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Journal ArticleDOI

A theory for investment across defences triggered at different stages of a predator-prey encounter

TL;DR: A novel explanation is proposed for the observation that herbivory damage is often not well explained by variation in concentrations of toxic plant secondary metabolites, and coevolutionary approaches will be profitable in future work.
About: This article is published in Journal of Theoretical Biology.The article was published on 2019-07-21 and is currently open access. It has received 8 citations till now. The article focuses on the topics: Investment (macroeconomics).

Summary (2 min read)

Introduction

  • All organisms face threats from enemies, be they predators attacking animal prey, herbivores eating plant tissue, or pathogens and parasites feeding on host tissues.
  • A major and important25 general biological question here is why organisms often invest in several defensive mechanisms, rather than putting all their defensive resources into one highly effective “superdefence”.
  • A good reason for assuming that many defences act sequentially - and hence the focus of this paper - is that interactions between victims and enemies can often be split into a number of stages at which one or more defences can be deployed.
  • The aim in this paper is to introduce a simple but general theoretical description of a combination of defences acting at different stages in the predatory sequence in order to make predictions about how prey should best allocate investment across different defensive stages.

The Sequential Defences Model

  • The authors assume that the prey can invest in at most n stages of defence, which the predator experiences sequentially.
  • The effectiveness of each defence depends upon the level of investment in it.
  • These two scenarios represent the two extreme possibilities for the fitness that ensues when all defences are breached: fitness is not decreased further by the nth defence failing in scenario (A), whereas all fitness is lost in scenario (B) if the nth defence fails.

Examples of investment in defences

  • The authors will give numerical examples for the cases when (1) investment happens in multiple defences, (2) only in one defences, and also (3) the investment functions are different, so that the investment in earlier defences can be either higher or lower than in later defences.
  • Note that the above process might only find a local, rather than global, maximum.
  • Also, the authors found that under some conditions defence investment will concentrated only in the first defence, while, under other conditions, investment can be distributed in several defences with more investment in earlier than in later defences.

Application to Plant Defences

  • The authors model can also apply to many plant-herbivore interactions in which a small insect damages, but does not kill, the plant on which260 it is feeding (Speed et al. 2015 also described a related model for these).
  • In scenario (A), breaching the final defence does not cause further fitness cost on the prey, so the fitness keeps the same between when the final defence is tested but not breached and when the final defence is breached.
  • They report that variation in concentrations of plant270 secondary metabolites is a poor predictor of herbivore damage overall.
  • If this interpretation has general validity, then it suggests that their framework can have widespread application in plant-animal interactions.
  • Key predictions could then be tested, for example that chemical defences never have more investment than earlier acting physical defences.

Relation to Other Theoretical Work on Sequential Defences

  • The authors present here a general model to predict the optimal investment in sequential defences.
  • When the ratio of the constitutive costs to the effectiveness of defences is generally similar and low for both defences, then investment across both defences can be optimal.
  • Britton et al. (2007) uses a concept called “strategy blocking” to explain this phenomenon.
  • They give as an example workers of the ant genus Temnothorax that can be enslaved by the species Protomognathus americanus, but which selectively destroy the slavemaking pupae in their care.
  • The last of their predictions is that where a parasite exploits more than one host,355 competition between the hosts to shift their parasite’s attention toward the others should again select for complexity of defensive portfolio.

Coevolutionary Considerations in Sequential Defence Suites

  • Jongepier et al. (2014) argue that for sequential lines of defence, later lines will be more expensive.
  • To put this a different way, the temporal order in which defences are employed will reflect the order in which they evolved.
  • Using a modelling framework, they argue that a prey is more likely to evolve a way to neutralise the predator as the number of defences increases or as the correlation between values across traits increases.
  • This is illustrated in the Gilman et al. (2012) model itself, and in a subsequent extension modelling plant toxicity by Speed and Ruxton (2014).
  • The word “exclusive” seems important here they mean there is nothing fundamentally beneficial about easy disruption of attacks per se from a population dynamic perspective.

Conclusions

  • In their view the sequential organisation of defences has received relatively little rigorous examination in the literature.
  • This is explained in part by expertise focusing on the mechanisms of individual defensive types (e.g. camouflage or chemical defence), rather than their integration into suites of defences.
  • A valuable predictive aspect of their model, is to make a general argument that explains why earlier defences395 may gain higher investment than later acting defences.
  • In their Discussion section, the authors have shown that the model can be applied to animal, plant and other defensive systems.
  • In relating it to other theoretical works in the field,405 the authors note that coevolutionary approaches to the general question they examine here would add predictive sophistication.

