Abstract
Natural populations that are exposed to pesticides in their environment may at the same time be exposed to natural stressors like parasites and predators, which may interact with pesticide exposure. This may not only impact target pest species but also a wide variety of non-target species. This review reports on a joint research program in the water flea Daphnia magna, a non-target species often used as model organism in ecology and ecotoxicology. The focus is on different aspects that are of key importance to understand the evolutionary ecology of pesticide exposure: (1) the capacity of natural populations to genetically adapt to pesticide exposure (2) the added complexity of synergistic effects caused by simultaneous exposure to natural stressors, and (3) the potential interference of evolutionary costs of adaptation to pesticide exposure. Our results showed that natural populations were able to rapidly evolve resistance to the pesticide carbaryl but at the expense of fitness costs. Individuals selected for carbaryl resistance had higher survival rates when exposed to the pesticide but also a greater susceptibility to the challenge imposed by the bacterial endoparasite Pasteuria ramosa. The evolved resistance to carbaryl was in some cases only expressed in the absence of fish kairomones. Further, it became clear that the responses to both exposure to single and combined stressors was for several life history variables strongly dependent upon past exposure to carbaryl. This indicates that past exposures to pesticides are important and can not be neglected when evaluating responses to current stressors.
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Aggarwal M, Naraharisetti SB, Dandapat S, Degen GH, Malik JK (2008) Perturbations in immune responses induced by concurrent subchronic exposure to arsenic and endosulfan. Toxicology 251:51–60
Agnew P, Berticat C, Bedhomme S, Sidobre C, Michalakis Y (2004) Parasitism increases and decreases the costs of insecticide resistance in mosquitoes. Evolution 58:579–586
Agra AR, Guilhermino L, Soares AMVM, Barata C (2010) Genetic costs of tolerance to metals in Daphnia longispina populations historically exposed to a copper mine drainage. Environ Toxicol Chem 29:939–946
Albert A, Drouillard K, Haffner GD, Dixon B (2007) Dietary exposure to low pesticide doses causes long-term immunosuppression in the leopard frog (Rana pipiens). Environ Toxicol Chem 26:1179–1185
Arnaud L, Haubruge E, Gage MJG (2005) The malathion-specific resistance gene confers a sperm competition advantage in Tribolium castaneum. Funct Ecol 19:1032–1039
Athrey NRG, Leberg PL, Klerks PL (2007) Laboratory culturing and selection for increased resistance to cadmium reduce genetic variation in the least killifish, Heterandria formosa. Environ Toxicol Chem 26:1916–1921
Auld SKJR, Scholefield JA, Little TJ (2010) Genetic variation in the cellular response of Daphnia magna (Crustacea: Cladocera) to its bacterial parasite. P Roy Soc B Biol Sci 227:3291–3297
Barata C, Baird DJ, Soares AM (2002) Determining genetic variability in the distribution of sensitivities to toxic stress among and within field populations of Daphnia magna. Environ Sci Technol 36:3045–3049
Berticat C, Rousset F, Raymond M, Berthomieu A, Weill M (2002) High Wolbachia density in insecticide-resistant mosquitoes. P Roy Soc B Biol Sci 269:1413–1416
Berticat C, Duron O, Heyse D, Raymond M (2004) Insecticide resistance genes confer a predation cost on mosquitoes, Culex pipiens. Genetical Research 83:189–196
Brausch JM, Smith PN (2009) Development of resistance to cyfluthrin and naphthalene among Daphnia magna. Ecotoxicology 18:600–609
Campero M, De Block M, Ollevier F, Stoks R (2008) Correcting the short-term effect of food deprivation in a damselfly: mechanisms and costs. J Anim Ecol 77:66–73
Carriere Y, Deland JP, Roff DA, Vincent C (1994) Life-history costs associated with the evolution of insecticide resistance. P Roy Soc B Biol Sci 258:35–40
