Automimicry and the evolution of discrete prey defences

We consider the neglected question of how secondary defences of prey animals evolve if they are discontinuous in nature, being either present or absent, or expressible over a limited number of levels. We present a novel computer model that evaluates the conditions in which defended mutant prey may (1) fail to rise above nontrivial levels within a population, (2) reach values close to fixation, or (3) find some evolutionarily stable strategy (ESS) frequency between these two situations. Undefended prey that coexist with defended conspecifics are known as automimics. One finding is that automimicry can be an ESS over a range of conditions, but especially when prey are relatively cryptic and secondary defences are very effective at deterring predation. Evolutionarily stable automimicry emerges from the interplay between the direct benefits of costly defences in surviving individual attacks by predators and frequency-dependent benefits conferred on all prey, from a reduction in the rate of attack on all identical-looking prey. When, in contrast, secondary defences have continuous variation, the result is effectively a monomorphic state of defence across the population. Thus the degree and kind of variation that a defence takes has a profound effect on its initial evolution. We discuss the interesting possibility that mixed ESSs may help explain some examples of variation in prey secondary defences.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 393–402.     

How can automimicry persist when predators can preferentially consume undefended mimics?

It is common for species that possess toxins or other defences to advertise these defences to potential predators using aposematic ("warning") signals. There is increasing evidence that within such species, there are individuals that have reduced or non-existent levels of defence but still signal. This phenomenon (generally called automimicry) has been a challenge to evolutionary biologists because of the need to explain why undefended automimics do not gain such as a fitness advantage by saving the physiological costs of defence that they increase in prevalence within the population, hence making the aposematic signal unreliable. The leading theory is that aposematic signals do not stop all predatory attacks but rather encourage predators to attack cautiously until they have identified the defence level of a specific individual. They can then reject defended individuals and consume the undefended. This theory has recently received strong empirical support, demonstrating that high-accuracy discrimination appears possible. However, this raises a new evolutionary problem: if predators can perfectly discriminate the defended from the undefended and preferentially consume the latter, then how can automimicry persist? Here, we present four different mechanisms that can allow non-trivial levels of automimics to be retained within a population, even in the extreme case where predators can differentiate defended from undefended individuals with 100% accuracy. These involve opportunity costs to the predator of sampling carefully, temporal fluctuation in predation pressure, predation pressure being correlated with the prevalence of automimicry, or developmental or evolutionary constraints on the availability of defence. These mechanisms generate predictions as to the conditions where we would expect aposematically signalling populations to feature automimicry and those where we would not.     

A field demonstration of the costs and benefits of group living to edible and defended prey

Both theoretical and laboratory research suggests that many prey animals should live in a solitary, dispersed distribution unless they lack repellent defences such as toxins, venoms and stings. Chemically defended prey may, by contrast, benefit substantially from aggregation because spatial localization may cause rapid predator satiation on prey toxins, protecting many individuals from attack. If repellent defences promote aggregation of prey, they also provide opportunities for new social interactions; hence the consequences of defence may be far reaching for the behavioural biology of the animal species. There is an absence of field data to support predictions about the relative costs and benefits of aggregation. We show here for the first time using wild predators that edible, undefended artificial prey do indeed suffer heightened death rates if they are aggregated; whereas chemically defended prey may benefit substantially by grouping. We argue that since many chemical defences are costly to prey, aggregation may be favoured because it makes expensive defences much more effective, and perhaps allows grouped individuals to invest less in chemical defences.     

Low nutritive quality as a plant defence: Effects of herbivore-mediated interactions

Summary A plant may lower its nutritive quality, for herbivores, by using secondary compounds, morphological characters and/or having a lowered nutrient content. If such traits decrease the amount of resources lost through herbivory, then they act as antiherbivore defences. However, if herbivores compensate for the lowered nutrient availability, by increasing their intake rates or by prolonging their feeding periods, then this may render the defence useless. I analyse the conditions for evolution of this type of plant defences in a game theoretical model. The predictions of the model depend on the amount of compensatory feeding performed by the herbivores and on the herbivores' mobility in relation to the spatial structure of the plant population. When herbivores cannot compensate for a lowered nutritive quality, the defence can evolve irrespective of the type of herbivore. When herbivores can compensate for such defences, the outcome depends on how the herbivores compensate. In situations where herbivores compensate only on defended plants, which could correspond to immobile herbivores, this type of defence can evolve only if the level of compensation is lower than a certain critical value. When herbivores compensate more on defended than on undefended plants, e.g. because of low mobility, the outcome depends on the level of compensation performed on defended plants. If this level of compensation is high, then the model predicts a stable coexistence of defended and undefended plants and, if it is low, then the populations can consist of only defended plants. When herbivores compensate more on undefended plants than on defended ones, e.g. highly mobile herbivores, the result is populations consisting of either only defended plants, or only undefended plants. Consequently, the fact that herbivores may compensate for lowered nutrient quality does not, as such, nullify the notion of low nutrient quality as a plant defence. However, compensatory feeding may restrict the conditions for the evolution of such defences.     

