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Modality matters for the expression of inducible defenses: introducing a concept of predator modality.

Herzog Q, Laforsch C - BMC Biol. (2013)

Bottom Line: We found for the first time that two invertebrate predators induce different shapes of the same morphological defensive traits in Daphnia, rather than showing gradual or opposing reaction norms.Additionally, our concept not only helps to classify different multipredator-systems, but also stresses the significance of costs of phenotype-environment mismatching in addition to classic 'costs of plasticity'.With that, we suggest that 'modality' matters as an important factor in understanding and explaining the evolution of inducible defenses.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology II, Ludwig-Maximilians-University Munich, Großhadernerstr, 2, Planegg-Martinsried 82152, Germany. q.herzog@biologie.uni-muenchen.de.

ABSTRACT

Background: Inducible defenses are a common and widespread form of phenotypic plasticity. A fundamental factor driving their evolution is an unpredictable and heterogeneous predation pressure. This heterogeneity is often used synonymously to quantitative changes in predation risk, depending on the abundance and impact of predators. However, differences in 'modality', that is, the qualitative aspect of natural selection caused by predators, can also cause heterogeneity. For instance, predators of the small planktonic crustacean Daphnia have been divided into two functional groups of predators: vertebrates and invertebrates. Predators of both groups are known to cause different defenses, yet predators of the same group are considered to cause similar responses. In our study we question that thought and address the issue of how multiple predators affect the expression and evolution of inducible defenses.

Results: We exposed D. barbata to chemical cues released by Triops cancriformis and Notonecta glauca, respectively. We found for the first time that two invertebrate predators induce different shapes of the same morphological defensive traits in Daphnia, rather than showing gradual or opposing reaction norms. Additionally, we investigated the adaptive value of those defenses in direct predation trials, pairing each morphotype (non-induced, Triops-induced, Notonecta-induced) against the other two and exposed them to one of the two predators. Interestingly, against Triops, both induced morphotypes offered equal protection. To explain this paradox we introduce a 'concept of modality' in multipredator regimes. Our concept categorizes two-predator-prey systems into three major groups (functionally equivalent, functionally inverse and functionally diverse). Furthermore, the concept includes optimal responses and costs of maladaptions of prey phenotypes in environments where both predators co-occur or where they alternate.

Conclusion: With D. barbata, we introduce a new multipredator-prey system with a wide array of morphological inducible defenses. Based on a 'concept of modality', we give possible explanations how evolution can favor specialized defenses over a general defense. Additionally, our concept not only helps to classify different multipredator-systems, but also stresses the significance of costs of phenotype-environment mismatching in addition to classic 'costs of plasticity'. With that, we suggest that 'modality' matters as an important factor in understanding and explaining the evolution of inducible defenses.

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Distinction between quantitative (a, b) and qualitative differences (c, d) of inducible defenses. C (white) represents a non-induced morph, P1 (light gray) represents a morph defended against the predator 1 and P2 (dark gray) represents a morph defended against predator 2. The triangles, the square and the circle depict the phenotype. In the case of quantitative differences, the changes can be put in order in terms of an increase or decrease (represented by the different sizes of the triangles). This is true for both a) gradual responses (C <P1 <P2) and b) antagonistic responses (P1 <C <P2) In contrast, qualitative differences cannot be put in order in terms of an increase or decrease (represented by the different shapes of the triangles), as changes in different traits would lead to differently shaped phenotypes. This can either be the case, because a) independent changes occur (here: P1 gets higher than C and P2 gets wider than C, so for one trait (for example, width) it is C = P1 <P2 for the other trait (for example, height) it is C = P2 <P1), or b) because the changes to the traits occur to a different extent (here: P1 is higher than P2, but P2 is wider than P1, so for one trait (for example, width) it is C <P1 <P2 for the other trait (for example, height) it is C <P2 <P1).
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Figure 3: Distinction between quantitative (a, b) and qualitative differences (c, d) of inducible defenses. C (white) represents a non-induced morph, P1 (light gray) represents a morph defended against the predator 1 and P2 (dark gray) represents a morph defended against predator 2. The triangles, the square and the circle depict the phenotype. In the case of quantitative differences, the changes can be put in order in terms of an increase or decrease (represented by the different sizes of the triangles). This is true for both a) gradual responses (C <P1 <P2) and b) antagonistic responses (P1 <C <P2) In contrast, qualitative differences cannot be put in order in terms of an increase or decrease (represented by the different shapes of the triangles), as changes in different traits would lead to differently shaped phenotypes. This can either be the case, because a) independent changes occur (here: P1 gets higher than C and P2 gets wider than C, so for one trait (for example, width) it is C = P1 <P2 for the other trait (for example, height) it is C = P2 <P1), or b) because the changes to the traits occur to a different extent (here: P1 is higher than P2, but P2 is wider than P1, so for one trait (for example, width) it is C <P1 <P2 for the other trait (for example, height) it is C <P2 <P1).

