Reverse evolution-selection against costly resistance in disease-free microcosm populations of paramecium caudatum (annotated article).pdf

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University of Alberta
Biology (Biological Sciences)
Lien Luong

ORIGINAL ARTICLE doi:10.1111/j.1558-5646.2011.01388.x REVERSE EVOLUTION: SELECTION AGAINST COSTLY RESISTANCE IN DISEASE-FREE MICROCOSM POPULATIONS OF PARAMECIUM CAUDATUM 1 1 1,2 Alison B. Duncan, Simon Fellous, and Oliver Kaltz 1 Institut des Sciences de l’Evolution (ISEM), UMR 5554 (CC065), UniversiteMontpellier2,PlaceEug ene Bataillon, 34095 Montpellier Cedex 05, France 2 E-mail: [email protected] Received January 11, 2011 Accepted May 20, 2011 Data Archived: Dryad doi:10.5061/dryad.4kb77 Evolutionary costs of parasite resistance arise if genes conferring resistance reduce fitness in the absence of parasites. Thus, parasite-mediated selection may lead to increased resistance and a correlated decrease in fitness, whereas relaxed parasite- mediated selection may lead to reverse evolution of increased fitness and a correlated decrease in resistance. We tested this idea in experimental populations of the protozoan Paramecium caudatum and the parasitic bacterium Holospora undulata.After eight years, resistance to infection and asexual reproduction were compared among paramecia from (1) “infected” populations, (2) uninfected “naive” populations, and (3) previously infected, parasite-free “recovered” populations. Paramecia from “infected” populations were more resistant (+12%), but had lower reproduction (–15%) than “naive” paramecia, indicating an evolutionary trade-off between resistance and fitness. Recovered populations showed similar reproduction to naive populations; however, resistance of recently (<3 years) recovered populations was similar to paramecia from infected populations, whereas longer (>3years)reclinswereasl asiepoins.i suggestsaweak,convextrade-offbetween resistance and fitness, allowing recovery of fitness, without complete loss of resistance, favoring the maintenance of a generalist strategy of intermediate fitness and resistance. Our results indicate that (co)evolution with parasites can leave a genetic signature in disease-free populations. KEY WORDS: Holospora undulata,life-history,parasite,selection,trade-off. Evolutionary trade-offs occur if selection on one trait reduces itive ability, fecundity, seed production, etc. Costs of resistance the value of another (Stearns 1992). Such a cost of adaptation are then defined (and measured) as a reduction of fitness in the can lead to negative genetic correlations between fitness compo-absence of parasites (Simms and Rausher 1987; Kraaijeveld et al. nents, thereby maintaining genetic diversity and preventing the 2002; Strauss et al. 2002). Associated costs are predicted to select evolution of omnipotent generalists (Kassen 2002). This univer- for optimal levels of resistance balanced against other impor- sal principle of adaptation costs may also play an important roltant fitness related life-history traits. Theoretical models show in coevolutionary interactions between hosts and parasites. Parathat trade-offs between resistance and other fitness components sites are generally expected to select for higher resistance in can help maintain resistance polymorphism within populations host. However, an increase in resistance can be accompanied by (e.g., Gillespie 1975; Parker 1992; Antonovics and Thrall 1994; areductioninfitness-relevantlife-historytraits,suchascompet- Bowers et al. 1994; Agrawal and Lively 2002), but also promote ⃝C2011 The Author(s). Evolutio2011 The Society for the Study of Evolution. 3462 Evolution 65-12: 3462–3474 SELECTION AGAINST COSTLY RESISTANCE genetic divergence between populations that vary in their expo- that initially set out to test the first prediction tentatively ex- sure to parasite-mediated selection (Elmqvist et al. 1993; Hasu plored the consequence of subsequent relaxed parasite-mediated et al. 2009) or that live in environments where costs of resistance selection for a relatively limited number of selection lines and are expressed differently (Jessup and Bohannan 2008). generations (Table 1A). Among these studies, one identified an Generally, costs of resistance are thought to arise from a increaseinfitnessaftertwotofourgenerationsofrelaxedparasite- conflict between allocation of limited resources to the defense mediatedselectioninonepopulation(BootsandBegon1993),and machinery and to other fitness-relevant functions (Simms and three studies a reduction in resistance (Fuxa and Richter 1998; Rausher 1987; Coustau et al. 2000; Labbeetal.2010).Invari- Luong and Polak 2007; Ye et al. 2009), but they do not report ous plant, invertebrate, or microbial systems, costs of resistance the corresponding changes in resistance or fitness, respectively. have been demonstrated among naturally occurring genotypes Other studies relaxed parasite-mediated selection for cost-free re- (Biere and Antonovics 1996; Strauss et al. 2002; Tian et al. 2003; sistance and, not surprisingly, no change in resistance was later Carton et al. 2005; Gwynn et al. 2005; Jessup and Bohannan observed (Milks et al. 2002; Kolss et al. 2006; Meyer et al. 2010). 