Colbourne J, Pfrender ME, Gilbert D et al (2011) The ecoresponsive genome of Daphnia pulex. Science 331:555–560
Coors A, De Meester L (2008) Synergistic, antagonistic and additive effects of multiple stressors: predation threat, parasitism and pesticide exposure in Daphnia magna. J Appl Ecol 45:1820–1828
Coors A, De Meester L (2010) Fitness and virulence of a bacterial endoparasite in an environmentally stressed crustacean host. Parasitology 138:122–131
Coors A, Decaestecker E, Jansen M, De Meester L (2008) Pesticide exposure strongly enhances parasite virulence in an invertebrate host model. Oikos 117:1840–1846
Coors A, Vanoverbeke J, De Bie T, De Meester L (2009) Land use, genetic diversity and toxicant tolerance in natural populations of Daphnia magna. Aquat Toxicol 95:71–79
Cothran RD, Greco RL, Relyea RA (2010) No evidence that a common pesticide impairs female mate choice in a freshwater amphipod. Environ Toxicol 25:310–314
Cousyn C, De Meester L, Colbourne JK, 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. P Natl Acad Sci USA 98:6256–6260
Davidson C (2004) Declining downwind: amphibian population declines in California and historical pesticide use. Ecol Appl 14:1892–1902
Decaestecker E, Gaba S, Raeymaekers JAM, Stoks R, Van Kerckhoven L, Ebert D, De Meester L (2007) Host-parasite ‘Red Queen’ dynamics archived in pond sediment. Nature 450:U816–U870
Denholm I, Devine GJ, Williamson MS (2002) Evolutionary genetics—insecticide resistance on the move. Science 297:2222–2223
Depledge MH (1994) Genotypic toxicity: implications for individuals and populations. Envrion Health Perp 102:101–104
Duron O, Labbé P, Berticat C, Rousset F, Guillot MR, Weill M (2006) High Wolbachia density correlates with cost of infection for insecticide resistant Culex pipiens mosquitoes. Evolution 60:303–314
Farenhorst M, Mouatcho JC, Kikankie CK, Brooke BD, Hunt RH, Thomas MB, Koekemoer LL, Knols BGJ, Coetzee M (2009) Fungal infection counters insecticide resistance in African malaria mosquitos. P Natl Acad Sci USA 106:17443–17447
Futuyma DJ (1986) Evolutionary biology. Sinauer Associates, Sunderland
Geiger F, Bengtsson J, Berendse F, Weisser WW, Emmerson M, Morales MB, Ceryngier P, Liira J, Tscharntke T, Winqvist C, Eggers S, Bommarco R, Part T, Bretagnolle V, Plantegenest M, Clement LW, Dennis C, Palmer C, Onate JJ, Guerrero I, Hawro V, Aavik T, Thies C, Flohre A, Hanke S, Fischer C, Goedhart PW, Inchausti P (2010) Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic Appl Ecol 11:97–105
Giddings JM, Biever RC, Annunziato MF, Hosmer AJ (1996) Effects of diazinon on large outdoor pond microcosms. Environ Toxicol Chem 15:618–629
Griggs JL, Belden LK (2008) Effects of atrazine and metolachlor on the survivorship and infectivity of Echinostoma trivolvis trematode cercariae. Arch Environ Con Tox 54:195–202
Hanazato T (1995) Combined effect of the insecticide carbaryl and the chaoborus kairomone on helmet development in Daphnia Ambigua. Hydrobiologia 310:95–100
Haubruge E, Arnaud L (2001) Fitness consequences of malathion-specific resistance in red flour beetle (Coleoptera: Tenebrionidae) and selection for resistance in the absence of malathion. J Econ Entomol 94:552–557
Jansen M, Stoks R, Coors A, De Meester L (2010) No evidence for a cost of selection by carbaryl exposure in terms of vulnerability to fish predation in Daphnia magna. Hydriobiologia 643:123–128
King KC, Mclaughlin JD, Boily M, Marcogliese DJ (2010) Effects of agricultural landscape and pesticides on parasitism in native bullfrogs. Biol Conserv 143:302–310
Klerks PL, Levinton JS (1989) Rapid evolution of metal resistance in a benthic oligochaete inhabiting a metal-polluted site. Biol Bull 179:135–141
Koehn RK, Bayne BL (1989) Towards a physiological and genetic understanding of the energetics of the stress response. Biol J Lin Soc 37:157–171
