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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.

Show MeSH
Concept for the role of modality in systems with two predators. The upper section describes the three basic types of modality differences with their subgroups (a) sensu strictu, b) andc) sensu latu). To visualize modality (that is, the qualitative aspect of selection pressure caused by predation) two points are needed. The basic phenotype (that is, the phenotype in an environment without any predation pressure) serves as the initial point C, lying on the origin. The ‘immunity point’ Ipx represents the terminal point, after which natural selection caused by predator x stops (that is, the phenotype is completely defended or ‘immune’). Its coordinates are defined by the modality of the predators given in the first and second row (‘Modality pred. 1’, colored black,’ Modality pred. 2’ colored gray) with k being a positive coefficient and A/B as variables. Between C and Ipx a vector can be formed, representing the direction and length of selection. In the case of predator 1, this vector always lies on the x-axis; therefore, the protection of a phenotype against predator 1 can be read off its x-coordinate. The same is true for predator 2 in type I and II systems, but not for type III. For each type, a description and a theoretical example are given. Additionally for type IIIb, optimal responses in environments with a single (left) or both (right) predators as well as the costs for a mismatching phenotype (defended against the wrong or only one predator) are described in the bottom boxes.
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Figure 4: Concept for the role of modality in systems with two predators. The upper section describes the three basic types of modality differences with their subgroups (a) sensu strictu, b) andc) sensu latu). To visualize modality (that is, the qualitative aspect of selection pressure caused by predation) two points are needed. The basic phenotype (that is, the phenotype in an environment without any predation pressure) serves as the initial point C, lying on the origin. The ‘immunity point’ Ipx represents the terminal point, after which natural selection caused by predator x stops (that is, the phenotype is completely defended or ‘immune’). Its coordinates are defined by the modality of the predators given in the first and second row (‘Modality pred. 1’, colored black,’ Modality pred. 2’ colored gray) with k being a positive coefficient and A/B as variables. Between C and Ipx a vector can be formed, representing the direction and length of selection. In the case of predator 1, this vector always lies on the x-axis; therefore, the protection of a phenotype against predator 1 can be read off its x-coordinate. The same is true for predator 2 in type I and II systems, but not for type III. For each type, a description and a theoretical example are given. Additionally for type IIIb, optimal responses in environments with a single (left) or both (right) predators as well as the costs for a mismatching phenotype (defended against the wrong or only one predator) are described in the bottom boxes.

Mentions: Regarding the adaptive value of these differing traits, the morphs exposed to chemical cues released by Triops had a clear disadvantage under predation by Notonecta compared to the morphs exposed to Notonecta cues. Still, compared to non-induced daphnids, they showed a limited defensive value. Surprisingly, both defended morphotypes performed equally well against T. cancriformis. At first glance, it seems contradictory that a mismatching defense works just as good as the specific adaptation. Even so, as two distinctive morphotypes have evolved instead of a single general defense, either the benefits or the costs (or both) have to differ in favor of the specific defense. Although the predation trials showed no direct benefits (increased survivorship), indirect benefits might exist. Such could be an increase in handling time or in predator mortality (the saw-like orientated microspines along the dorsal ridge may be able to cause injuries within Triops’ food groove). Differences in costs are more difficult to assess, as they are often manifold [50] and depend on both abiotic and biotic factors. As such, they differ in multi-predator environments from single predator environments [48]. Depending on whether predators co-occur or occur subsequently, the costs may change even further. Therefore, it is insufficient to assess the costs of defenses by simple comparisons of predator-exposed and non-predator-exposed individuals. Predator-related environmental costs, like ‘survival trade-offs’ [48,49], can possibly surpass ‘costs of plasticity’ (that is, the costs for the ability to be plastic, for a review see [51]) by far. Costs may also be reduced under certain circumstances; for instance, when a defense against one predator simultaneously offers protection against another predator (as here in the case of D. barbata). Consequently, it is crucial to understand the modalities of the predators in a given system to evaluate the costs of inducible defenses. To this end, it is helpful to visualize modality as an Euclidean vector, showing both the direction and limit of natural selection caused by a predator. Based on that, we developed a novel concept on the influence of modality in multi-predator regimes (Figure 4). In a system with one prey and two predators, three different scenarios are possible: The predators can be functionally equivalent (type I, Figure 4), with both vectors pointing in the same direction, functionally inverse (type II), with both vectors pointing in opposite directions or functionally diverse (type III), with both vectors pointing in different directions. Depending on the conditions, predator-specific inducible defenses can be found within each of the three categories.


