstelling aan het vis-signaal wees naar twee andere genetische regio's, elk met eigen kandidaatgenen.
Een netwerk van gene dat samen reageert
Gedrag verandert niet door één gen alleen. Na blootstelling aan het vis-signaal bleken meer dan 700 genen hun activiteit aan te passen. Door deze data te combineren met informatie over welke stukken DNA op dat moment toegankelijk zijn voor regulatie, kon ik een eerste schets maken van het onderliggende genregulatorisch netwerk: welke genen sturen de activiteit van welke andere genen aan?
Daaruit kwamen twee genen naar voren die als een soort knooppunt fungeren, met verbindingen naar tientallen andere gene: een gen uit de FOX-familie (FOXL1/FOXI1/FOXS1) en een Hox-gen (ftz/HOXC13). Beide zijn bekend uit ander onderzoek als belangrijke sturende factoren in ontwikkeling en stressrespons bij andere diersoorten. Deze genen lijken bij Daphnia mogelijk een vergelijkbare rol te spelen in de reactie op predatiegevaar.
Waarom dit ertoe doet
Samen tekenen deze resultaten een beeld van hoe dieren hun gedrag kunnen bijsturen zodra hun omgeving verandert. Dit van het niveau van een enkel gen tot een heel netwerk van genen die samen schakelen. Meer algemeen laat dit onderzoek zien hoe kleine verschillen in genetische achtergrond kunnen bepalen hoe goed een organisme in staat is om op gevaar te reageren. In een wereld waarin leefomgevingen snel veranderen, (door klimaatverandering, door het verdwijnen of verschijnen van predatoren, door menselijke ingerepen in waterlopen, etc.) is precies dat aanpassingsvermogen essentieel om te kunnen overleven.
aaronkiggen/daphnia-ATAC-pipeline. (n.d.). Retrieved June 3, 2026, from https://github.com/aaronkiggen/daphnia-ATAC-pipeline
Balloux, F., Lehmann, L., & De Meeûs, T. (2003). The population genetics of clonal and partially clonal diploids. Genetics, 164(4), 1635–1644. https://doi.org/10.1093/GENETICS/164.4.1635
Barabási, A. L., & Oltvai, Z. N. (2004). Network biology: understanding the cell’s functional organization. Nature Reviews Genetics 2004 5:2, 5(2), 101–113. https://doi.org/10.1038/nrg1272
Barbasch, T. A., Abuwa, V. I., Carswell, B., & Bell, A. M. (2024). Managing the tradeoff between reproduction and survival requires flexibility in behaviour and gene regulation in three-spined stickleback. Proceedings of the Royal Society B: Biological Sciences, 291(2036). https://doi.org/10.1098/rspb.2024.2296
Baudach, A., & Vilcinskas, A. (2021). The European Map Butterfly Araschnia levana as a Model to Study the Molecular Basis and Evolutionary Ecology of Seasonal Polyphenism. Insects, 12(4). https://doi.org/10.3390/INSECTS12040325
Bedrossiantz, J., Fuertes, I., Raldua, D., & Barata, C. (2021). Pharmacological modulation of fish-induced depth selection in D. magna: the role of cholinergic and GABAergic signalling. Scientific Reports 2021 11:1, 11(1), 19407-. https://doi.org/10.1038/s41598-021-98886-w
Beldade, P., Mateus, A. R. A., & Keller, R. A. (2011). Evolution and molecular mechanisms of adaptive developmental plasticity. Molecular Ecology, 20(7), 1347–1363. https://doi.org/10.1111/J.1365-294X.2011.05016.X
Bellot, M., Gómez-Canela, C., & Barata, C. (2022). Phototactic behaviour and neurotransmitter profiles in two Daphnia magna clones: Vertical and horizontal responses to fish kairomones and psychotropic drugs. Science of The Total Environment, 830, 154684. https://doi.org/10.1016/J.SCITOTENV.2022.154684
Bendesky, A., & Bargmann, C. I. (2011). Genetic contributions to behavioural diversity at the gene-environment interface. Nature Reviews. Genetics, 12(12), 809–820. https://doi.org/10.1038/NRG3065
Boeing, W. J., Ramcharan, C. W., & Riessen, H. P. (2006). Multiple predator defence strategies in Daphnia pulex and their relation to native habitat. Journal of Plankton Research, 28(6), 571–584. https://doi.org/10.1093/PLANKT/FBI142
Boersma, M., Spaak, P., & De Meester, L. (1998). Predator-mediated plasticity in morphology, life history, and behavior of Daphnia: the uncoupling of responses. The American Naturalist, 152(2), 237–248. https://doi.org/10.1086/286164
Brandon, C. S., Greenwold, M. J., & Dudycha, J. L. (2017). Ancient and Recent Duplications Support Functional Diversity of Daphnia Opsins. Journal of Molecular Evolution, 84(1), 12–28. https://doi.org/10.1007/S00239-016-9777-1/TABLES/2
Bravo González-Blas, C., De Winter, S., Hulselmans, G., Hecker, N., Matetovici, I., Christiaens, V., Poovathingal, S., Wouters, J., Aibar, S., & Aerts, S. (2023). SCENIC+: single-cell multiomic inference of enhancers and gene regulatory networks. Nature Methods, 20(9), 1355–1367. https://doi.org/10.1038/s41592-023-01938-4
Brewer, M. C., Dawidowicz, P., & Dodson, S. I. (n.d.). Interactive effects of fish kairomone and light on Daphnia escape behavior.
Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y., & Greenleaf, W. J. (2013). Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nature Methods 2013 10:12, 10(12), 1213–1218. https://doi.org/10.1038/nmeth.2688
Buenrostro, J. D., Wu, B., Chang, H. Y., & Greenleaf, W. J. (2015). ATAC-seq: A Method for Assaying Chromatin Accessibility Genome-Wide. Current Protocols in Molecular Biology, 109, 21.29.1-21.29.9. https://doi.org/10.1002/0471142727.MB2129S109
Carrillo, M. P., Piña, B., Vila-Costa, M., & Barata, C. (2025). Molecular mechanisms that regulate scopolamine effects on inducible fish antipredation responses in Daphnia magna. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 289, 110116. https://doi.org/10.1016/J.CBPC.2024.110116
Chang, J., Xu, Y., Fu, Y., Liu, J., Jiang, D., Pan, J., Ouyang, H., Liu, W., Xu, J., Tian, Y., Huang, Y., Ruan, J., & Shen, X. (2024). The dynamic landscape of chromatin accessibility and active regulatory elements in the mediobasal hypothalamus influences the seasonal activation of the reproductive axis in the male quail under long light exposure. BMC Genomics, 25(1), 197. https://doi.org/10.1186/S12864-024-10097-5
Chari, S., & Dworkin, I. (2013). The Conditional Nature of Genetic Interactions: The Consequences of Wild-Type Backgrounds on Mutational Interactions in a Genome-Wide Modifier Screen. PLOS Genetics, 9(8), e1003661. https://doi.org/10.1371/JOURNAL.PGEN.1003661
Chaturvedi, A., Li, X., Dhandapani, V., Marshall, H., Kissane, S., Cuenca-Cambronero, M., Asole, G., Calvet, F., Ruiz-Romero, M., Marangio, P., Guigó, R., Rago, D., Mirbahai, L., Eastwood, N., Colbourne, J. K., Zhou, J., Mallon, E., & Orsini, L. (2023). The hologenome of Daphnia magna reveals possible DNA methylation and microbiome-mediated evolution of the host genome. Nucleic Acids Research, 51(18), 9785–9803. https://doi.org/10.1093/NAR/GKAD685
Chen, Z. L., Meng, J. M., Cao, Y., Yin, J. L., Fang, R. Q., Fan, S. B., Liu, C., Zeng, W. F., Ding, Y. H., Tan, D., Wu, L., Zhou, W. J., Chi, H., Sun, R. X., Dong, M. Q., & He, S. M. (2019). A high-speed search engine pLink 2 with systematic evaluation for proteome-scale identification of cross-linked peptides. Nature Communications 2019 10:1, 10(1), 3404-. https://doi.org/10.1038/s41467-019-11337-z
Chevin, L. M., Leung, C., Le Rouzic, A., & Uller, T. (2022). Using phenotypic plasticity to understand the structure and evolution of the genotype–phenotype map. Genetica, 150(3–4), 209–221. https://doi.org/10.1007/s10709-021-00135-5
Choi, T. J., Han, S. M., Malik, A., & Kim, C. B. (2023). Comparative transcriptome analysis of two Daphnia galeata genotypes displaying contrasting phenotypic variation induced by fish kairomones in the same environment of the Han River, Korea. BMC Genomics, 24(1). https://doi.org/10.1186/S12864-023-09701-X
Colbourne, J. K., Pfrender, M. E., Gilbert, D., Thomas, W. K., Tucker, A., Oakley, T. H., Tokishita, S., Aerts, A., Arnold, G. J., Basu, M. K., Bauer, D. J., Cáceres, C. E., Carmel, L., Casola, C., Choi, J. H., Detter, J. C., Dong, Q., Dusheyko, S., Eads, B. D., … Boore, J. L. (2011). The Ecoresponsive Genome of Daphnia pulex. Science (New York, N.Y.), 331(6017), 555. https://doi.org/10.1126/SCIENCE.1197761
Corces, M. R., Trevino, A. E., Hamilton, E. G., Greenside, P. G., Sinnott-Armstrong, N. A., Vesuna, S., Satpathy, A. T., Rubin, A. J., Montine, K. S., Wu, B., Kathiria, A., Cho, S. W., Mumbach, M. R., Carter, A. C., Kasowski, M., Orloff, L. A., Risca, V. I., Kundaje, A., Khavari, P. A., … Chang, H. Y. (2017). An improved ATAC-seq protocol reduces background and enables interrogation of frozen tissues. Nature Methods, 14(10), 959–962. https://doi.org/10.1038/NMETH.4396
Cousyn, C., De Meester, L., Colbourne, J. K., Brendonck, L., Verschuren, D., & Volckaert, F. (2001). Rapid, local adaptation of zooplankton behavior to changes in predation pressure in the absence of neutral genetic changes. Proceedings of the National Academy of Sciences, 98(11), 6256–6260. https://doi.org/10.1073/pnas.111606798
Craddock, N., Kendler, K., Neale, M., Nurnberger, J., Purcell, S., Rietschel, M., Perlis, R., Santangelo, S. L., Schulze, T., Smoller, J. W., & Thapar, A. (2009). Dissecting the phenotype in genome-wide association studies of psychiatric illness. The British Journal of Psychiatry : The Journal of Mental Science, 195(2), 97. https://doi.org/10.1192/BJP.BP.108.063156
Cresswell, K. A., Tarling, G. A., Thorpe, S. E., Burrows, M. T., Wiedenmann, J., & Mangel, M. (2009). Diel vertical migration of Antarctic krill (Euphausia superba) is flexible during advection across the Scotia Sea. Journal of Plankton Research, 31(10), 1265–1281. https://doi.org/10.1093/PLANKT/FBP062
Crispo, E. (2007). The Baldwin effect and genetic assimilation: Revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. In Evolution (Vol. 61, Number 11, pp. 2469–2479). https://doi.org/10.1111/j.1558-5646.2007.00203.x
De Meester, L. (1993). Genotype, fish-mediated chemicals, and phototactic behavior in Daphnia magna. Ecology, 74(5), 1467. https://kuleuven.e-bronnen.be/login?url=https://www.proquest.com/schola…
De Meester, L. (1996). EVOLUTIONARY POTENTIAL AND LOCAL GENETIC DIFFERENTIATION IN A PHENOTYPICALLY PLASTIC TRAIT OF A CYCLICAL PARTHENOGEN, DAPHNIA MAGNA. Evolution, 50(3), 1293–1298. https://doi.org/10.1111/j.1558-5646.1996.tb02369.x
De Meester, L., & Cousyn, C. (1997). The change in phototactic behaviour of a Daphnia magna clone in the presence of fish kairomones: The effect of exposure time. Hydrobiologia, 360(1), 169–175. https://doi.org/10.1023/A:1003119827390/METRICS
De Meester, L., Dawidowicz, P., & Gool, E. (1999). Ecology and evolution of predator-induced behavior of zooplankton: Depth selection behavior and diel vertical migration. The Ecology and Evolution of Inducible Defences, 160–176.