Testing Müllerian mimicry: an experiment with wild birds

Experiments with wild birds feeding on pastry 'prey' were performed to test competing theories of Müllerian mimicry Conventional theories predict that all resemblances between defended prey will be mutually advantageous and, hence, Müllerian. In contrast, unconventional theories predict that, if there are inequalities in defences between mimetic species, the less well-defended prey may dilute the protection of the better defended species in a quasi-Batesian manner. This unconventional prediction follows from an assumption that birds learn about the edibilities of prey using rules of Pavlovian learning. We report on two experiments, each lasting 40 days, which showed that a moderately defended prey can dilute the protection of a better defended mimic in a quasi-Batesian fashion, but can add protection to a mimic which has the same moderate levels of defence. These results match predictions of unconventional theories of mimicry and go some way to resolving the long-running arguments over the nature of Müllerian mimicry.     

Parameterising a public good: how experiments on predation can be used to predict cheat frequencies

Chemical defence is superficially easy to understand as a means for individuals to protect themselves from enemies. The evolution of chemical defence is however potentially complex because such defences may cause the generation of a public good, protecting members of the population as a whole as well as individuals that deploy toxins defensively. If a public good of protection exists, it may be exploited and degraded by “cheats” that do not invest in defence. This can in turn lead to complex frequency (and density) dependent effects in toxin evolution. To investigate this we used ecologically relevant predators (Great tits, Parus major) and examined how individual and public benefits vary depending on the frequency of non-defended “cheating” prey and their spatial distribution. We found that the public benefit, of reduced attack probability, increased with increasing frequency of defended individuals. In contrast the individual benefit of chemical defence, measured as increased chance of rejection during an attack before injury, did not vary with the frequency of defended forms. Hence the selective dynamics of these two levels of benefits responded differently to the frequency of defended forms. Surprisingly, given the strong associations of chemical defences and grouping in animals, large aggregations did not help individuals in the group regardless of their defence status. The explanation for the result, may be that in our experiment birds did not have information about other potential aggregations (i.e. set up was sequential) and thus their giving up density was lower compared to the situations where set ups were simultaneous. We use behavioural data of our predators to construct a simple model of toxin evolution which can make quantitative predictions about the frequencies to which defence cheats evolve. We use this model to discuss how toxin evolution can be investigated in the wild and in laboratory settings.     

Evolutionarily stable defence and signalling of that defence

We examine the evolution and maintenance of defence and conspicuousness in prey species using a game theoretic model. In contrast to previous works, predators can raise as well as lower their attack probabilities as a consequence of encountering moderately defended prey. Our model predicts four distinct possibilities for evolutionarily stable strategies (ESSs) featuring maximum crypsis. Namely that such a solution can exist with (1) zero toxicity, (2) a non-zero but non-aversive level of toxicity, (3) a high, aversive level of toxicity or (4) that no such maximally cryptic solution exists. Maximally cryptic prey may still invest in toxins, because of the increased chance of surviving an attack (should they be discovered) that comes from having toxins. The toxin load of maximally cryptic prey may be sufficiently strong that the predators will find them aversive, and seek to avoid similar looking prey in future. However, this aversiveness does not always necessarily trigger aposematic signalling, and highly toxic prey can still be maximally cryptic, because the increased initial rate of attack from becoming more conspicuous is not necessarily always compensated for by increased avoidance of aversive prey by predators. In other circumstances, the optimal toxin load may be insufficient to generate aversion but still be non-zero (because it increases survival), and in yet other circumstances, it is optimal to make no investment in toxins at all. The model also predicts ESSs where the prey are highly defended and aversive and where this defence is advertised at a cost of increased conspicuousness to predators. In many circumstances there is an infinite array of these aposematic ESSs, where the precise appearance is unimportant as long as it is highly visible and shared by all members of the population. Yet another class of solutions is possible where there is strong between-individual variation in appearance between conspicuous, poorly defended prey.     

