Predatorinduced Defense Makes Daphnia More

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Predatorinduced Defense Makes Daphnia More BRIEF COMMUNICATION doi:10.1111/j.1558-5646.2011.01240.x PREDATOR-INDUCED DEFENSE MAKES DAPHNIA MORE VULNERABLE TO PARASITES Mingbo Yin,1 Christian Laforsch,1,2 Jennifer N. Lohr,1,3 and Justyna Wolinska1,4 1Ludwig-Maximilians University Munich, Department Biology II, Großhaderner Str. 2, D-82152 Planegg-Martinsried, Germany 2Ludwig-Maximilians University Munich, Geo Bio-Center, Munich, Germany 4E-mail: [email protected] Received September 16, 2010 Accepted January 10, 2011 Inducible defensive traits against herbivores or predators are widespread in plants and animals. Theory predicts that defended morphs have greater fitness in the presence of predators, but lower fitness than undefended morphs in the absence of predators. If such costs did not exist, then a constitutively defended morph would be favored by natural selection; yet, evidence for such costs has been elusive. Our current work reveals a significant cost to inducible defenses. Using the waterflea (Daphnia) model system, we show that induced defended morphs are significantly more vulnerable to infection by a virulent yeast parasite than undefended morphs. In two independent experiments, the proportion of successful infections and the number of parasite spores were higher among defended versus undefended Daphnia. Thus, by demonstrating a previously unknown and environmentally relevant cost to inducible defenses, this study enhances our understanding of adaptive phenotypic plasticity and its evolution. KEY WORDS: Inducible defenses, kairomones, Metschnikowia, phenotypic plasticity. Predation is a major driver of natural selection. Phenotypic plas- (e.g., Tollrian 1995; DeWitt 1998; Scheiner and Berrigan 1998; ticity for the induction of defensive traits has proven to be a Van Buskirk 2000; Relyea 2002; Van Kleunen and Fischer 2005; widespread mechanism for plants and animals to cope with the risk Van Buskirk and Steiner 2009; Auld et al. 2010). For example, of consumption by herbivores and predators (Agrawal 2001). On life-table experiments conducted on the rotifer Brachionus caly- theoretical grounds, inducible defenses are most likely to evolve ciflorus showed that neither the possession of long spines nor the when there is spatial or temporal heterogeneity in predation, and production of offspring with long spines interfered with rotifer when there are reliable cues that can be used to indicate the fu- survivorship, fecundity, or reproductive potential (Gilbert 1980). ture risk of attack (Lively 1986; Riessen 1992; Frank 1993; Hazel It has been suggested that the primary cost of inducible et al. 2004). Present models for the evolutionary stability of in- defenses is a reduction in growth and development (Clark and duced defense suggest that there must be a cost associated with Harvell 1992; Tollrian and Harvell 1999). For example, tadpoles the defended morph in the absence of predators; otherwise we build large tails to escape predators, but this comes at the cost of would expect the defense to be constitutively expressed (Lively slower growth (meta-analysis in Van Buskirk 2000). Small plank- 1986; Van Tienderen 1991; Clark and Harvell 1992; Moran 1992; tonic waterfleas (Daphnia) with induced neck spines (called neck- Riessen 1992; Frank 1993; Hazel et al. 2004). Nonetheless, em- teeth) have an approximately 5–15% delay in reproduction com- pirical studies in some systems have revealed only weak costs pared to undefended morphs (Black and Dodson 1990; Riessen and Sprules 1990). However, these observations of growth and de- 3Present address: Unite´ d’Ecologie et d’Evolution, Departement´ velopmental costs have been questioned. Tollrian (1995) argued de Biologie, Universite´ de Fribourg, Chemin du Musee´ 10, 1700 that the increased time to maturity is not the result of a direct phys- Fribourg, Switzerland. iological cost but a trade-off for larger body size. Consequently, C 2011 The Author(s). Evolution C 2011 The Society for the Study of Evolution. 1482 Evolution 65-5: 1482–1488 BRIEF COMMUNICATION by studying the way morphological and life-history traits respond morphs. This is because the authors focused either primarily on to fish cues in a set of Daphnia clones, Boersma et al. (1998) the host, but not on the parasite fitness (Lass and Bittner 2002; concluded that morphological defenses are often independent of Coors and De Meester 2008), or because each individual Daphnia developmental shifts. Thus, the commonly observed reductions became infected, independently of the kairomone-exposure treat- in growth and developmental rates may not represent costs in ment (Coors and De Meester 2011), probably due to extremely the formation of morphological defenses, but trade-offs between high infectious doses. Thus, the