2008); over the past few years, an increasing number of studies To our knowledge only one study has explored the effect of long- has also addressed this issue in laboratory selection experiments term relaxed parasite-mediated selection for populations where (Table 1). It is commonly assumed that these trade-offs result costs of resistance were identified. In Escherichia coli popu- from antagonistic pleiotropy of genes conferring resistance, but lations, the cost of resistance against a bacteriophage declined impairing other fitness functions (Lenski 1988; Tian et al. 2003). by 50% over 400 generations in the absence of phage, and this The underlying functional basis may vary from system to system. without loss of resistance (Lenski 1988). This was explained by Overproduction of defense structures or molecules may have en- the action of compensatory mutations restoring fitness functions, ergetic costs, interfere with other biochemical pathways, or even without compromising resistance. Similarly, when retracting the be immunopathogenic (Coustau et al. 2000; Kraaijeveld et al. bacterial biopesticide Bacillus thuringiensis, resistant diamond- 2001; Brown 2003). back moth populations showed reversal toward susceptibility and The form of the relationship between parasite resistance and an increase in fitness within several generations, although not other fitness traits is important for the evolution of resistance necessarily to ancestral levels (Tabashnik et al. 1994). Thus re- characteristics in host populations. In particular the shape of the laxed selection does not necessarily lead to the evolutionary re- relationship is important regarding whether parasite-mediated se- turn to the ancestral state, raising the general question of the lection will maintain resistance polymorphism or not. An increas- reversibility of evolutionary trajectories (Teotonio and Rose ingly costly, or convex, relationship between parasite resistance 2000). and other fitness traits may select for one evolutionary stable, We investigated reverse evolution of costs of resistance in ex- generalist strategy in a host population. Conversely, for a de- perimental long-term populations of the protozoan Paramecium creasingly costly relationship, coexistence of highly resistant and caudatumandthebacterialparasiteHolosporaundulata.Forthese highly susceptible types is possible (Boots and Haraguchi 1999). populations, a previous study had indicated parasite-mediated se- Given the above genetic and functional constraints, we can lection and costs of resistance: paramecia from populations co- establish two main predictions about the evolution of costs of evolving with the parasite had higher levels of resistance, but resistance. First, parasite-mediated selection for increased re- lower growth rates than paramecia from naive populations, never sistance should lead to a correlated decrease in fitness in the exposed to the parasite (Lohse et al. 2006). The present study absence of the parasite. This can be tested by artificial selec- was motivated by the occurrence of a third population type: Over tion or experimental evolution, comparing the direct response to the course of the long-term experiment, some initially infected selection for resistance and the correlated response for fitness populations lost infection and became disease-free. We compared (Table 1A). These types of experiments can reveal very strong resistanceandfitness(reproductiverate)ofthese“recovered”pop- evolutionarytrade-offsbetweenresistanceandfitness;often,how- ulationswithstill“infected”populations,and“naive”populations ever,thesecostsareonlydetectableforcertainfitnesscomponents that had never been exposed to the parasite. We predicted selec- and under certain environmental conditions (mostly stressful). In tion for increased fitness and a concomitant decrease in resistance afwcasetncebtfiwetdfori tia in the “recovered” populations, after extinction of the parasite. If (Table 1A). selection occurs along a trade-off function, we expected fitness The second prediction holds that costly resistance should and resistance of the “recovered” populations to be identical to be selected against in the absence of parasites. That is, relax- that of naive populations (full reversal) or intermediate between ing parasite-mediated selection should re-establish fitness and those of still “infected” and naive populations (partial reversal). lead to a correlated decrease in resistance. Only very few studies The position of the recovered populations along this trade-off have properly tested this second prediction. 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