De Pittà, C., Biscontin, A., Albiero, A., Sales, G., Millino, C., Mazzotta, G. M., Bertolucci, C., & Costa, R. (2013). The Antarctic Krill Euphausia superba Shows Diurnal Cycles of Transcription under Natural Conditions. PLOS ONE, 8(7), e68652. https://doi.org/10.1371/JOURNAL.PONE.0068652
Decaestecker, E., Gaba, S., Raeymaekers, J. A. M., Stoks, R., Van Kerckhoven, L., Ebert, D., & De Meester, L. (2007). Host-parasite “Red Queen” dynamics archived in pond sediment. Nature, 450(7171), 870–873. https://doi.org/10.1038/NATURE06291
Des Marais, D. L., Hernandez, K. M., & Juenger, T. E. (2013). Genotype-by-environment interaction and plasticity: Exploring genomic responses of plants to the abiotic environment. In Annual Review of Ecology, Evolution, and Systematics (Vol. 44, pp. 5–29). Annual Reviews Inc. https://doi.org/10.1146/annurev-ecolsys-110512-135806
Dingemanse, N. J., Kazem, A. J. N., Réale, D., & Wright, J. (2010). Behavioural reaction norms: animal personality meets individual plasticity. Trends in Ecology & Evolution, 25(2), 81–89. https://doi.org/10.1016/J.TREE.2009.07.013
Dodson, S. (1990). Predicting diel vertical migration of zooplankton. Limnology and Oceanography, 35(5), 1195–1200. https://doi.org/10.4319/LO.1990.35.5.1195
Dodson, S. I., Ryan, S., Tollrian, R., & Lampert, W. (1997). Individual swimming behavior of Daphnia: Effects of food, light and container size in four clones. Journal of Plankton Research, 19(10), 1537–1552. https://doi.org/10.1093/PLANKT/19.10.1537
Doe, C. Q., Hiromi, Y., Gehring, W. J., & Goodman, C. S. (1988). Expression and function of the segmentation gene fushi tarazu during Drosophila neurogenesis. Science (New York, N.Y.), 239(4836), 170–175. https://doi.org/10.1126/SCIENCE.2892267
Dölling, R., Becker, D., Hawat, S., Koch, M., Schwarzenberger, A., & Zeis, B. (2016). Adjustments of serine proteases of Daphnia pulex in response to temperature changes. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 194–195, 1–10. https://doi.org/10.1016/J.CBPB.2016.01.001
Donovan, K. W., & Bretscher, A. (2012). Myosin-V is activated by binding secretory cargo and released in coordination with Rab/exocyst function. Developmental Cell, 23(4), 769. https://doi.org/10.1016/J.DEVCEL.2012.09.001
Ebert, D. (2022). Daphnia as a versatile model system in ecology and evolution. EvoDevo 2022 13:1, 13(1), 16-. https://doi.org/10.1186/S13227-022-00199-0
Falconer, D. S. . (1996). Introduction to quantitative genetics. Prentice Hall.