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Citations
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Journal ArticleDOI
TL;DR: In this paper , a working hypothesis for deimatic behaviour is proposed, and the available evidence for the evolution, ontogeny, causation, and survival value of deimal behaviour using Tinbergen's Four Questions as a framework.
Abstract: Deimatic behaviours, also referred to as startle behaviours, are used against predators and rivals. Although many are spectacular, their proximate and ultimate causes remain unclear. In this review we aim to synthesise what is known about deimatic behaviour and identify knowledge gaps. We propose a working hypothesis for deimatic behaviour, and discuss the available evidence for the evolution, ontogeny, causation, and survival value of deimatic behaviour using Tinbergen's Four Questions as a framework. Our overarching aim is to direct future research by suggesting ways to address the most pressing questions in this field.

12 citations

Journal ArticleDOI
TL;DR: Analysis of feeding trials of nematode-infected waxworms with wild-caught great tits found no overall benefit in terms of initial attack on the first prey item, although this does not rule out the possibility of multimodality within this system.

9 citations


Cites background from "A theory for investment across defe..."

  • ...Although the costs of each defence are currently unknown, having both defences present at an early stagemaymean each is relatively cheap to produce or that the nematodeebacterium complex has more resources available for investment in defence (Wang et al., 2017)....

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Journal ArticleDOI
17 Mar 2023-Science
TL;DR: Loeffler-Henry et al. as mentioned in this paper presented a large-scale analysis of evolutionary transitions in amphibian antipredation coloration and demonstrated that the evolutionary transition from camouflage to aposematism is rarely direct but tends to involve an intermediary stage, namely cryptic species that facultatively reveal conspicuous coloration.
Abstract: The initial evolution of warning signals in unprofitable prey, termed aposematism, is often seen as a paradox because any new conspicuous mutant would be easier to detect than its cryptic conspecifics and not readily recognized by naïve predators as defended. One possibility is that permanent aposematism first evolved through species using hidden warning signals, which are only exposed to would-be predators on encounter. Here, we present a large-scale analysis of evolutionary transitions in amphibian antipredation coloration and demonstrate that the evolutionary transition from camouflage to aposematism is rarely direct but tends to involve an intermediary stage, namely cryptic species that facultatively reveal conspicuous coloration. Accounting for this intermediate step can resolve the paradox and thereby advance our understanding of the evolution of aposematism. Description Warning signs Using bright coloration to warn predators off of toxic prey, or aposematism, presents a conundrum in evolution. How do brightly colored organisms survive long enough to warn predators when they are easier to predate than their cryptic peers? Loeffler-Henry et al. used a large phylogeny of amphibians with known warning coloration to assess how such displays evolve. After comparing a series of models, they determined that aposematism likely appears through intermediate steps in which coloration is only visible when an organism is fleeing or intentionally displaying a hidden feature. This work demonstrates how the cost of such a trait may be circumvented through intermediary phenotypes. —CNS Conditionally visible coloration in amphibians may be an important step in the evolution of warning coloration.

3 citations

Journal ArticleDOI
TL;DR: Pupae behavior is concluded that pupa behavior is primarily targeted at minimizing energy expenditure, as compared with larval behavior, which appears to balance energy expenditure between the opposing pressures of foraging and of avoiding predation.
Abstract: Antipredatory behavioral responses tend to be energetically expensive, and prey species thus need to resolve trade-offs between these behaviors and other activities such as foraging and mating. While these trade-offs have been well-studied across taxa, less is known about how costs and benefits vary in different life-history contexts, and associated consequences. To address this question, we compared responses of the yellow fever mosquito (Aedes aegypti [Diptera: Culicidae]) to predation threat from guppy (Poecilia reticulata [Cyprinodontiformes: Poeciliidae]) across two life-history stages-larvae (data from previous study) and pupae (from this study). Pupae are motile but do not feed and are comparable to larvae in terms of behavior. To understand how physiological costs affect the threat sensitivity of pupae, we used sex (with size as a covariate) as a proxy for stored energy reserves, and quantified movement and space use patterns of male (small-sized) and female (large-sized) pupae when exposed to predation threat. We found that pupae did not alter movement when exposed to predator cues but instead altered spatial use by spending more time at the bottom of the water column. We found no effect of pupa sex (or size) on the behavioral responses we measured. We conclude that pupa behavior, both antipredatory and otherwise, is primarily targeted at minimizing energy expenditure, as compared with larval behavior, which appears to balance energy expenditure between the opposing pressures of foraging and of avoiding predation. We suggest that antipredatory defenses in metamorphosing prey are modulated by varying energetic trade-offs associated with different life-history stages.

