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Transgenerational plasticity in a zooplankton in response to elevated temperature and parasitism

dc.contributor.authorSun, Syuan-Jyun
dc.contributor.authorDziuba, Marcin K.
dc.contributor.authorJaye, Riley N.
dc.contributor.authorDuffy, Meghan A.
dc.date.accessioned2023-03-03T21:09:09Z
dc.date.available2024-03-03 16:09:08en
dc.date.available2023-03-03T21:09:09Z
dc.date.issued2023-02
dc.identifier.citationSun, Syuan-Jyun ; Dziuba, Marcin K.; Jaye, Riley N.; Duffy, Meghan A. (2023). "Transgenerational plasticity in a zooplankton in response to elevated temperature and parasitism." Ecology and Evolution (2): n/a-n/a.
dc.identifier.issn2045-7758
dc.identifier.issn2045-7758
dc.identifier.urihttps://hdl.handle.net/2027.42/175897
dc.description.abstractOrganisms are increasingly facing multiple stressors, which can simultaneously interact to cause unpredictable impacts compared with a single stressor alone. Recent evidence suggests that phenotypic plasticity can allow for rapid responses to altered environments, including biotic and abiotic stressors, both within a generation and across generations (transgenerational plasticity). Parents can potentially “prime” their offspring to better cope with similar stressors or, alternatively, might produce offspring that are less fit because of energetic constraints. At present, it remains unclear exactly how biotic and abiotic stressors jointly mediate the responses of transgenerational plasticity and whether this plasticity is adaptive. Here, we test the effects of biotic and abiotic environmental changes on within- and transgenerational plasticity using a Daphnia–Metschnikowia zooplankton-fungal parasite system. By exposing parents and their offspring consecutively to the single and combined effects of elevated temperature and parasite infection, we showed that transgenerational plasticity induced by temperature and parasite stress influenced host fecundity and lifespan; offsprings of mothers who were exposed to one of the stressors were better able to tolerate elevated temperature, compared with the offspring of mothers who were exposed to neither or both stressors. Yet, the negative effects caused by parasite infection were much stronger, and this greater reduction in host fitness was not mitigated by transgenerational plasticity. We also showed that elevated temperature led to a lower average immune response, and that the relationship between immune response and lifetime fecundity reversed under elevated temperature: the daughters of exposed mothers showed decreased fecundity with increased hemocyte production at ambient temperature but the opposite relationship at elevated temperature. Together, our results highlight the need to address questions at the interface of multiple stressors and transgenerational plasticity and the importance of considering multiple fitness-associated traits when evaluating the adaptive value of transgenerational plasticity under changing environments.Different environmental stressors, including biotic and abiotic, can interact and cause unpredictable impacts. Yet, it is unclear when transgenerational effects might help or hinder the fitness of the next generation. Our study shows the evidence of stressor-induced transgenerational plasticity, but its adaptive significance depends on the identity and combinations of environmental stressors.
dc.publisherNational Library of Medicine (USA), Center for Biotechnology Information
dc.publisherWiley Periodicals, Inc.
dc.subject.otherhost–parasite interactions
dc.subject.othertransgenerational plasticity
dc.subject.otheradaptation
dc.subject.otherMetschnikowia
dc.subject.otherenvironmental stressors
dc.subject.otherDaphnia
dc.titleTransgenerational plasticity in a zooplankton in response to elevated temperature and parasitism
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelEcology and Evolutionary Biology
dc.subject.hlbtoplevelScience
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/175897/1/ece39767_am.pdf
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/175897/2/ece39767.pdf
dc.identifier.doi10.1002/ece3.9767
dc.identifier.sourceEcology and Evolution
dc.identifier.citedreferenceShocket, M. S., Vergara, D., Sickbert, A. J., Walsman, J. M., Strauss, A. T., Hite, J. L., Duffy, M. A., Cáceres, C. E., & Hall, S. R. ( 2018 ). Parasite rearing and infection temperatures jointly influence disease transmission and shape seasonality of epidemics. Ecology, 99 ( 9 ), 1975 – 1987.