Ferreira, M. S., Alves, P. C., Callahan, C. M., Giska, I., Farelo, L., Jenny, H., Mills, L. S., Hackländer, K., Good, J. M., & Melo-Ferreira, J. (2020). Transcriptomic regulation of seasonal coat color change in hares. Ecology and Evolution, 10(3), 1180. https://doi.org/10.1002/ECE3.5956
Ghalambor, C. K., McKay, J. K., Carroll, S. P., & Reznick, D. N. (2007). Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology, 21(3), 394–407. https://doi.org/10.1111/J.1365-2435.2007.01283.X
Graeve, A., Huster, J., Mayweg, J., Fiedler, R., Plaßmann, J., Görl, D., Keilmann, A., Alev, S., Wahle, P., & Weiss, L. C. (2026). Predator cue detection in Daphnia involves ionotropic receptors IR25a and IR93a. Proceedings of the Royal Society B: Biological Sciences, 293(2070). https://doi.org/10.1098/RSPB.2025.3283
Graeve, A., Ioannidou, I., Reinhard, J., Görl, D. M., Faissner, A., & Weiss, L. (2021). Brain volume increase and neuronal plasticity underly predator-induced morphological defense expression in Daphnia longicephala. Scientific Reports 2021 11:1, 11(1), 12612-. https://doi.org/10.1038/s41598-021-92052-y
Gross, K., Pasinelli, G., & Kunc, H. P. (2010). Behavioral Plasticity Allows Short‐Term Adjustment to a Novel Environment. Https://Doi.Org/10.1086/655428, 176(4), 456–464. https://doi.org/10.1086/655428
Grunau, C., Augusto, R. de C., Rey, O., Cosseau, C., Chaparro, C., Vidal-Dupiol, J., Allienne, J. F., Duval, D., Pinaud, S., Tönges, S., Andriantsoa, R., Luquet, E., Aubret, F., Dia Sow, M., David, P., Thomson, V., Joly, D., Gomes Lima, M., Federico, D., … Minoda, A. (2021). A simple ATAC-seq protocol for population epigenetics. Wellcome Open Research, 5, 121. https://doi.org/10.12688/WELLCOMEOPENRES.15552.2
Gusev, A., Mancuso, N., Won, H., Kousi, M., Finucane, H. K., Reshef, Y., Song, L., Safi, A., McCarroll, S., Neale, B. M., Ophoff, R. A., O’Donovan, M. C., Crawford, G. E., Geschwind, D. H., Katsanis, N., Sullivan, P. F., Pasaniuc, B., & Price, A. L. (2018). Transcriptome-wide association study of schizophrenia and chromatin activity yields mechanistic disease insights. Nature Genetics, 50(4), 538–548. https://doi.org/10.1038/S41588-018-0092-1
Hahn, M., & von Elert, E. (2022). One Kairomone and Multiple Effects in Daphnia Species—5α-Cyprinol Sulfate Induces Morphological Defenses in the Invasive Species Daphnia lumholtzi. Frontiers in Ecology and Evolution, 10, 804521. https://doi.org/10.3389/FEVO.2022.804521/TEXT
Hammond, R. K., Pahl, M. C., Su, C., Cousminer, D. L., Leonard, M. E., Lu, S., Doege, C. A., Wagley, Y., Hodge, K. M., Lasconi, C., Johnson, M. E., Pippin, J. A., Hankenson, K. D., Leibel, R. L., Chesi, A., Wells, A. D., & Grant, S. F. A. (2021). Biological constraints on GWAS SNPs at suggestive significance thresholds reveal additional BMI loci. ELife, 10, 1–19. https://doi.org/10.7554/ELIFE.62206
Hecker, N., Sharma, V., & Hiller, M. (2017). Transition to an Aquatic Habitat Permitted the Repeated Loss of the Pleiotropic KLK8 Gene in Mammals. Genome Biology and Evolution, 9(11), 3179. https://doi.org/10.1093/GBE/EVX239
Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y. C., Laslo, P., Cheng, J. X., Murre, C., Singh, H., & Glass, C. K. (2010). Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Molecular Cell, 38(4), 576–589. https://doi.org/10.1016/J.MOLCEL.2010.05.004
Herman, J. J., & Sultan, S. E. (2011). Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations. Frontiers in Plant Science, 2(DEC). https://doi.org/10.3389/FPLS.2011.00102
Hernández-Plaza, A., Deng, Z., Robledo-Yagüe, F., Szklarczyk, D., von Mering, C., Bork, P., & Huerta-Cepas, J. (2026). eggNOG v7: phylogeny-based orthology predictions and functional annotations. Nucleic Acids Research, 54(D1), D402–D408. https://doi.org/10.1093/NAR/GKAF1249
Herrel, A., Joly, D., & Danchin, E. (2020). Epigenetics in ecology and evolution. Functional Ecology, 34(2), 381–384. https://doi.org/10.1111/1365-2435.13494
Heuschele, J., Ekvall, M. T., Bianco, G., Hylander, S., & Hansson, L. A. (2017). Context-dependent individual behavioral consistency in Daphnia. Ecosphere, 8(2), e01679. https://doi.org/10.1002/ECS2.1679
Hinch, S. G., & Rand, P. S. (2011). Optimal swimming speeds and forward-assisted propulsion: energy-conserving behaviours of upriver-migrating adult salmon. Https://Doi.Org/10.1139/F00-238, 57(12), 2470–2478. https://doi.org/10.1139/F00-238
Hitzemann, R., Bottomly, D., Darakjian, P., Walter, N., Iancu, O., Searles, R., Wilmot, B., & Mcweeney, S. (2013). Genes, behavior and next-generation RNA sequencing. Genes, Brain and Behavior, 12(1), 1–12. https://doi.org/10.1111/gbb.12007
Huang, S. (2009). Reprogramming cell fates: Reconciling rarity with robustness. BioEssays, 31(5), 546–560. https://doi.org/10.1002/bies.200800189
Hutchings, J. A. (2011). Old wine in new bottles: reaction norms in salmonid fishes. Heredity 2011 106:3, 106(3), 421–437. https://doi.org/10.1038/hdy.2010.166
Irschick, D. J., Albertson, R. C., Brennan, P., Podos, J., Johnson, N. A., Patek, S., & Dumont, E. (2013). Evo-devo beyond morphology: From genes to resource use. Trends in Ecology and Evolution, 28(5), 267–273. https://doi.org/10.1016/j.tree.2012.12.004