Lampert W (1987) Predictability in lake ecosystems: the role of biotic intercations. In: Schultze ED, Zwölfer H (eds) Ecological studies. Springer, Berlin, Heidelberg, pp 333–346
Lenormand T, Bourget D, Guillemaud T, Raymond M (1999) Tracking the evolution of insecticide resistance in the mosquito Culex pipiens. Nature 400:861–864
Lopes I, Baird DJ, Ribeiro R (2006) Genetic adaptation to metal stress by natural populations of Daphnia longispina. Ecotox Environ Safe 63:275–285
Lopes PC, Sucena E, Santos ME, Magalhaes S (2008) Rapid experimental evolution of pesticide resistance in C. elegans entails no cost and affects the mating system. Plos one 3:e3741
Palumbi SR (2001) Humans as the world’s greatest evolutionary force. Science 293:1786–1790
Pauwels K, De Meester L, Deceastecker E, Stoks R (2010). Phenoloxidase but not lytic activity reflects resistance against Pasteuria ramosa in Daphnia magna. Biol Lett. doi: 10.1098/rsbl.2010.0634
Pestana JLT, Loureiro S, Baird DJ, Soares AMVM (2010) Pesticide exposure and inducible antipredator responses in the zooplankton grazer, Daphnia magna Straus. Chemosphere 78:241–248
Poynton HC, Varshavsky JR, Chang B, Cavigiolio G, Chan S, Holman PS, Loguinov AV, Bauer DJ, Komachi K, Theil EC, Perkins EJ, Hughes O, Vulpe CD (2007) Daphnia magna ecotoxicogenomics provides mechanistic insights into metal toxicity. Environ Sci Technol 41:1044–1050
Raymond M, Berticat C, Weill M, Pasteur N, Chevillon C (2001) Insecticide resistance in the mosquito Culex pipiens: What have we learned about adaptation? Genetica 112(113):287–296
Relyea RA (2003) Predator cues and pesticides: a double dose of danger for amphibians. Ecol Appl 13:1515–1521
Relyea RA (2006) The effects of pesticides, pH, and predatory stress on amphibians under mesocosm conditions. Ecotoxicology 15:503–511
Relyea RA, Hoverman JT (2008) Interactive effects of predators and a pesticide on aquatic communities. Oikos 117:1647–1658
Relyea RA, Mills N (2001) Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor). P Natl Acad Sci USA 98:2491–2496
Roff DA (1997) Evolutionary quantitative genetics. Chapman and Hall, New York
Rohr JR, Crumrine PW (2005) Effects of an herbicide and an insecticide on pond community structure and processes. Ecol Appl 15:1135–1147
Rohr JR, Raffel TR, Sessions SK, Hudson PJ (2008) Understanding the net effects of pesticides on amphibian trematode infections. Ecol Appl 18:1743–1753
Sih A, Bell AM, Kerby JL (2004) Two stressors are far deadlier than one. Trends Ecol Evol 19:274–276
Tabashnik BE, Dennehy TJ, Carriere Y (2005) Delayed resistance to transgenic cotton in pink bollworm. P Natl Acad Sci USA 102:15389–15393
Van Doorslaer W, Stoks R, Duvivier C, Bednarska A, De Meester L (2009) Population dynamics determine genetic adaptation to temperature in Daphnia. Evolution 63:1867–1878
Vitousek PM, Mooney HALJ, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499
Walker CH, Hopkin SPSRM, Peakall DB (2006) Principles of ecotoxicology, 3rd edn. Taylor and Francis Group, CRC press, New York
Acknowledgments
M.J. enjoyed a PhD fellowship of the Agency for Innovation by Science and Technology in Flanders (IWT, Flanders) during this study. A.C. was supported by a postdoctoral fellowship of the K.U. Leuven. This research was financially supported by projects GOA/08/06 and PF/2010/07 of the K.U. Leuven Research Fund and project G.0229.09 of FWO, Flanders. We thank two anonymous reviewers and the committee members of the PhD of MJ (Nico van Straalen, John Colbourne, Karel De Schamphelaere, Dries Knapen, Luisa Orsini, Ellen Decaestecker, Filip Volckaert) for their valuable comments on earlier versions of the manuscript.
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Jansen, M., Coors, A., Stoks, R. et al. Evolutionary ecotoxicology of pesticide resistance: a case study in Daphnia . Ecotoxicology 20, 543–551 (2011). https://doi.org/10.1007/s10646-011-0627-z
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DOI: https://doi.org/10.1007/s10646-011-0627-z