3 citations

Journal ArticleDOI
TL;DR: In this paper , a comprehensive framework for conceptualizing the evolution of multiple predator defences is presented, with hypotheses for the evolution and role of multiple defences in general and defence portfolios in particular.
Abstract: Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such “defence portfolios” that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade‐offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.

2 citations

References
More filters
Journal ArticleDOI
TL;DR: The hypothesis that herbivores select most strongly on genetic variation in life-history, morphological and physical resistance traits, but the greater pleiotropic effects of genes controlling these traits impose strong constraints on their evolution is proposed.
Abstract: Summary 1. Although secondary metabolites are recognized as fundamental to the defence of plants against insect and mammalian herbivores, their relative importance compared to other potential defensive plant traits (e.g. physical resistance, gross morphology, life-history, primary chemistry and physiology) are not well understood. 2. We conducted a meta-analysis to answer the question: What types of genetically variable plant traits most strongly predict resistance against herbivores? We performed a comprehensive literature search and obtained 499 separate measurements of the strength of covariation (measured as genetic correlations) between plant traits and herbivore susceptibility – these were extracted from 72 studies involving 19 plant families. 3. Surprisingly, we found no overall association between the concentrations of secondary metabolites and herbivore susceptibility – plant traits other than secondary metabolites most strongly predicted herbivore susceptibility. Specifically, genetic variation in life-history traits (e.g. flowering time, growth rate) consistently exhibited the strongest genetic correlations with susceptibility. Genetic variation in gross morphological traits (e.g. no. branches, plant size) and physical resistance traits (e.g. latex, trichomes) were also frequently correlated with variation in herbivore susceptibility, but these relationships depended on attributes of the herbivores (e.g. feeding guild) and plants (e.g. longevity). 4. These results call into question the conventional wisdom that secondary metabolites are the most important anti-herbivore defence of plants. We propose the hypothesis that herbivores select most strongly on genetic variation in life-history, morphological and physical resistance traits, but the greater pleiotropic effects of genes controlling these traits impose strong constraints on their evolution. Meanwhile, secondary metabolites could have evolved to be important defensive mechanisms not because they have the largest effect on herbivores, but because the constraints on their evolution are the weakest.

452 citations


"A theory for investment across defe..." refers background in this paper

  • ...We also explore its application to the evolution of sequentially acting plant defences, proposing a new explanation for the otherwise puzzling lack of effects on herbivory for variation in plant chemical defences (Carmona et al. 2011)....

    [...]

  • ...If plant defences do offer sequential barriers to herbivores, what can our model tell us about variation in investment in these defences? Some insight is possible here from the notable meta-analysis of studies in herbivore damage reported by Carmona et al. (2011). They report that variation in concentrations of plant 270...

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Book
21 May 1987

421 citations


"A theory for investment across defe..." refers background in this paper

  • ...The coevolution between such enemies is a major driving force in evolution, which has contributed substantially to the diversification of defensive mechanisms deployed by organisms, and indeed of life’s forms (Vermeij 1987)....

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Journal ArticleDOI
Akira Sasaki1
TL;DR: Although assuming an empirically common type of asymmetrical gene–for–gene interaction, both host and parasite populations can maintain polymorphism in each locus and retain complex fluctuations.
Abstract: This paper examines a mathematical model for the coevolution of parasite virulence and host resistance under a multilocus gene-for-gene interaction. The degrees of parasite virulence and host resistance show coevolutionary cycles for sufficiently small costs of virulence and resistance. Besides these coevolutionary cycles of a longer period, multilocus genotype frequencies show complex fluctuations over shorter periods. All multilocus genotypes are maintained within host and parasite classes having the same number of resistant/virulent alleles and their frequencies fluctuate with approximately equally displaced phases. If either the cost of virulence or the number of resistance loci is larger then a threshold, the host maintains the static polymorphism of singly (or doubly or more, depending on the cost of resistance) resistant genotypes and the parasite remains universally avirulent. In other words, host polymorphism can prevent the invasion of any virulent strain in the parasite. Thus, although assuming an empirically common type of asymmetrical gene-for-gene interaction, both host and parasite populations can maintain polymorphism in each locus and retain complex fluctuations. Implications for the red queen hypothesis of the evolution of sex and the control of multiple drug resistance are discussed.

244 citations


"A theory for investment across defe..." refers background in this paper

  • ...Sasaki (2000) considers the multiplicative interaction among the effect of defence genes, and finds that the cost of resistance and virulence values can influence the coexistence of multiple defences in static equilibria or coevolutionary cycle.375 In contrast, Bateman et al. (2014) introduce…...