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

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

Concept for the role of modality in systems with two predators. The upper section describes the three basic types of modality differences with their subgroups (a) sensu strictu, b) andc) sensu latu). To visualize modality (that is, the qualitative aspect of selection pressure caused by predation) two points are needed. The basic phenotype (that is, the phenotype in an environment without any predation pressure) serves as the initial point C, lying on the origin. The ‘immunity point’ Ipx represents the terminal point, after which natural selection caused by predator x stops (that is, the phenotype is completely defended or ‘immune’). Its coordinates are defined by the modality of the predators given in the first and second row (‘Modality pred. 1’, colored black,’ Modality pred. 2’ colored gray) with k being a positive coefficient and A/B as variables. Between C and Ipx a vector can be formed, representing the direction and length of selection. In the case of predator 1, this vector always lies on the x-axis; therefore, the protection of a phenotype against predator 1 can be read off its x-coordinate. The same is true for predator 2 in type I and II systems, but not for type III. For each type, a description and a theoretical example are given. Additionally for type IIIb, optimal responses in environments with a single (left) or both (right) predators as well as the costs for a mismatching phenotype (defended against the wrong or only one predator) are described in the bottom boxes.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4225664&req=5

Figure 4: Concept for the role of modality in systems with two predators. The upper section describes the three basic types of modality differences with their subgroups (a) sensu strictu, b) andc) sensu latu). To visualize modality (that is, the qualitative aspect of selection pressure caused by predation) two points are needed. The basic phenotype (that is, the phenotype in an environment without any predation pressure) serves as the initial point C, lying on the origin. The ‘immunity point’ Ipx represents the terminal point, after which natural selection caused by predator x stops (that is, the phenotype is completely defended or ‘immune’). Its coordinates are defined by the modality of the predators given in the first and second row (‘Modality pred. 1’, colored black,’ Modality pred. 2’ colored gray) with k being a positive coefficient and A/B as variables. Between C and Ipx a vector can be formed, representing the direction and length of selection. In the case of predator 1, this vector always lies on the x-axis; therefore, the protection of a phenotype against predator 1 can be read off its x-coordinate. The same is true for predator 2 in type I and II systems, but not for type III. For each type, a description and a theoretical example are given. Additionally for type IIIb, optimal responses in environments with a single (left) or both (right) predators as well as the costs for a mismatching phenotype (defended against the wrong or only one predator) are described in the bottom boxes.
Mentions: Regarding the adaptive value of these differing traits, the morphs exposed to chemical cues released by Triops had a clear disadvantage under predation by Notonecta compared to the morphs exposed to Notonecta cues. Still, compared to non-induced daphnids, they showed a limited defensive value. Surprisingly, both defended morphotypes performed equally well against T. cancriformis. At first glance, it seems contradictory that a mismatching defense works just as good as the specific adaptation. Even so, as two distinctive morphotypes have evolved instead of a single general defense, either the benefits or the costs (or both) have to differ in favor of the specific defense. Although the predation trials showed no direct benefits (increased survivorship), indirect benefits might exist. Such could be an increase in handling time or in predator mortality (the saw-like orientated microspines along the dorsal ridge may be able to cause injuries within Triops’ food groove). Differences in costs are more difficult to assess, as they are often manifold [50] and depend on both abiotic and biotic factors. As such, they differ in multi-predator environments from single predator environments [48]. Depending on whether predators co-occur or occur subsequently, the costs may change even further. Therefore, it is insufficient to assess the costs of defenses by simple comparisons of predator-exposed and non-predator-exposed individuals. Predator-related environmental costs, like ‘survival trade-offs’ [48,49], can possibly surpass ‘costs of plasticity’ (that is, the costs for the ability to be plastic, for a review see [51]) by far. Costs may also be reduced under certain circumstances; for instance, when a defense against one predator simultaneously offers protection against another predator (as here in the case of D. barbata). Consequently, it is crucial to understand the modalities of the predators in a given system to evaluate the costs of inducible defenses. To this end, it is helpful to visualize modality as an Euclidean vector, showing both the direction and limit of natural selection caused by a predator. Based on that, we developed a novel concept on the influence of modality in multi-predator regimes (Figure 4). In a system with one prey and two predators, three different scenarios are possible: The predators can be functionally equivalent (type I, Figure 4), with both vectors pointing in the same direction, functionally inverse (type II), with both vectors pointing in opposite directions or functionally diverse (type III), with both vectors pointing in different directions. Depending on the conditions, predator-specific inducible defenses can be found within each of the three categories.

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