title: Biotic interactions govern genetic adaptation to toxicants.
abstract: The genetic recovery of resistant populations released from pesticide exposure is accelerated by the presence of environmental stressors. By contrast, the relevance of environmental stressors for the spread of resistance during pesticide exposure has not been studied. Moreover, the consequences of interactions between different stressors have not been considered. Here we show that stress through intraspecific competition accelerates microevolution, because it enhances fitness differences between adapted and non-adapted individuals. By contrast, stress through interspecific competition or predation reduces intraspecific competition and thereby delays microevolution. This was demonstrated in mosquito populations (Culex quinquefasciatus) that were exposed to the pesticide chlorpyrifos. Non-selective predation through harvesting and interspecific competition with Daphnia magna delayed the selection for individuals carrying the ace-1(R) resistance allele. Under non-toxic conditions, susceptible individuals without ace-1(R) prevailed. Likewise, predation delayed the reverse adaptation of the populations to a non-toxic environment, while the effect of interspecific competition was not significant. Applying a simulation model, we further identified how microevolution is generally determined by the type and degree of competition and predation. We infer that interactions with other species-especially strong in ecosystems with high biodiversity-can delay the development of pesticide resistance.
authors.affiliation: Department System Ecotoxicology, UFZ-Helmholtz Centre for Environmental Research, Permoserstrasse 15, 04318 Leipzig, Germany Department of Ecosystem Analysis, RWTH-Aachen University, Institute for Environmental Research, Worringerweg 1, 52074 Aachen, Germany jeremias.becker@ufz.de.
authors.forename: Jeremias Martin
authors.identifier: 0000-0003-1496-0312
authors.initials: JM
authors.lastname: Becker
authors.affiliation: Department System Ecotoxicology, UFZ-Helmholtz Centre for Environmental Research, Permoserstrasse 15, 04318 Leipzig, Germany Department of Ecosystem Analysis, RWTH-Aachen University, Institute for Environmental Research, Worringerweg 1, 52074 Aachen, Germany.
authors.forename: Matthias
authors.identifier: 0000-0002-3321-8909
authors.initials: M
authors.lastname: Liess
mesh_terms: D000220:Adaptation, Biological; D000818:Animals; D004390:Chlorpyrifos / Q000494:pharmacology*; D003163:Competitive Behavior; D003465:Culex / Q000187:drug effects* / Q000235:genetics*; D003621:Daphnia / Q000502:physiology; D004785:Environmental Pollutants / Q000494:pharmacology*; D020387:Food Chain; D056084:Genetic Fitness; D007305:Insecticide Resistance; D007306:Insecticides / Q000494:pharmacology*; D011156:Population Density
chemical_list: D004785:Environmental Pollutants; D007306:Insecticides; D004390:Chlorpyrifos
keywords: Culex quinquefasciatus; competition; ecotoxicology; pesticide resistance; population ecology; predation
references.citation: Evolution. 2006 Feb;60(2):303-14
references.pmid: 16610322
references.citation: Annu Rev Entomol. 2009;54:147-63
references.pmid: 19067630
references.citation: Science. 1908 Jul 10;28(706):49-50
references.pmid: 17779291
references.citation: Aquat Toxicol. 2010 Apr 1;97(1):15-22
references.pmid: 20053462
references.citation: Ecotoxicology. 2011 May;20(3):543-51
references.pmid: 21380529
references.citation: J Econ Entomol. 2000 Dec;93(6):1588-95
references.pmid: 11142285
references.citation: Proc Natl Acad Sci U S A. 2013 Jul 2;110(27):11039-43
references.pmid: 23776226
references.citation: Philos Trans R Soc Lond B Biol Sci. 1985 Aug 17;310(1142):1-75
references.pmid: 2864710
references.citation: Aquat Toxicol. 2012 Mar;109:243-9
references.pmid: 22000337
references.citation: Genet Res. 1997 Dec;70(3):195-203
references.pmid: 9494436
references.citation: Genetica. 2001;112-113:287-96
references.pmid: 11838771
references.citation: Genet Res. 2002 Feb;79(1):41-7
references.pmid: 11974602
references.citation: Proc Biol Sci. 2014 Jul 7;281(1786). pii: 20140558. doi: 10.1098/rspb.2014.0558
references.pmid: 24850927
references.citation: Ecotoxicology. 2011 Nov;20(8):1840-51
references.pmid: 21701843
references.citation: Aquat Toxicol. 2012 Apr;110-111:91-8
references.pmid: 22277250
references.citation: Genetics. 1996 May;143(1):407-16
references.pmid: 8722792
references.citation: Proc Biol Sci. 2005 Jul 22;272(1571):1519-24
references.pmid: 16011928
references.citation: Pestic Biochem Physiol. 1996 Jun;55(2):122-8
references.pmid: 8980036
references.citation: Emerg Infect Dis. 1998 Oct-Dec;4(4):605-13
references.pmid: 9866736
references.citation: Evolution. 2004 Jan;58(1):128-35
references.pmid: 15058725
references.citation: Proc Biol Sci. 2005 May 22;272(1567):1031-8
references.pmid: 16024361
references.citation: Proc Natl Acad Sci U S A. 2014 Apr 8;111(14):5141-6
references.pmid: 24639498
references.citation: Proc Natl Acad Sci U S A. 2012 Nov 20;109(47):19063-70
references.pmid: 23118337
references.citation: Curr Biol. 2004 Jul 27;14(14):R552-3
references.pmid: 15268871
references.citation: Proc Biol Sci. 2014 Dec 22;281(1797). pii: 20141382. doi: 10.1098/rspb.2014.1382
references.pmid: 25355473
references.citation: J Med Entomol. 2010 Mar;47(2):188-98
references.pmid: 20380299
references.citation: BMC Evol Biol. 2009;9:42
references.pmid: 19228410
references.citation: Pest Manag Sci. 2012 Nov;68(11):1431-7
references.pmid: 22945853
references.citation: Evolution. 2014 Jul;68(7):2092-101
references.pmid: 24494966
references.citation: Nature. 1999 Aug 26;400(6747):861-4
references.pmid: 10476962
references.citation: Genet Res. 2004 Jun;83(3):189-96
references.pmid: 15462412
references.citation: Ecotoxicology. 2012 Oct;21(7):1857-66
references.pmid: 22572781
references.citation: Ecotoxicol Environ Saf. 2006 Oct;65(2):145-50
references.pmid: 16545452
references.citation: Trends Ecol Evol. 2013 Feb;28(2):110-8
references.pmid: 23040463
references.citation: J Vector Ecol. 2013 Jun;38(1):82-9
references.pmid: 23701611
references.citation: Environ Pollut. 2014 Feb;185:24-34
references.pmid: 24212068
references.citation: Evolution. 2011 Sep;65(9):2681-91
references.pmid: 21884064
references.citation: Aquat Toxicol. 2012 Jan 15;106-107:25-31
references.pmid: 22057252
references.citation: Environ Toxicol Chem. 2008 Feb;27(2):461-70
references.pmid: 18348641