dc.identifier.citedreferenceGarcía, F. C., Bestion, E., Warfield, R., & Yvon-Durochera, G. ( 2018 ). Changes in temperature alter the relationship between biodiversity and ecosystem functioning. Proceedings of the National Academy of Sciences of the United States of America, 115 ( 43 ), 10989 – 10994.
dc.identifier.citedreferenceGwynn, D. M., Callaghan, A., Gorham, J., Walters, K. F. A., & Fellowes, M. D. E. ( 2005 ). Resistance is costly: Trade-offs between immunity, fecundity and survival in the pea aphid. Proceedings of the Royal Society B: Biological Sciences, 272 ( 1574 ), 1803 – 1808. https://doi.org/10.1098/rspb.2005.3089
dc.identifier.citedreferenceRoth, O., & Landis, S. H. ( 2017 ). Trans-generational plasticity in response to immune challenge is constrained by heat stress. Evolutionary Applications, 10 ( 5 ), 514 – 528.
dc.identifier.citedreferenceSalinas, S., & Munch, S. B. ( 2012 ). Thermal legacies: Transgenerational effects of temperature on growth in a vertebrate. Ecology Letters, 15 ( 2 ), 159 – 163.
dc.identifier.citedreferenceSadd, B. M., Kleinlogel, Y., Schmid-Hempel, R., & Schmid-Hempel, P. ( 2005 ). Trans-generational immune priming in a social insect. Biology Letters, 1 ( 4 ), 386 – 388.
dc.identifier.citedreferenceSchäfer, R. B., & Piggott, J. J. ( 2018 ). Advancing understanding and prediction in multiple stressor research through a mechanistic basis for null models. Global Change Biology, 24 ( 5 ), 1817 – 1826. https://doi.org/10.1111/gcb.14073
dc.identifier.citedreferenceSchwenke, R. A., Lazzaro, B. P., & Wolfner, M. F. ( 2016 ). Reproduction–immunity trade-offs in insects. Annual Reviews in Entomology, 61, 239.
dc.identifier.citedreferenceSelbach, C., Barsøe, M., Vogensen, T. K., Samsing, A. B., & Mouritsen, K. N. ( 2020 ). Temperature–parasite interaction: Do trematode infections protect against heat stress? International Journal for Parasitology, 50 ( 14 ), 1189 – 1194.
dc.identifier.citedreferenceShocket, M. S., Magnante, A., Duffy, M. A., Cáceres, C. E., & Hall, S. R. ( 2019 ). Can hot temperatures limit disease transmission? A test of mechanisms in a zooplankton–fungus system. Functional Ecology, 33 ( 10 ), 2017 – 2029. https://doi.org/10.1111/1365-2435.13403
dc.identifier.citedreferenceJackson, M. C., Pawar, S., & Woodward, G. ( 2021 ). The temporal dynamics of multiple stressor effects: From individuals to ecosystems. Trends in Ecology & Evolution, 36 ( 5 ), 402 – 410.
dc.identifier.citedreferenceSimmons, B. I., Blyth, P. S. A., Blanchard, J. L., Clegg, T., Delmas, E., Garnier, A., Griffiths, C. A., Jacob, U., Pennekamp, F., Petchey, O. L., Poisot, T., Webb, T. J., & Beckerman, A. P. ( 2021 ). Refocusing multiple stressor research around the targets and scales of ecological impacts. Nature Ecology & Evolution, 5, 1478 – 1489.
dc.identifier.citedreferenceSinclair, B. J., Ferguson, L. V., Salehipour-Shirazi, G., & Macmillan, H. A. ( 2013 ). Cross-tolerance and cross-talk in the cold: Relating low temperatures to desiccation and immune stress in insects. Integrative and Comparative Biology, 53 ( 4 ), 545 – 556.
dc.identifier.citedreferenceSnell-Rood, E. C., Kobiela, M. E., Sikkink, K. L., & Shephard, A. M. ( 2018 ). Mechanisms of plastic rescue in novel environments. Annual Review of Ecology, Evolution, and Systematics, 49, 331 – 354. https://doi.org/10.1146/annurev-ecolsys-110617-062622
dc.identifier.citedreferenceStewart Merrill, T. E., Hall, S. R., Merrill, L., & Cáceres, C. E. ( 2019 ). Variation in immune defense shapes disease outcomes in laboratory and wild Daphnia. Integrative and Comparative Biology, 59 ( 5 ), 1203 – 1219.