Janeček, Š., Svensson, B., & MacGregor, E. A. (2013). α-Amylase: an enzyme specificity found in various families of glycoside hydrolases. Cellular and Molecular Life Sciences: CMLS, 71(7), 1149. https://doi.org/10.1007/S00018-013-1388-Z
Jeschke, J. M., Laforsch, C., & Tollrian, R. (2008). Animal Prey Defenses. Encyclopedia of Ecology, Five-Volume Set, 1–5, 189–194. https://doi.org/10.1016/B978-008045405-4.00858-2
Jones, B. M., Rao, V. D., Gernat, T., Jagla, T., Cash-Ahmed, A. C., Rubin, B. E. R., Comi, T. J., Bhogale, S., Husain, S. S., Blatti, C., Middendorf, M., Sinha, S., Chandrasekaran, S., & Robinson, G. E. (2020). Individual differences in honey bee behavior enabled by plasticity in brain gene regulatory networks. ELife, 9, 1–28. https://doi.org/10.7554/ELIFE.62850
Kim, D. H., Lee, B. Y., Kim, H. S., Jeong, C. B., Hwang, D. S., Kim, I. C., & Lee, J. S. (2018). Identification and characterization of homeobox (Hox) genes and conservation of the single Hox cluster (324.6 kb) in the water flea Daphnia magna. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 330(2), 76–82. https://doi.org/10.1002/JEZ.B.22793
Kim, D., Paggi, J. M., Park, C., Bennett, C., & Salzberg, S. L. (2019). Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nature Biotechnology, 37(8), 907–915. https://doi.org/10.1038/S41587-019-0201-4
Klug, A. (1999). Zinc finger peptides for the regulation of gene expression. Journal of Molecular Biology, 293(2), 215–218. https://doi.org/10.1006/JMBI.1999.3007
Korte, A., & Farlow, A. (2013). The advantages and limitations of trait analysis with GWAS: A review. In Plant Methods (Vol. 9, Number 1). https://doi.org/10.1186/1746-4811-9-29
Lafuente, E., Duneau, D., & Beldade, P. (2018). Genetic basis of thermal plasticity variation in Drosophila melanogaster body size. PLOS Genetics, 14(9), e1007686. https://doi.org/10.1371/JOURNAL.PGEN.1007686
Lalejini, A., Ferguson, A. J., Grant, N. A., & Ofria, C. (2021). Adaptive Phenotypic Plasticity Stabilizes Evolution in Fluctuating Environments. Frontiers in Ecology and Evolution | Www.Frontiersin.Org, 1, 715381. https://doi.org/https://doi.org/10.3389/fevo.2021.715381
Landry, L., & Bernatchez, L. (2010). Role of epibenthic resource opportunities in the parallel evolution of lake whitefish species pairs ( Coregonus sp.). Journal of Evolutionary Biology, 23(12), 2602–2613. https://doi.org/10.1111/j.1420-9101.2010.02121.x
Landy, J. A., Oschmann, A., Munch, S. B., & Walsh, M. R. (2020). Ancestral genetic variation in phenotypic plasticity underlies rapid evolutionary changes in resurrected populations of waterfleas. Proceedings of the National Academy of Sciences of the United States of America, 117(51), 32535–32544. https://doi.org/10.1073/PNAS.2006581117/-/DCSUPPLEMENTAL
Langer, S. M., Weiss, L. C., Ekvall, M. T., Bianco, G., Hansson, L., & Tollrian, R. (2019). A three‐dimensional perspective of Daphnia ’s swimming behavior with and without predator cues. Limnology and Oceanography, 64(4), 1515–1525. https://doi.org/10.1002/lno.11132
Lee, B. Y., Choi, B. S., Kim, M. S., Park, J. C., Jeong, C. B., Han, J., & Lee, J. S. (2019). The genome of the freshwater water flea Daphnia magna: A potential use for freshwater molecular ecotoxicology. Aquatic Toxicology, 210, 69–84. https://doi.org/10.1016/J.AQUATOX.2019.02.009
Li, H., & Barrett, J. (2011). A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics, 27(21), 2987–2993. https://doi.org/10.1093/BIOINFORMATICS/BTR509
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., & Durbin, R. (2009). The Sequence Alignment/Map format and SAMtools. Bioinformatics, 25(16), 2078–2079. https://doi.org/10.1093/BIOINFORMATICS/BTP352
Li, Q., Barish, S., Okuwa, S., & Volkan, P. C. (2015). Examination of Endogenous Rotund Expression and Function in Developing Drosophila Olfactory System Using CRISPR-Cas9–Mediated Protein Tagging. G3 Genes|Genomes|Genetics, 5(12), 2809–2816. https://doi.org/10.1534/G3.115.021857
Liao, Y., Smyth, G. K., & Shi, W. (2014). featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics, 30(7), 923–930. https://doi.org/10.1093/BIOINFORMATICS/BTT656
Loose, C. J., & Dawidowicz, P. (1994). Trade-Offs in Diel Vertical Migration by Zooplankton: The Costs of Predator Avoidance. Ecology, 75(8), 2255–2263. https://doi.org/10.2307/1940881
López-Valcárcel, M. E., del Arco, A., Araújo, C. V. M., & Parra, G. (2025). Reduced avoidance behaviour in Daphnia magna due to agrochemical-induced vulnerability. Ecotoxicology and Environmental Safety, 291, 117673. https://doi.org/10.1016/J.ECOENV.2025.117673
Love, M. I., Huber, W., & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15(12), 550-. https://doi.org/10.1186/S13059-014-0550-8/FIGURES/9
Lynch, M., Ye, Z., Urban, L., Maruki, T., & Wei, W. (2022). The Linkage-Disequilibrium and Recombinational Landscape in Daphnia pulex. Genome Biology and Evolution, 14(11). https://doi.org/10.1093/gbe/evac145