Toxin depletion has no effect on antipredator responses in common toad (Bufo bufo) tadpoles

Antipredator responses often involve changes in several phenotypic traits and these changes interactively influence fitness. However, gaining insight into how the overall fitness effect of the overall response comes about is notoriously difficult. One promising avenue is to manipulate a single defensive trait and observe how that modifies fitness as well as the expression of other inducible responses. In chemically‐defended animals, toxins are likely to be costly to produce but it is still unknown how their depletion influences other characteristics. In the present study, we artificially depleted bufadienolide toxin stores in common toad (Bufo bufo) tadpoles, and assessed the effect of this with respect to the interaction with predator presence and limited food availability. We found that toxin depletion in tadpoles did not significantly affect any of the measured life‐history traits. Tadpoles in the predator treatment exhibited an elevated development rate, although this was only apparent when food availability was limited. Also, body mass at metamorphosis was lower in tadpoles exposed to chemical cues indicating a predation threat and when food availability was limited. These results provide evidence that, in larval common toads, the expression of inducible defences may incur fitness costs, whereas chemical defences are either expressed constitutively or, if inducible, elevated toxin production has negligible costs.     

Costs and limits of dosage response to predation risk: to what extent can tadpoles invest in anti-predator morphology?

Inducible defences have long been considered as a polyphenism opposing defended and undefended morphs. However, in nature, preys are exposed to various levels of predation risk and scale their investment in defence to actual predation risk. Still, among the traits that are involved in the defence, some are specific to one predator type while others act as a more generalised defence. The existence of defence costs could prevent an individual investing in all these traits simultaneously. In this study, we investigate the impact of an increasing level of predator density (stickleback, Gasterosteus aculeatus) on the expression of morphological inducible defences in tadpoles of Rana dalmatina. In this species, investment in tail length and tail muscle is a stickleback-specific response while increased tail fin depth is a more general defence. As expected, we found a relationship between investment in defence and level of risk through the responses of tail fin depth and tail length. We also found an exponential increase of defence cost, notably expressed by convex decrease of growth and developmental rates. We found a relative independence of investment in the different traits that compose the defence, revealing a high potential for fine tuning the expression of defended phenotypes with respect to local ecological conditions.     

Density-dependent investment in costly anti-predator defences: an explanation for the weak survival benefit of group living

A central explanation for group living across animal taxa is the reduced rate of attack by predators. However, many field observations show a weak or non-existent effect of group size on per capita mortality rates. Herein we resolve this apparent paradox. We found that Pieris brassicae larvae defended themselves less readily when in groups than when alone, in that they were more reluctant to regurgitate in response to simulated attacks and produced less regurgitant. Furthermore, a simple model demonstrates that this reluctance was sufficient to cancel out the benefit from being in a group. This conditional strategy can be understood in terms of the costs and benefits of defences. For grouped individuals, defence is less often required because attack rates are lower and the costs of defence may be higher due to competition for resources. These phenomena are likely to be widespread in facultatively gregarious species that utilise anti-predator defences.     

Inducible defenses: continuous reaction norms or threshold traits?

Phenotypically plastic traits can be expressed as continuous reaction norms or as threshold traits, but little is known about the selective conditions that favor one over the other. We study this question using a model of prey defenses in which prey can induce any level of defense conditional on cues that are informative of local predator density. The model incorporates a trade-off between defense expression and fecundity and feedback between the defense level of prey and predator attack rates. Both continuous reaction norms and threshold traits can emerge as evolutionarily stable solutions of defense induction, and we show that the shape of the trade-off curve plays a key role in determining the outcome. Threshold traits are favored when selection is disruptive. Ecological conditions that favor defense dimorphisms in the absence of cues will favor threshold traits in the presence of slightly informative cues. We caution that continuous reaction norms and threshold traits may result in similar patterns of defense expression at the population level, and we discuss potential pitfalls of inferring reaction norm type from observational data.     