dc.identifier.citedreferenceSun, S. J., Catherall, A. M., Pascoal, S., Jarrett, B. J. M., Miller, S. E., Sheehan, M. J., & Kilner, R. M. ( 2020 ). Rapid local adaptation linked with phenotypic plasticity. Evolution Letters, 4 ( 4 ), 345 – 359. https://doi.org/10.1002/evl3.176
dc.identifier.citedreferenceSun, S. J., Dziuba, M. K., Jaye, R. N., & Duffy, M. A. ( 2022 ). Temperature modifies trait-mediated infection outcomes in a Daphnia -fungal parasite system. Philosophical Transactions of the Royal Society B. https://doi.org/10.1101/2022.06.03.494706v1
dc.identifier.citedreferenceSun, S. J., Dziuba, M. K., Mclntire, K. M., Jaye, R. N., & Duffy, M. A. ( 2022 ). Transgenerational plasticity alters parasite fitness in changing environments. Parasitology, 149 ( 11 ), 1515 – 1520. https://doi.org/10.1017/S0031182022001056
dc.identifier.citedreferenceTessier, A. J., Woodruff, P., & Kellogg, W. K. ( 2002 ). Cryptic trophic cascade along a gradient of lake size. Ecology, 83 ( 5 ), 1263 – 1270.
dc.identifier.citedreferenceTetreau, G., Dhinaut, J., Gourbal, B., & Moret, Y. ( 2019 ). Trans-generational immune priming in invertebrates: Current knowledge and future prospects. Frontiers in Immunology, 10, 1938.
dc.identifier.citedreferenceTherneau, T. ( 2012 ). Coxme: Mixed effects Cox models. R Package Version. p. 2.2-3.
dc.identifier.citedreferenceTran, T. T., Janssens, L., Dinh, K. v., & Stoks, R. ( 2019 ). An adaptive transgenerational effect of warming but not of pesticide exposure determines how a pesticide and warming interact for antipredator behaviour. Environmental Pollution, 245, 307 – 315.
dc.identifier.citedreferenceUller, T. ( 2008 ). Developmental plasticity and the evolution of parental effects. Trends Ecology & Evolution, 23 ( 8 ), 432 – 438.
dc.identifier.citedreferenceVale, P. F., Stjernman, M., & Little, T. J. ( 2008 ). Temperature-dependent costs of parasitism and maintenance of polymorphism under genotype-by-environment interactions. Journal of Evolutionary Biology, 21 ( 5 ), 1418 – 1427.
dc.identifier.citedreferenceVisser, M. E. ( 2008 ). Keeping up with a warming world; assessing the rate of adaptation to climate change. Proceedings of the Royal Society B: Biological Sciences, 275 ( 1635 ), 649 – 659. https://doi.org/10.1098/rspb.2007.0997
dc.identifier.citedreferenceWalsh, M. R., Whittington, D., & Funkhouser, C. ( 2014 ). Thermal transgenerational plasticity in natural populations of Daphnia. Integrative Comparative Biology, 54 ( 5 ), 822 – 829.
dc.identifier.citedreferenceWoolway, R. I., Albergel, C., Frölicher, T. L., & Perroud, M. ( 2022 ). Severe lake heatwaves attributable to human-induced global warming. Geophysical Research Letters, 49 ( 4 ), e2021GL097031. https://doi.org/10.1029/2021GL097031
dc.identifier.citedreferenceZhang, S., Dong, H. G., & Wei, D. Y. ( 2014 ). Temporal patterns of cardiac performance and genes encoding heat shock proteins and metabolic sensors of an intertidal limpet Cellana toreuma during sublethal heat stress. Journal of Thermal Biology, 41 ( 1 ), 31 – 37.