Maurano, M. T., Humbert, R., Rynes, E., Thurman, R. E., Haugen, E., Wang, H., Reynolds, A. P., Sandstrom, R., Qu, H., Brody, J., Shafer, A., Neri, F., Lee, K., Kutyavin, T., Stehling-Sun, S., Johnson, A. K., Canfield, T. K., Giste, E., Diegel, M., … Stamatoyannopoulos, J. A. (2012). Systematic localization of common disease-associated variation in regulatory DNA. Science (New York, N.Y.), 337(6099), 1190–1195. https://doi.org/10.1126/SCIENCE.1222794
McManus, J. N. J., Lovelett, R. J., Lowengrub, D., & Christensen, S. (2023). A unifying statistical framework to discover disease genes from GWASs. Cell Genomics, 3(3), 100264. https://doi.org/10.1016/J.XGEN.2023.100264
Min, H., Lee, J. Y., & Kim, M. H. (2013). Hoxc Gene Collinear Expression and Epigenetic Modifications Established during Embryogenesis Are Maintained until after Birth. International Journal of Biological Sciences, 9(9), 960. https://doi.org/10.7150/IJBS.6739
Miyakawa, H., Sato, M., Colbourne, J. K., & Iguchi, T. (2015). Ionotropic Glutamate Receptors Mediate Inducible Defense in the Water Flea Daphnia pulex. PLOS ONE, 10(3), e0121324. https://doi.org/10.1371/JOURNAL.PONE.0121324
Muñoz, J., Chaturvedi, A., De Meester, L., & Weider, L. J. (2016). Characterization of genome-wide SNPs for the water flea Daphnia pulicaria generated by genotyping-by-sequencing (GBS). Scientific Reports, 6(1), 28569. https://doi.org/10.1038/srep28569
Nicolini, F., Martelossi, J., Forni, G., Savojardo, C., Mantovani, B., & Luchetti, A. (2023). Comparative genomics of Hox and ParaHox genes among major lineages of Branchiopoda with emphasis on tadpole shrimps. Frontiers in Ecology and Evolution, 11. https://doi.org/10.3389/fevo.2023.1046960
Nussey, D. H., Wilson, A. J., & Brommer, J. E. (2007). The evolutionary ecology of individual phenotypic plasticity in wild populations. Journal of Evolutionary Biology, 20(3), 831–844. https://doi.org/10.1111/J.1420-9101.2007.01300.X
Oram, E., & Spitze, K. (2013). Depth selection by Daphnia pulex in response to Chaoborus kairomone. Freshwater Biology, 58(2), 409–415. https://doi.org/10.1111/FWB.12069
Orsini, L., Gilbert, D., Podicheti, R., Jansen, M., Brown, J. B., Solari, O. S., Spanier, K. I., Colbourne, J. K., Rush, D., Decaestecker, E., Asselman, J., De Schamphelaere, K. A. C., Ebert, D., Haag, C. R., Kvist, J., Laforsch, C., Petrusek, A., Beckerman, A. P., Little, T. J., … Frilander, M. J. (2016). Daphnia magna transcriptome by RNA-Seq across 12 environmental stressors. Scientific Data 2016 3:1, 3(1), 160030-. https://doi.org/10.1038/sdata.2016.30
Panhwar, W. A., & Mustafa, S. B. (2022). Phenotypic plasticity in grasshoppers and locusts: a review. Asian Journal of Science, Engineering and Technology (AJSET), 1(1), 38–51. https://doi.org/10.47264/idea.ajset/1.1.4
Pauwels, K., Stoks, R., & De Meester, L. (2005). Coping with predator stress: Interclonal differences in induction of heat-shock proteins in the water flea Daphnia magna. Journal of Evolutionary Biology, 18(4), 867–872. https://doi.org/10.1111/j.1420-9101.2005.00890.x
Pigliucci, M. (2005). Evolution of phenotypic plasticity: where are we going now? Trends in Ecology & Evolution, 20(9), 481–486. https://doi.org/10.1016/j.tree.2005.06.001
Pigliucci, M., & Murren, C. J. (2003). EVOLUTION I N T E R N A T I O N A L J O U R N A L O F O R G A N I C E V O L U T I O N PUBLISHED BY THE SOCIETY FOR THE STUDY OF EVOLUTION PERSPECTIVE: GENETIC ASSIMILATION AND A POSSIBLE EVOLUTIONARY PARADOX: CAN MACROEVOLUTION SOMETIMES BE SO FAST AS TO PASS US BY? In Evolution (Vol. 57, Number 7). https://academic.oup.com/evolut/article/57/7/1455/6756153
Pijanowska, J., & Kowalczewski, A. (1997). Predators can induce swarming behaviour and locomotory responses in Daphnia. Freshwater Biology, 37(3), 649–656. https://doi.org/10.1046/j.1365-2427.1997.00192.x
Price, A. L., Zaitlen, N. A., Reich, D., & Patterson, N. (2010). New approaches to population stratification in genome-wide association studies. Nature Reviews. Genetics, 11(7), 459. https://doi.org/10.1038/NRG2813
Price, T. D., Qvarnström, A., & Irwin, D. E. (2003). The role of phenotypic plasticity in driving genetic evolution. In Proceedings of the Royal Society B: Biological Sciences (Vol. 270, Number 1523, pp. 1433–1440). Royal Society. https://doi.org/10.1098/rspb.2003.2372
R Core Team (2025). _R: A Language and Environment for Statistical Computing_. R Foundation for Statistica Computing, Vienna, Austria. https://www.R-project.org/
Randel, N., & Jékely, G. (2016). Phototaxis and the origin of visual eyes. Philosophical Transactions of the Royal Society B: Biological Sciences, 371(1685), 20150042. https://doi.org/10.1098/RSTB.2015.0042
Ringelberg, J. (1999). The photobehaviour of Daphnia spp. as a model to explain diel vertical migration in zooplankton. Biological Reviews, 74(4), 397–423. https://doi.org/10.1111/J.1469-185X.1999.TB00036.X
Robinson, G. E., Grozinger, C. M., & Whitfield, C. W. (2005). Sociogenomics: social life in molecular terms. Nature Reviews. Genetics, 6(4), 257–270. https://doi.org/10.1038/NRG1575
Posit team (2025). RStudio: Integrated Development Environment for R.