potential trade-offs between these adaptive changes in life-history parameters. two selection pressures, which would be of high ecological and Alternatively, it has been suggested that the evolution of evolutionary relevance, remain unknown. inducible defenses may be favored by alterations in the abun- In the study described here, we raised individuals from mul- dance of predators with different hunting strategies, which may tiple clones, representing two Daphnia taxa, in the presence create mismatches between induced defenses and predation risk or absence of fish kairomones, and subsequently exposed them (Tollrian and Harvell 1999). For example, freshwater snails can to parasite spores. We predicted that the kairomone treatment either produce invasion-resistant shells for defense against water would induce life-history changes known to improve fitness in bugs or crush-resistant shells for defense against crayfish, but not the presence of predators (Tollrian and Dodson 1999), but that both (Hoverman et al. 2005). Likewise, waterfleas are trapped in the predator-induced individuals would show greater infection the same paradoxical situation. In the presence of fish, which feed prevalence and/or intensity than the individuals not exposed to selectively on larger prey (Brooks and Dodson 1965), Daphnia kairomones. reproduce at an earlier age (at smaller size) and produce a greater number of small offspring (Stibor and Luning¨ 1994; Boersma et al. 1998). When gape-limited invertebrate predators are the Materials and Methods most dominant threat, however, Daphnia react in the opposite STUDY SYSTEM way; by delaying reproduction and producing larger offspring Host (Daphnia longispina complex, as revised in Petrusek et al. (Stibor and Luning¨ 1994; Riessen 1999). Consequently, if the rel- 2008) and parasite (Metschnikowia sp., Fig. 1) were isolated ative abundance of different enemies changes, then the induced from Ammersee, Germany, in 2008. Two D. galeata and three phenotype becomes a handicap rather than an advantage. D. galeata × D. longispina hybrid clones were selected from a Despite numerous studies investigating these costs in light of larger collection of sampled clones, to represent two Daphnia adaptation to the wrong form of predation (reviewed in Tollrian taxa inhabiting lake Ammersee (Yin et al. 2010) and different and Harvell 1999), the potential costs of prey exposure to enemies multilocus genotypes within each taxon (as assessed at 15 mi- from different functional levels, predators and parasites, remain crosatellite loci, for methods see Yin et al. 2010). The parasite insufficiently explored. This lack of knowledge is surprising as strain was isolated by exposing one of the clones (Clone_53) nearly all organisms are affected, to some extent, by parasitism. to a spore extract from crushed, lake-infected Daphnia.Stock For example, recent work shows that food webs, previously re- garded to be built on predator–prey relationships, are incomplete without the incorporation of parasites (Lafferty et al. 2008). It has even been argued that parasitism is the most common animal life style (Lafferty et al. 2006). Daphnia provide a textbook example of inducible life-history defenses against predators (reviewed in Tollrian and Dodson 1999; Laforsch and Tollrian 2009) and, at the same time, they are known to face strong pressure from multiple parasites in nature. Given that parasites are often highly virulent to their Daphnia host (re- viewed in Ebert 2005), a higher susceptibility of defended Daph- nia to infection would represent an environmentally relevant cost. Among the hundreds of predator–prey and host–parasite exper- imental surveys using Daphnia as the target prey or host, only three studies have investigated the consequences of simultaneous exposure to both stressors: predator cues (kairomones) and para- Figure 1. Image of noninfected (left-hand side) and heavily in- site spores (Lass and Bittner 2002; Coors and De Meester 2008, fected Daphnia hosts (from D. longispina complex). These animals 2010). In none of these studies, however, was the prevalence of in- were kept in the control media. Arrows indicate regions of high fection compared between the predator-defended and undefended spore density. EVOLUTION MAY 2011 1483 BRIEF COMMUNICATION parasite cultures were maintained by adding uninfected Daphnia Hall et al. 2007). On day 9, Daphnia were transferred to 30 mL of every second week (Lohr et al. 2010). Both infected and unin- fresh kairomone or control medium, respectively. Offspring were fected Daphnia cultures were kept in synthetic media (based on removed and counted daily. Dead Daphnia were ground up and ultrapure water, trace elements and phosphate buffer), at 20◦C, the number of mature spores (Lohr et al. 2010) was determined 16:8 light-dark
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