dc.identifier.citedreferenceHall, S. R., Sivars-Becker, L., Becker, C., Duffy, M. A., Tessier, A. J., & Cáceres, C. E. ( 2007 ). Eating yourself sick: Transmission of disease as a function of foraging ecology. Ecology Letters, 10 ( 3 ), 207 – 218.
dc.identifier.citedreferenceHarvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson, A. P., Ostfeld, R. S., & Samuel, M. D. ( 2002 ). Climate warming and disease risks for terrestrial and marine biota. Science, 296 ( 5576 ), 2158 – 2162. https://doi.org/10.1126/science.1063699
dc.identifier.citedreferenceHector, T. E., Sgrò, C. M., & Hall, M. D. ( 2021 ). Temperature and pathogen exposure act independently to drive host phenotypic trajectories. Biology Letters, 17 ( 6 ), 20210072.
dc.identifier.citedreferenceBates, D., Mächler, M., Bolker, B., & Walker, S. ( 2015 ). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67 ( 1 ), 1 – 48.
dc.identifier.citedreferenceBubliy, O. A., Kristensen, T. N., Kellermann, V., & Loeschcke, V. ( 2012 ). Plastic responses to four environmental stresses and cross-resistance in a laboratory population of Drosophila melanogaster. Functional Ecology, 26 ( 1 ), 245 – 253. https://doi.org/10.1111/j.1365-2435.2011.01928.x
dc.identifier.citedreferenceChevin, L. M., & Hoffmann, A. A. ( 2017 ). Evolution of phenotypic plasticity in extreme environments. Philosophical Transactions of the Royal Society B: Biological Sciences, 372 ( 1723 ), 20160138. https://doi.org/10.1098/rstb.2016.0138
dc.identifier.citedreferenceClaar, D. C., & Wood, C. L. ( 2020 ). Pulse heat stress and parasitism in a warming world. Trends in Ecology & Evolution, 35 ( 8 ), 704 – 715.
dc.identifier.citedreferenceClay, P. A., Dhir, K., Rudolf, V. H. W., & Duffy, M. A. ( 2019 ). Within-host priority effects systematically alter pathogen coexistence. The American Naturalist, 193 ( 2 ), 187 – 199. https://doi.org/10.1086/701126
dc.identifier.citedreferenceCohen, J. M., Venesky, M. D., Sauer, E. L., Civitello, D. J., McMahon, T. A., Roznik, E. A., & Rohr, J. R. ( 2017 ). The thermal mismatch hypothesis explains host susceptibility to an emerging infectious disease. Ecology Letters, 20 ( 2 ), 184 – 193. https://doi.org/10.1111/ele.12720
dc.identifier.citedreferenceCurley, J. P., Mashoodh, R., & Champagne, F. A. ( 2011 ). Epigenetics and the origins of paternal effects. Hormones and Behavior, 59 ( 3 ), 306 – 314.
dc.identifier.citedreferencede Laender, F., Rohr, J. R., Ashauer, R., Baird, D. J., Berger, U., Eisenhauer, N., Grimm, V., Hommen, U., Maltby, L., Meliàn, C. J., Pomati, F., Roessink, I., Radchuk, V., & van den Brink, P. J. ( 2016 ). Reintroducing environmental change drivers in biodiversity–ecosystem functioning research. Trends in Ecology & Evolution, 31 ( 12 ), 905 – 915.
dc.identifier.citedreferenceDonelan, S. C., Hellmann, J. K., Bell, A. M., Luttbeg, B., Orrock, J. L., Sheriff, M. J., & Sih, A. ( 2020 ). Transgenerational plasticity in human-altered environments. Trends in Ecology & Evolution, 35 ( 2 ), 115 – 124.
dc.identifier.citedreferenceDonelson, J. M., Salinas, S., Munday, P. L., & Shama, L. N. S. ( 2018 ). Transgenerational plasticity and climate change experiments: Where do we go from here? Global Chang Biology, 24 ( 1 ), 13 – 34. https://doi.org/10.1111/gcb.13903
dc.identifier.citedreferenceEbert, D. ( 2005 ). Ecology, epidemiology, and evolution of parasitism in Daphnia. National Library of Medicine (USA), Center for Biotechnology Information.