Inducible chemical defences in animals

Phenotypic plasticity is extremely widespread in the behaviour, morphology and life‐history of animals. However, inducible changes in the production of defensive chemicals are described mostly in plants and surprisingly little is known about similar plasticity in chemical defences of animals. Inducible chemical defences may be common in animals because many are known to produce toxins, the synthesis of toxins is likely to be costly, and there are a few known cases of animals adjusting their toxin production to changes in environmental conditions. We outline what is known about the occurrence of inducible chemical defences in animals and argue that there is immense potential for progress in this field. Possible directions include surveying diverse taxa to explore how general its occurrence may be and testing for selection acting on inducible chemical defences. Data on inducible chemical defences would provide insight into life‐history tradeoffs by enabling novel tests of how time‐costs and resource‐costs affect life‐history. If the synthesis of toxic compounds by animals proves accessible to manipulation, as it is in plants and fungi, this will open the way to refined estimates of the fitness costs of defence, ultimately providing a clearer picture of how plasticity evolves and is maintained in nature. Synthesis Inducible changes in the behaviour, morphology, and life‐history of animals are extremely widespread, but surprisingly little is known about similar changes in the production of defensive chemicals. We outline what is known about the occurrence of inducible chemical defences in animals and argue that there is immense potential for progress in this field. Possible directions include surveying diverse taxa to explore how general its occurrence may be and testing for selection acting on inducible chemical defences. Data on inducible chemical defences would provide insight into life‐history tradeoffs by enabling novel tests of how time‐costs and resource‐costs affect life‐history. If the synthesis of toxic compounds by animals proves accessible to manipulation, we will be able to estimate the fitness costs of defence more precisely, and ultimately provide a clearer picture of how plasticity evolves and is maintained in nature.     

Physiological mechanisms underlying the costs of chemical defence in Junonia coenia Hu¨bner (Nymphalidae): A gravimetric and quantitative genetic analysis

Several recent studies document that specialist insect phytophages may be less subject to predation than generalists and suggest that hostplant-derived chemical defences may be an important explanation for the predominance of specialized feeding among insect herbivores. The evolution of such chemical defences depends upon both their advantages versus natural enemies and their physiological costs, but data on these costs, particularly genetic data, are few. Here I report the results of an ecological genetic investigation of food use efficiency and allelochemical sequestration in Junonia coenia Hu¨bner (Nymphalidae). I used standard gravimetric techniques to estimate the efficiency of dry matter incorporation and iridoid glycoside sequestration in the larvae of 37 full-sib families fed artificial diets containing trace, low (2%) and high (10%) concentrations of iridoid glycosides. I found a significant reduction in the efficiency of dry matter incorporation on a high iridoid diet that is entirely attributable to reduced digestibility rather than post-digestive toxic effects. Larvae fed high-iridoid diets sequestered them less efficiently, but this difference was due largely to post-digestive effects. Analyses of genetic variation and architecture of dry matter and iridoid budgets reveal substantial genetic variation in both suites of traits, but only chemical defence showed a significant genotype×environment interaction which would be conducive to the evolution of specialization. Neither group of traits showed across-diet trade-offs in the form of negative correlations of family means among diets. Family means correlations of sequestration indices with dry matter indices within diets reveals that chemical defence comes at a cost to growth, but only in the high diet. I also found evidence of specialized physiological machinery for iridoid glycoside processing. These data indicate that even adapted specialists are negatively affected by plant toxins, but in this species, dietary specialization is more likely to result from selection from natural enemies than from hostplant toxins.     

Aggregation, defence and warning signals: the evolutionary relationship

In a seminal contribution, Fisher argued how distastefulness could incrementally evolve in a prey species that was distributed in family groups. Many defended prey species occur in aggregations, but did aggregation facilitate the evolution of defence as Fisher proposed or did the possession of a defence allow individuals to enjoy the benefits of group living? Contemporary theory suggests that it can work both ways: pre-existing defences can make the evolution of gregariousness easier, but gregariousness can also aid the evolution of defence and warning signals. Unfortunately, the key phylogenetic analyses to elucidate the ordering of events have been hampered by the relative rarity of gregarious species, which in itself indicates that aggregation is not a pre-requisite for defence. Like the underlying theory, experimental studies have not given a definitive answer to the relative timing of the evolution of defence and aggregation, except to demonstrate that both orderings are possible. Conspicuous signals are unlikely to have evolved in the absence of a defence and aggregated undefended prey are likely to be vulnerable to predation in the absence of satiation effects. It therefore seems most likely that defence generally preceded the evolution of both aggregation and signalling, but alternative routes may well be possible.     