Posit Software, PBC, Boston, MA. URL http://www.posit.co/.
Sakamoto, K., Hisatomi, O., Tokunaga, F., & Eguchi, E. (1996). Two Opsins From the Compound Eye of the Crab Hemigrapsus Sanguineus. Journal of Experimental Biology, 199(2), 441–450. https://doi.org/10.1242/JEB.199.2.441
Saltz, J. B., Bell, A. M., Flint, J., Gomulkiewicz, R., Hughes, K. A., & Keagy, J. (2018). Why does the magnitude of genotype-by-environment interaction vary? Ecology and Evolution, 8(12), 6342–6353. https://doi.org/10.1002/ECE3.4128
Schaeper, N. D., Prpic, N.-M., & Wimmer, E. A. (2010). A clustered set of three Sp-family genes is ancestral in the Metazoa: evidence from sequence analysis, protein domain structure, developmental expression patterns and chromosomal location. https://doi.org/10.1186/1471-2148-10-88
Schlichting, C. D., & Pigliucci, M. (1998). Phenotypic evolution : a reaction norm perspective. Sinauer Associates.
Schneider, H. M. (2022). Characterization, costs, cues and future perspectives of phenotypic plasticity. Annals of Botany, 130(2), 131. https://doi.org/10.1093/AOB/MCAC087
Schomburg, C., Janssen, R., & Prpic, N. M. (2022). Phylogenetic analysis of forkhead transcription factors in the Panarthropoda. Development Genes and Evolution, 232(1), 39–48. https://doi.org/10.1007/S00427-022-00686-3/FIGURES/3
Schumpert, C. A., Dudycha, J. L., & Patel, R. C. (2015). Development of an efficient RNA interference method by feeding for the microcrustacean Daphnia. BMC Biotechnology, 15(1). https://doi.org/10.1186/S12896-015-0209-X
Seetharam, A., Bai, Y., & Stuart, G. W. (2010). A survey of well conserved families of C2H2 zinc-finger genes in Daphnia. BMC Genomics, 11(1), 276. https://doi.org/10.1186/1471-2164-11-276
Shackelford, T. K., & Weekes-Shackelford, V. A. (2021). Encyclopedia of Evolutionary Psychological Science. In Encyclopedia of Evolutionary Psychological Science. Springer Science+Business Media. https://doi.org/10.1007/978-3-319-19650-3
Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., & Ideker, T. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Research, 13(11), 2498–2504. https://doi.org/10.1101/GR.1239303
Sih, A., Bell, A., & Johnson, J. C. (2004). Behavioral syndromes: an ecological and evolutionary overview. Trends in Ecology & Evolution, 19(7), 372–378. https://doi.org/10.1016/J.TREE.2004.04.009
Sih, A., Ferrari, M. C. O., & Harris, D. J. (2011). Evolution and behavioural responses to human-induced rapid environmental change. Evolutionary Applications, 4(2), 367–387. https://doi.org/10.1111/J.1752-4571.2010.00166.X
Sinha, S., Jones, B. M., Traniello, I. M., Bukhari, S. A., Halfon, M. S., Hofmann, H. A., Huang, S., Katz, P. S., Keagy, J., Lynch, V. J., Sokolowski, M. B., Stubbs, L. J., Tabe-Bordbar, S., Wolfner, M. F., & Robinson, G. E. (2020). Behavior-related gene regulatory networks: A new level of organization in the brain. Proceedings of the National Academy of Sciences of the United States of America, 117(38), 23270–23279. https://doi.org/10.1073/PNAS.1921625117/ASSET/7C854164-3081-48B9-9E79-E…
Slatkin, M. (2008). Linkage disequilibrium - Understanding the evolutionary past and mapping the medical future. In Nature Reviews Genetics (Vol. 9, Number 6, pp. 477–485). https://doi.org/10.1038/nrg2361
Snell-Rood, E. C. (2013). An overview of the evolutionary causes and consequences of behavioural plasticity. Animal Behaviour, 85(5), 1004–1011. https://doi.org/10.1016/J.ANBEHAV.2012.12.031
Stoks, R., Govaert, L., Pauwels, K., Jansen, B., & De Meester, L. (2016). Resurrecting complexity: The interplay of plasticity and rapid evolution in the multiple trait response to strong changes in predation pressure in the water flea Daphnia magna. Ecology Letters, 19(2), 180–190. https://doi.org/10.1111/ele.12551
Swaegers, J., & Koch, E. L. (2022). Gene expression studies of plastic and evolutionary responses to global warming. In Current Opinion in Insect Science (Vol. 51). Elsevier Inc. https://doi.org/10.1016/j.cois.2022.100918
The MathWorks Inc. (2023). Optimization Toolbox version: 9.14 (R2023a), Natick, Massachusetts: The MathWorks Inc. https://www.mathworks.com