dc.identifier.citedreferenceEbert, D., Lipsitch, M., & Mangin, K. L. ( 2000 ). The effect of parasites on host population density and extinction: Experimental epidemiology with Daphnia and six microparasites. The American Naturalist, 156 ( 5 ), 459 – 477.
dc.identifier.citedreferenceForsyth, R. B., Candido, E. P. M., Babich, S. L., & Iwama, G. K. ( 1997 ). Stress protein expression in coho salmon with bacterial kidney disease. Journal of Aquatic Animal Health, 9 ( 1 ), 18 – 25. https://doi.org/10.1577/1548-8667%281997%29009%3C0018%3ASPEICS%3E2.3.CO%3B2
dc.identifier.citedreferenceFox, J., Weisberg, S., Price, B., Adler, D., Bates, D., Baud-Bovy, G., Bolker, B., Ellison, S., Firth, D., Friendly, M., Gorjanc, G., Graves, S., Heiberger, R., Krivitsky, P., Laboissiere, R., Maechler, M., Monette, G., Murdoch, D., Nilsson, H., … R-Core. ( 2021 ). Package “car”. R Foundation for Statistical Computing. https://r-forge.r-project.org/projects/car/
dc.identifier.citedreferenceFox, R. J., Donelson, J. M., Schunter, C., Ravasi, T., & Gaitán-Espitia, J. D. ( 2019 ). Beyond buying time: The role of plasticity in phenotypic adaptation to rapid environmental change. Philosophical Transactions of the Royal Society B: Biological Sciences, 374, 20180174. https://doi.org/10.1098/rstb.2018.0174
dc.identifier.citedreferenceGarbutt, J. S., Scholefield, J. A., Vale, P. F., & Little, T. J. ( 2014 ). Elevated maternal temperature enhances offspring disease resistance in Daphnia magna. Functional Ecology, 28 ( 2 ), 424 – 431. https://doi.org/10.1111/1365-2435.12197
dc.identifier.citedreferenceKielland, N., Bech, C., & Einum, S. ( 2017 ). No evidence for thermal transgenerational plasticity in metabolism when minimizing the potential for confounding effects. Proceedings of the Royal Society B: Biological Sciences, 284 ( 1846 ), 20162494. https://doi.org/10.1098/rspb.2016.2494
dc.identifier.citedreferenceLenth, R. V. ( 2021 ). emmeans: Estimated marginal means, aka least-squares means. R package version 1.7.1 (Vol. 34 ). R Foundation for Statistical Computing. https://CRAN.R-project.org/package=emmeans
dc.identifier.citedreferenceLevis, N. A., & Pfennig, D. W. ( 2016 ). Evaluating “plasticity-first” evolution in nature: Key criteria and empirical approaches. Trends in Ecology & Evolution, 31 ( 7 ), 563 – 574.
dc.identifier.citedreferenceManzi, F., Agha, R., Lu, Y., Ben-Ami, F., & Wolinska, J. ( 2020 ). Temperature and host diet jointly influence the outcome of infection in a Daphnia -fungal parasite system. Freshwater Biology, 65 ( 4 ), 757 – 767. https://doi.org/10.1111/fwb.13464
dc.identifier.citedreferenceMartinez, J., Perez Serrano, J., Bernadina, W. E., & Rodriguez-Caabeiro, F. ( 1999 ). Influence of parasitization by Trichinella spiralis on the levels of heat shock proteins in rat liver and muscle. Parasitology, 118 ( 2 ), 201 – 209.
dc.identifier.citedreferenceMeng, S., Tran, T. T., Delnat, V., & Stoks, R. ( 2021 ). Transgenerational exposure to warming reduces the sensitivity to a pesticide under warming. Environmental Pollution, 284, 117217.
dc.identifier.citedreferenceMerino, S., Martínez, J., Barbosa, A., Møller, A. P., de Lope, F., Pérez, J., & Rodríguez-Caabeiro, F. ( 1998 ). Increase in a heat-shock protein from blood cells in response of nestling house martins ( Delichon urbica ) to parasitism: An experimental approach. Oecologia, 116 ( 3 ), 343 – 347.