Inducible defences are a stabilizing factor for predator and prey populations: a field experiment

1. Based on mathematical models, antipredator defence mechanisms are commonly believed to have stabilizing effects on communities. However, empirical data are still lacking. 2. We tested stabilizing effects of an inducible vertical migration defence in two Daphnia pulex clones in a 5‐week field enclosure experiment. A defended (migrated down into darker water layers in the presence of fish chemicals in both laboratory and field experiments) and non‐defended (no ability to react to fish chemicals) clone were directly exposed to fish predators and compared to control enclosures (no fish). 3. In the absence of planktivorous fish, both defended and non‐defended clones exhibited boom‐and‐bust dynamics, probably owing to over‐exploitation of the food source. Predation almost led to extinction of the non‐defended Daphnia clone during the experiment and the fish, deprived of food, lost weight. However, the population density of the defended clone was stable and it did not over‐exploit the algal food source, while there was a continuous supply of food to the fish, which consequently gained weight. 4. We conclude that both consumptive and non‐consumptive (also called non‐lethal or trait‐mediated) predator effects, coupled with prey defences, are key contributors to prey stability. This has a positive effect on both the predator and the food organism of the prey.     

Defence Cheats Can Degrade Protection of Chemically Defended Prey

Many species defend themselves against enemies using repellent chemicals. An important but unanswered question is why investment in chemical defence is often variable within prey populations. One explanation is that some prey benefit by cheating, paying no costs of defence, but gaining a reduced attack rate because of the presence of defended conspecifics. Two important assumptions about predator behaviour must be met to explain cheating as a stable strategy: first, predators increase attack rates as cheats increase in frequency; second, defended prey survive attacks better than non‐defended conspecifics. We lack data from wild predators that evaluate these hypotheses. Here, we examine how changes in the frequency of non‐defended ‘cheats’ affect predation by wild birds on a group of otherwise defended prey. We presented mealworm larvae that were either edible (‘cheats’) or unpalatable (bitter tasting), and varied the proportion of cheats from 0 to 1 by increments of 0.25. We found strong frequency‐dependent effects on the birds' foraging behaviour, with the proportion of prey attacked increasing nonlinearly with the frequency of cheats. We did not, however, observe that birds taste‐rejected defended prey at the site of capture. One explanation is that wild birds may not assess prey palatability at the site of capture, but do this elsewhere. If so, defended and undefended prey may pay high costs of initial attack and relocation away from ecologically favourable locations. Alternatively, defended prey may not be taste‐rejected because with acute time constraints, wild birds do not have time to make fine‐grained decisions during feeding. We discuss the data in relation to the evolutionary ecology of prey defences.     

Metabolomic assessment of induced and activated chemical defence in the invasive red alga Gracilaria vermiculophylla

In comparison with terrestrial plants the mechanistic knowledge of chemical defences is poor for marine macroalgae. This restricts our understanding in the chemically mediated interactions that take place between algae and other organisms. Technical advances such as metabolomics, however, enable new approaches towards the characterisation of the chemically mediated interactions of organisms with their environment. We address defence responses in the red alga Gracilaria vermiculophylla using mass spectrometry based metabolomics in combination with bioassays. Being invasive in the north Atlantic this alga is likely to possess chemical defences according to the prediction that well-defended exotics are most likely to become successful invaders in systems dominated by generalist grazers, such as marine macroalgal communities. We investigated the effect of intense herbivore feeding and simulated herbivory by mechanical wounding of the algae. Both processes led to similar changes in the metabolic profile. Feeding experiments with the generalist isopod grazer Idotea baltica showed that mechanical wounding caused a significant increase in grazer resistance. Structure elucidation of the metabolites of which some were up-regulated more than 100 times in the wounded tissue, revealed known and novel eicosanoids as major components. Among these were prostaglandins, hydroxylated fatty acids and arachidonic acid derived conjugated lactones. Bioassays with pure metabolites showed that these eicosanoids are part of the innate defence system of macroalgae, similarly to animal systems. In accordance with an induced defence mechanism application of extracts from wounded tissue caused a significant increase in grazer resistance and the up-regulation of other pathways than in the activated defence. Thus, this study suggests that G. vermiculophylla chemically deters herbivory by two lines of defence, a rapid wound-activated process followed by a slower inducible defence. By unravelling involved pathways using metabolomics this work contributes significantly to the understanding of activated and inducible defences for marine macroalgae.     