Tollrian, R., & Harvell, C. D. (Eds.). (1999). The Ecology and Evolution of Inducible Defenses. Princeton University Press. https://doi.org/10.2307/j.ctv1ddd1cn
Toyota, K., Miyagawa, S., Ogino, Y., & Iguchi, T. (2016). Microinjection-Based RNA Interference Method in the Water Flea, Daphnia pulex and Daphnia magna. RNA Interference. https://doi.org/10.5772/61485
Traniello, I. M., Bukhari, S. A., Dibaeinia, P., Serrano, G., Avalos, A., Ahmed, A. C., Sankey, A. L., Hernaez, M., Sinha, S., Zhao, S. D., Catchen, J., & Robinson, G. E. (2023). Single-cell dissection of aggression in honeybee colonies. Nature Ecology and Evolution, 7(8), 1232–1244. https://doi.org/10.1038/s41559-023-02090-0
Tuomainen, U., & Candolin, U. (2011). Behavioural responses to human-induced environmental change. Biological Reviews, 86(3), 640–657. https://doi.org/10.1111/j.1469-185X.2010.00164.x
Van Kleunen, M., & Fischer, M. (2005). Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytologist, 166(1), 49–60. https://doi.org/10.1111/J.1469-8137.2004.01296.X
Van Tienderen, P. H., & Koelewijn, H. P. (1994). Selection on reaction norms, genetic correlations and constraints. Genetics Research, 64(2), 115–125. https://doi.org/10.1017/S0016672300032729
Velotta, J. P., & Cheviron, Z. A. (2018). Remodeling Ancestral Phenotypic Plasticity in Local Adaptation: A New Framework to Explore the Role of Genetic Compensation in the Evolution of Homeostasis. Integrative and Comparative Biology, 58(6), 1098–1110. https://doi.org/10.1093/ICB/ICY117
Waddington, C. H. (1942). CANALIZATION OF DEVELOPMENT AND THE INHERITANCE OF ACQUIRED CHARACTERS. Nature 1942 150:3811, 150(3811), 563–565. https://doi.org/10.1038/150563a0
Waddington, C. H. (1952). Selection of the Genetic Basis for an Acquired Character. Nature 1952 169:4302, 169(4302), 625–626. https://doi.org/10.1038/169625b0
Wang, Z., Gerstein, M., & Snyder, M. (2009). RNA-Seq: a revolutionary tool for transcriptomics. Nature Reviews Genetics 2008 10:1, 10(1), 57–63. https://doi.org/10.1038/nrg2484
Weiss, L. C. (2019). Sensory ecology of predator-induced phenotypic plasticity. Frontiers in Behavioral Neuroscience, 12, 427852. https://doi.org/10.3389/FNBEH.2018.00330/XML
Weiss, L. C., Kruppert, S., Laforsch, C., & Tollrian, R. (2012). Chaoborus and Gasterosteus Anti-Predator Responses in Daphnia pulex Are Mediated by Independent Cholinergic and Gabaergic Neuronal Signals. PLOS ONE, 7(5), e36879. https://doi.org/10.1371/JOURNAL.PONE.0036879
West-Eberhard, M. J. (1989). Phenotypic Plasticity and the Origins of Diversity. Annual Review of Ecology and Systematics, 20, 249–278. http://www.jstor.org/stable/2097092
Wund, M. A., Baker, J. A., Clancy, B., Golub, J. L., & Foster, S. A. (2008). A test of the “flexible stem” model of evolution: Ancestral plasticity, genetic accommodation, and morphological divergence in the threespine stickleback radiation. American Naturalist, 172(4), 449–462. https://doi.org/10.1086/590966
Yang, J., Weedon, M. N., Purcell, S., Lettre, G., Estrada, K., Willer, C. J., Smith, A. V., Ingelsson, E., O’Connell, J. R., Mangino, M., Mägi, R., Madden, P. A., Heath, A. C., Nyholt, D. R., Martin, N. G., Montgomery, G. W., Frayling, T. M., Hirschhorn, J. N., McCarthy, M. I., … Visscher, P. M. (2011). Genomic inflation factors under polygenic inheritance. European Journal of Human Genetics 2011 19:7, 19(7), 807–812. https://doi.org/10.1038/ejhg.2011.39
Yu, G., Wang, L. G., Han, Y., & He, Q. Y. (2012). clusterProfiler: an R Package for Comparing Biological Themes Among Gene Clusters. OMICS : A Journal of Integrative Biology, 16(5), 284. https://doi.org/10.1089/OMI.2011.0118
Yuan, W., Zhou, Y., Chen, Y., Liu, X., & Wang, J. (2020). Toxicological effects of microplastics and heavy metals on the Daphnia magna. Science of The Total Environment, 746, 141254. https://doi.org/10.1016/J.SCITOTENV.2020.141254
Zaidi, A. A., & Mathieson, I. (2020). Demographic history mediates the effect of stratification on polygenic scores. ELife, 9, 1–30. https://doi.org/10.7554/ELIFE.61548
Zhou, X., & Stephens, M. (2012). Genome-wide efficient mixed-model analysis for association studies. Nature Genetics, 44(7), 821–824. https://doi.org/10.1038/NG.2310