dc.identifier.citedreferenceMoe, S. J., de Schamphelaere, K., Clements, W. H., Sorensen, M. T., van den Brink, P. J., & Liess, M. ( 2013 ). Combined and interactive effects of global climate change and toxicants on populations and communities. Environmental Toxicology and Chemistry, 32 ( 1 ), 49 – 61. https://doi.org/10.1002/etc.2045
dc.identifier.citedreferenceMousseau, T. A., & Fox, C. W. ( 1998 ). The adaptive significance of maternal effects. Trends in Ecology & Evolution, 13 ( 10 ), 403 – 407.
dc.identifier.citedreferenceNoyes, P. D., McElwee, M. K., Miller, H. D., Clark, B. W., van Tiem, L. A., Walcott, K. C., Erwin, K. N., & Levin, E. D. ( 2009 ). The toxicology of climate change: Environmental contaminants in a warming world. Environment International, 35 ( 6 ), 971 – 986.
dc.identifier.citedreferenceop de Beeck, L., Verheyen, J., & Stoks, R. ( 2017 ). Integrating both interaction pathways between warming and pesticide exposure on upper thermal tolerance in high- and low-latitude populations of an aquatic insect. Environmental Pollution., 224, 714 – 721.
dc.identifier.citedreferenceOrr, J. A., Vinebrooke, R. D., Jackson, M. C., Kroeker, K. J., Kordas, R. L., Mantyka-Pringle, C., Van den Brink, P. J., De Laender, F., Stoks, R., Holmstrup, M., Matthaei, C. D., Monk, W. A., Penk, M. R., Leuzinger, S., Schäfer, R. B., & Piggott, J. J. ( 2020 ). Towards a unified study of multiple stressors: Divisions and common goals across research disciplines. Proceedings of the Royal Society B, 287 ( 1926 ), 20200421. https://doi.org/10.1098/rspb.2020.0421
dc.identifier.citedreferenceParaskevopoulou, S., Gattis, S., & Ben-Ami, F. ( 2022 ). Parasite resistance and parasite tolerance: Insights into transgenerational immune priming in an invertebrate host. Biology Letters, 18 ( 4 ), 20220018.
dc.identifier.citedreferencePaull, S. H., & Johnson, P. T. J. ( 2014 ). Experimental warming drives a seasonal shift in the timing of host-parasite dynamics with consequences for disease risk. Ecology Letters, 17 ( 4 ), 445 – 453.
dc.identifier.citedreferencePiccolroaz, S., Woolway, R. I., & Merchant, C. J. ( 2020 ). Global reconstruction of twentieth century lake surface water temperature reveals different warming trends depending on the climatic zone. Climate Change, 160 ( 3 ), 427 – 442. https://doi.org/10.1007/s10584-020-02663-z
dc.identifier.citedreferencePiggott, J. J., Townsend, C. R., & Matthaei, C. D. ( 2015 ). Reconceptualizing synergism and antagonism among multiple stressors. Ecology & Evolution, 5 ( 7 ), 1538 – 1547. https://doi.org/10.1002/ece3.1465
dc.identifier.citedreferenceR Development Core Team. ( 2014 ). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
dc.identifier.citedreferenceRadchuk, V., Reed, T., Teplitsky, C., van de Pol, M., Charmantier, A., Hassall, C., Adamík, P., Adriaensen, F., Ahola, M. P., Arcese, P., Miguel Avilés, J., Balbontin, J., Berg, K. S., Borras, A., Burthe, S., Clobert, J., Dehnhard, N., de Lope, F., Dhondt, A. A., … Kramer-Schadt, S. ( 2019 ). Adaptive responses of animals to climate change are most likely insufficient. Nature Communications, 10 ( 1 ), 1 – 14.
dc.identifier.citedreferenceRoth, O., Beemelmanns, A., Barribeau, S. M., & Sadd, B. M. ( 2018 ). Recent advances in vertebrate and invertebrate transgenerational immunity in the light of ecology and evolution. Heredity, 121 ( 3 ), 225 – 238.
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dc.owningcollnameInterdisciplinary and Peer-Reviewed


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