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Journal ArticleDOI
TL;DR: An adaptive explanation of co‐evolution between brood parasites and their hosts is proposed, which centres on the relative strength of two opposing processes: strategy‐facilitation, in which one line of host defence promotes the evolution of another form of resistance, and strategy‐blocking, which may relax selection on another so completely that it causes it to decay.
Abstract: Avian parents and social insect colonies are victimized by interspecific brood parasites-cheats that procure costly care for their dependent offspring by leaving them in another species' nursery. Birds and insects defend themselves from attack by brood parasites; their defences in turn select counter-strategies in the parasite, thus setting in motion antagonistic co-evolution between the two parties. Despite their considerable taxonomic disparity, here we show striking parallels in the way that co-evolution between brood parasites and their hosts proceeds in insects and birds. First, we identify five types of co-evolutionary arms race from the empirical literature, which are common to both systems. These are: (a) directional co-evolution of weaponry and armoury; (b) furtiveness in the parasite countered by strategies in the host to expose the parasite; (c) specialist parasites mimicking hosts who escape by diversifying their genetic signatures; (d) generalist parasites mimicking hosts who escape by favouring signatures that force specialization in the parasite; and (e) parasites using crypsis to evade recognition by hosts who then simplify their signatures to make the parasite more detectable. Arms races a and c are well characterized in the theoretical literature on co-evolution, but the other types have received little or no formal theoretical attention. Empirical work suggests that hosts are doomed to lose arms races b and e to the parasite, in the sense that parasites typically evade host defences and successfully parasitize the nest. Nevertheless hosts may win when the co-evolutionary trajectory follows arms race a, c or d. Next, we show that there are four common outcomes of the co-evolutionary arms race for hosts. These are: (1) successful resistance; (2) the evolution of defence portfolios (or multiple lines of resistance); (3) acceptance of the parasite; and (4) tolerance of the parasite. The particular outcome is not determined by the type of preceding arms race but depends more on whether hosts or parasites control the co-evolutionary trajectory: tolerance is an outcome that parasites inflict on hosts, whereas the other three outcomes are more dependent on properties intrinsic to the host species. Finally, our review highlights considerable interspecific variation in the complexity and depth of host defence portfolios. Whether this variation is adaptive or merely reflects evolutionary lag is unclear. We propose an adaptive explanation, which centres on the relative strength of two opposing processes: strategy-facilitation, in which one line of host defence promotes the evolution of another form of resistance, and strategy-blocking, in which one line of defence may relax selection on another so completely that it causes it to decay. We suggest that when strategy-facilitation outweighs strategy-blocking, hosts will possess complex defence portfolios and we identify selective conditions in which this is likely to be the case.

178 citations


"A theory for investment across defe..." refers background in this paper

  • ...Kilner and Langmore (2011) also argue that defences can operate at levels of organisation greater than the individual that are often overlooked....

    [...]

  • ...Kilner and Langmore (2011) speculate that as a generality kin-structuring in a host population will select for a more extensive portfolio of defences....

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  • ...Kilner and Langmore (2011) argue that if the strategy of such random rejection evolves then this will allow subsequent evolution of egg recognition to facilitate non-random targeting of the alien egg....

    [...]

Journal ArticleDOI
TL;DR: Prey may respond evolutionarily to predator pressure either by removing themselves from the foraging microhabitat of the predators (predator avoidance mechanisms) or by reducing the probability of successful predation when they are within the perceptual field of the predator (antipredator mechanisms).
Abstract: Prey may respond evolutionarily to predator pressure either by removing themselves from the foraging microhabitat of the predators (predator avoidance mechanisms) or by reducing the probability of successful predation when they are within the perceptual field of the predators (antipredator mechanisms). These two categories of survival mechanisms are under different selective regimes and the evolution of one type of prey survival mechanism reduces selection on the other.

121 citations

Frequently Asked Questions (2)
Q1. What have the authors contributed in "A theory for investment across defences triggered at different stages of a predator-prey encounter" ?

The authors introduce a general theoretical description of a combination of defences acting sequentially at differ5 ent stages in the predatory sequence in order to make predictions about how animal prey should best allocate investment across different defensive stages. The framework the authors propose can be applied to other victim-exploiter systems, such as insect herbivores feeding on plant tissues. The authors compare their general theoretical structure with related examples in the literature, and conclude that coevolutionary approaches will be profitable in future work. 

In their Discussion section, the authors have shown that the model can be applied to animal, plant and other defensive systems.