Mentions: Our findings are the first records of inducible defenses in D. barbata. Furthermore, we show that D. barbata responds to two different invertebrate predators (Notonecta and Triops) with distinctive morphological responses, rather than displaying a general defense. Unlike in previous records of predator-specific morphological responses across wide taxonomical groups, they consist of neither a gradual extension of the same trait (that is, an intermediate response against one predator and a stronger response against the other predator for example, [24,36]), nor of opposing traits (that is, when a trait increases against one predator and decreases against the other predator compared to the non-induced morph for example, [11,48,49]) or the addition of a new trait (for example, a high-tail against one predator and a high tail and a bulgy head against another [7]). Instead, the defenses are based on the same structures, but formed in a different way. This makes it impossible to order the morphotypes of D. barbata by the magnitude of expression of their traits (that is, quantitative differences, see Figure 3). Rather, the differences represent distinctive shapes, providing a rare example of qualitative predator specific defenses (see Figure 3, in accordance with Bourdeau [20]).


Modality matters for the expression of inducible defenses: introducing a concept of predator modality.

Herzog Q, Laforsch C - BMC Biol. (2013)

Distinction between quantitative (a, b) and qualitative differences (c, d) of inducible defenses. C (white) represents a non-induced morph, P1 (light gray) represents a morph defended against the predator 1 and P2 (dark gray) represents a morph defended against predator 2. The triangles, the square and the circle depict the phenotype. In the case of quantitative differences, the changes can be put in order in terms of an increase or decrease (represented by the different sizes of the triangles). This is true for both a) gradual responses (C <P1 <P2) and b) antagonistic responses (P1 <C <P2) In contrast, qualitative differences cannot be put in order in terms of an increase or decrease (represented by the different shapes of the triangles), as changes in different traits would lead to differently shaped phenotypes. This can either be the case, because a) independent changes occur (here: P1 gets higher than C and P2 gets wider than C, so for one trait (for example, width) it is C = P1 <P2 for the other trait (for example, height) it is C = P2 <P1), or b) because the changes to the traits occur to a different extent (here: P1 is higher than P2, but P2 is wider than P1, so for one trait (for example, width) it is C <P1 <P2 for the other trait (for example, height) it is C <P2 <P1).
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Figure 3: Distinction between quantitative (a, b) and qualitative differences (c, d) of inducible defenses. C (white) represents a non-induced morph, P1 (light gray) represents a morph defended against the predator 1 and P2 (dark gray) represents a morph defended against predator 2. The triangles, the square and the circle depict the phenotype. In the case of quantitative differences, the changes can be put in order in terms of an increase or decrease (represented by the different sizes of the triangles). This is true for both a) gradual responses (C <P1 <P2) and b) antagonistic responses (P1 <C <P2) In contrast, qualitative differences cannot be put in order in terms of an increase or decrease (represented by the different shapes of the triangles), as changes in different traits would lead to differently shaped phenotypes. This can either be the case, because a) independent changes occur (here: P1 gets higher than C and P2 gets wider than C, so for one trait (for example, width) it is C = P1 <P2 for the other trait (for example, height) it is C = P2 <P1), or b) because the changes to the traits occur to a different extent (here: P1 is higher than P2, but P2 is wider than P1, so for one trait (for example, width) it is C <P1 <P2 for the other trait (for example, height) it is C <P2 <P1).
Mentions: Our findings are the first records of inducible defenses in D. barbata. Furthermore, we show that D. barbata responds to two different invertebrate predators (Notonecta and Triops) with distinctive morphological responses, rather than displaying a general defense. Unlike in previous records of predator-specific morphological responses across wide taxonomical groups, they consist of neither a gradual extension of the same trait (that is, an intermediate response against one predator and a stronger response against the other predator for example, [24,36]), nor of opposing traits (that is, when a trait increases against one predator and decreases against the other predator compared to the non-induced morph for example, [11,48,49]) or the addition of a new trait (for example, a high-tail against one predator and a high tail and a bulgy head against another [7]). Instead, the defenses are based on the same structures, but formed in a different way. This makes it impossible to order the morphotypes of D. barbata by the magnitude of expression of their traits (that is, quantitative differences, see Figure 3). Rather, the differences represent distinctive shapes, providing a rare example of qualitative predator specific defenses (see Figure 3, in accordance with Bourdeau [20]).