Disengtangling the evolution of weak warning signals: high detection risk and low production costs of chemical defences in gregarious pine sawfly larvae

Evolution of costly secondary defences for a cryptic prey is puzzling, if the prey is already well protected by camouflage. However, if the chemical defence is not sufficient to deter all predators, selection can favour low signal intensity in defended prey. Alternatively, if the costs of chemical defence are low or cost-free, chemical defences can be expected to evolve also for non-signalling prey, particularly if conspicuous signalling is costly. We tested these assumptions with pine sawfly larvae (Neodiprion sertifer and Diprion pini) that are cryptically coloured and chemically defended with resin acids sequestered from their host plant (Pinus sp.). Larvae feed in large aggregations, which we hypothesise could function as a signal of unprofitability. Our results show that even though the birds found N. sertifer larvae unprofitable in the controlled laboratory assays, they continued attacking and consuming them in the wild. When we tested the signal value of aggregation we found that a large group size did not offer protection for a defended larva: the survival was higher in groups of 10 individuals compared to groups of 50, suggesting increased detectability costs for individuals in larger groups. Finally, we tested how costly the production and maintenance of a chemical defence is for D. pini larvae by manipulating the resin acid content of the diet. We did not find any life history or immunological costs of the chemical defence for the larvae. In contrast, pupal weights were higher on the high resin diet than on the low resin diet. Also, larvae were able to produce higher amounts of defence fluids on the high diet than on the low diet. Thus, our result suggests high detectability costs and low production costs of defences could explain why some unprofitable species have not evolved conspicuous signals.     

Why are defensive toxins so variable? An evolutionary perspective

Defensive toxins are widely used by animals, plants and micro-organisms to deter natural enemies. An important characteristic of such defences is diversity both in the quantity of toxins and the profile of specific defensive chemicals present. Here we evaluate evolutionary and ecological explanations for the persistence of toxin diversity within prey populations, drawing together a range of explanations from the literature, and adding new hypotheses. We consider toxin diversity in three ways: (1) the absence of toxicity in a proportion of individuals in an otherwise toxic prey population (automimicry); (2) broad variation in quantities of toxin within individuals in the same population; (3) variation in the chemical constituents of chemical defence. For each of these phenomena we identify alternative evolutionary explanations for the persistence of variation. One important general explanation is diversifying (frequency- or density-dependent) selection in which either costs of toxicity increase or their benefits decrease with increases in the absolute or relative abundance of toxicity in a prey population. A second major class of explanation is that variation in toxicity profiles is itself nonadaptive. One application of this explanation requires that predator behaviour is not affected by variation in levels or profiles of chemical defence within a prey population, and that there are no cost differences between different quantities or forms of toxins found within a population. Finally, the ecology and life history of the animal may enable some general predictions about toxin variation. For example, in animals which only gain their toxins in their immature forms (e.g. caterpillars on host plants) we may expect a decline in toxicity during adult life (or at least no change). By contrast, when toxins are also acquired during the adult form, we may for example expect the converse, in which young adults have less time to acquire toxicity than older adults. One major conclusion that we draw is that there are good reasons to consider within-species variation in defensive toxins as more than mere ecological noise. Rather there are a number of compelling evolutionary hypotheses which can explain and predict variation in prey toxicity.     

Intragroup and intragenomic conflict over chemical defense against predators

Insects are often chemically defended against predators. There is considerable evidence for a group‐beneficial element to their defenses, and an associated potential for individuals to curtail their own investment in costly defense while benefitting from the investments of others, termed “automimicry.” Although females in chemically defended taxa often lay their eggs in clusters, leading to siblings living in close proximity, current models of automimicry have neglected kin‐selection effects, which may be expected to curb the evolution of such selfishness. Here, we develop a general theory of automimicry that explicitly incorporates kin selection. We investigate how female promiscuity modulates intragroup and intragenomic conflicts overinvestment into chemical defense, finding that individuals are favored to invest less than is optimal for their group, and that maternal‐origin genes favor greater investment than do paternal‐origin genes. We translate these conflicts into readily testable predictions concerning gene expression patterns and the phenotypic consequences of genomic perturbations, and discuss how our results may inform gene discovery in relation to economically important agricultural products.