Predator avoidance and immune defence: costs and trade–offs in snails

Rigby, Mark C.; Jokela, Jukka

doi:10.1098/rspb.2000.0983

Cited by 172 publications

(151 citation statements)

References 24 publications

(19 reference statements)

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“…Tradeoffs between predator and parasite defenses are expected to be common, and previous studies have reported tradeoffs between particular predator-defense responses and parasite-specific resistance mechanisms (30,31). In this study, we document a tradeoff in a multiple antagonist environment mediated by encounter rates with parasites and predators.…”

Section: Discussionmentioning

confidence: 53%

In deep trouble: Habitat selection constrained by multiple enemies in zooplankton

Decaestecker

Meester

Ebert

2002

Proc. Natl. Acad. Sci. U.S.A.

150

153

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Habitat selection behavior is an important predator-avoidance strategy for many organisms. Its particular expression is often explained as the result of a tradeoff between avoiding antagonists and acquiring resources. However, there is need for a broader perspective on this behavior, as organisms are often simultaneously involved in complex antagonistic relationships with multiple types of enemies. We show experimentally that a tradeoff between predator and parasite avoidance may be important in the evolution of habitat selection behavior in the waterflea, Daphnia magna. In this species, negatively phototactic clones suffer less from visually hunting predators by residing in deeper and darker portions of the water column during the day. However, this behavior increases the risk of parasitic infections when the Daphnia are exposed to pond sediments containing parasite spores. Positively phototactic clones, which are at a higher risk of predation, are less exposed to parasite spores in the sediment and consequently suffer less from parasitic infection. We show that the increased risk of infection remains even if the animals change their phototactic behavior on exposure to chemical cues from fish. This tradeoff highlights a substantial cost of predator-induced changes in habitat selection behavior. Tradeoffs caused by multiple enemies may explain genetic polymorphism for habitat selection behavior in many natural populations.I n the face of antagonistic interactions, habitat selection strategies in time and space are essential for the survival of many organisms. Many studies on predation have documented the ecological costs of antipredatory habitat selection behavior, such as reduced food intake, reduced competitive strength, and increased susceptibility to predation by a different kind of predator (1, 2). It has been suggested that such costs favor the evolution of inducible defenses (2) such as diel vertical migration (DVM), which is generally considered to be a predatoravoidance strategy of zooplankton (3-5). In this strategy, the zooplankton reside at greater depths during the day, thus reducing their chance of being detected by visual predators (4, 5). It has been shown that DVM can be induced in several taxa by exposing them to predator kairomones (6-8), i.e., chemical cues that indicate the presence of the predator. Phenotypic variation in induced and constitutive (not dependent on environmental stimuli for activation; ref. 9) DVM has a strong genetic component (8,(10)(11)(12), and the trait shows rapid evolutionary response to changing predator regimes (13).Predators are not the only antagonists that the zooplankton face. Parasites (including pathogens) are common in zooplankton populations, and the fitness costs of infection are severe (14-19). Many parasites produce infective stages within the bottom sediments, where they form long-lasting spore banks (14-16). Because DVM is often so pronounced that the zooplankton reside in, at, or near the bottom sediments during the day (20, 21), we hypothesized that t...

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Section: Discussionmentioning

confidence: 53%

In deep trouble: Habitat selection constrained by multiple enemies in zooplankton

Decaestecker

Meester

Ebert

2002

Proc. Natl. Acad. Sci. U.S.A.

150

153

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“…There is a general premise in life-history theory that maintaining the immune system [5] and avoiding predators [6,7] is costly, and also conditiondependent (e.g. [8,9]).…”

Section: Introductionmentioning

confidence: 99%

Predation selects for increased immune function in male damselflies,Calopteryx splendens

et al. 2010

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Predation selects for numerous traits in many animal species, with sick or parasitized prey often being at high risk. When challenged by parasites and pathogens, prey with poor immune functions are thus likely to be at a selective disadvantage. We tested the hypothesis that predation by birds selects for increased immune function in a wild population of male damselflies Calopteryx splendens, while controlling for a trait known to be under selection by bird predation, dark wing-spots. We found that selection on both immune function and wing-spot size was significantly positive, and that selection on either trait was independent of selection on the other. We found no evidence of nonlinear quadratic or correlational selection. In contrast to previous studies, we found no phenotypic correlation between immune function and wingspot size. There was also no difference in immune response between territorial and non-territorial males. Our study suggests that predation may be an important agent of selection on the immune systems of prey, and because the selection we detected was directional, has the potential to cause phenotypic change in populations.

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“…Similar environment-dependent expression of costs have been detected in animal-parasite systems as well (Kraaijeveld and Godfray, 1997;Fellowes et al, 1998;Lochmiller and Deerenberg, 2000;Moret and Schmid-Hempel, 2000;Hoang, 2001). For example, Rigby and Jokela (2000) showed that the threat of predation modified the costs of immune defense. Hence, investigating trade-offs under variable, ecologically relevant, environmental conditions is crucial for predicting the importance of costs of resistance in natural host populations.…”

Section: Introductionmentioning

confidence: 62%

Environment-dependent trade-offs between ectoparasite resistance and larval competitive ability in the Drosophila–Macrocheles system

Luong

Polák

2007

Heredity

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Costs of resistance are expected to contribute to the maintenance of genetic variation for resistance in natural host populations. In the present study, we experimentally test for genetic trade-offs between parasite resistance and larval competitive ability expressed under varying levels of crowding and temperature. Artificial selection for increased behavioral resistance was applied against an ectoparasitic mite (Macrocheles subbadius) in replicate lines of the fruit fly Drosophila nigrospiracula. We then measured correlated responses to selection in larval competitive ability by contrasting replicate selected and control (unselected) lines in the absence of parasitism. Experiments were conducted under variable environmental conditions: two temperatures and three levels of larval density. Our results reveal a negative genetic correlation between resistance and larval-adult survival under conditions of moderate and severe intra-specific competition. At both low and high temperature, percent emergence was significantly higher among control lines than selected lines. This divergence in larval competitive ability was magnified under high levels of competition, but only at low temperature. Hence, the interaction between selection treatment and larval density was modified by temperature. As predicted, larvae experiencing medium and high levels of competition exhibited an overall reduction in female body size compared to larvae at low levels of competition. Female flies emerging from selected lines were significantly smaller than those females from control lines, but this effect was only significant under conditions of moderate to severe competition. These results provide evidence of environment-dependent trade-offs between ectoparasite resistance and larval competitive ability, a potential mechanism maintaining genetic polymorphism for resistance.

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Predator avoidance and immune defence: costs and trade–offs in snails

Cited by 172 publications

References 24 publications

In deep trouble: Habitat selection constrained by multiple enemies in zooplankton

In deep trouble: Habitat selection constrained by multiple enemies in zooplankton

Predation selects for increased immune function in male damselflies,Calopteryx splendens

Environment-dependent trade-offs between ectoparasite resistance and larval competitive ability in the Drosophila–Macrocheles system

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