Bottom Line: We found for the first time that two invertebrate predators induce different shapes of the same morphological defensive traits in Daphnia, rather than showing gradual or opposing reaction norms.Additionally, our concept not only helps to classify different multipredator-systems, but also stresses the significance of costs of phenotype-environment mismatching in addition to classic 'costs of plasticity'.With that, we suggest that 'modality' matters as an important factor in understanding and explaining the evolution of inducible defenses.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology II, Ludwig-Maximilians-University Munich, Großhadernerstr, 2, Planegg-Martinsried 82152, Germany. q.herzog@biologie.uni-muenchen.de.

ABSTRACT

Background: Inducible defenses are a common and widespread form of phenotypic plasticity. A fundamental factor driving their evolution is an unpredictable and heterogeneous predation pressure. This heterogeneity is often used synonymously to quantitative changes in predation risk, depending on the abundance and impact of predators. However, differences in 'modality', that is, the qualitative aspect of natural selection caused by predators, can also cause heterogeneity. For instance, predators of the small planktonic crustacean Daphnia have been divided into two functional groups of predators: vertebrates and invertebrates. Predators of both groups are known to cause different defenses, yet predators of the same group are considered to cause similar responses. In our study we question that thought and address the issue of how multiple predators affect the expression and evolution of inducible defenses.

Results: We exposed D. barbata to chemical cues released by Triops cancriformis and Notonecta glauca, respectively. We found for the first time that two invertebrate predators induce different shapes of the same morphological defensive traits in Daphnia, rather than showing gradual or opposing reaction norms. Additionally, we investigated the adaptive value of those defenses in direct predation trials, pairing each morphotype (non-induced, Triops-induced, Notonecta-induced) against the other two and exposed them to one of the two predators. Interestingly, against Triops, both induced morphotypes offered equal protection. To explain this paradox we introduce a 'concept of modality' in multipredator regimes. Our concept categorizes two-predator-prey systems into three major groups (functionally equivalent, functionally inverse and functionally diverse). Furthermore, the concept includes optimal responses and costs of maladaptions of prey phenotypes in environments where both predators co-occur or where they alternate.

Conclusion: With D. barbata, we introduce a new multipredator-prey system with a wide array of morphological inducible defenses. Based on a 'concept of modality', we give possible explanations how evolution can favor specialized defenses over a general defense. Additionally, our concept not only helps to classify different multipredator-systems, but also stresses the significance of costs of phenotype-environment mismatching in addition to classic 'costs of plasticity'. With that, we suggest that 'modality' matters as an important factor in understanding and explaining the evolution of inducible defenses.

Show MeSH