Intimate Rendezvous in a Tritrophic Context? Nothing but the Girls for Male Lysiphlebus testaceipes

In insects, mating often occurs after natal dispersal, and hence relies on a coevolved combination of sexual communication and movement allowing mate encounter. Volatile sex pheromones are widespread, generally emitted by females and triggering in‐flight orientation of conspecific males. In parasitoid wasps, unmated females can start laying unfertilized eggs via parthenogenesis so that host patches could serve as sites of rendezvous for mating. Males could therefore use cues associated with host patches to focus their search on females that have successfully found oviposition sites. We hypothesized that in parasitoids exploiting herbivorous hosts, sex pheromones, and herbivore‐induced plant volatiles (HIPV) should act in synergy, triggering male orientation toward ovipositing females. We tested this hypothesis with the aphid parasitoid Lysiphlebus testaceipes. Results from both field and laboratory experiments show that males are strongly attracted to virgin females, but that volatiles from aphid‐infested plants have no effect on male orientation, neither has a cue, nor in interaction with the female sex pheromone. The absence of synergy between sex pheromones and HIPV contrasts with results on other species and raises interesting questions on mating systems and sexual selection in parasitoid wasps.     

Preference and performance of the hyperparasitoid Syrphophagus aphidivorus (Hymenoptera: Encyrtidae): fitness consequences of selecting hosts in live aphids or aphid mummies

Abstract.  1. Theoretical models predict that ovipositional decisions of parasitoid females should lead to the selection of the most profitable host for parasitoid development. Most parasitoid species have evolved specific adaptations to exploit a single host stage. However, females of the aphid hyperparasitoid Syrphophagous aphidivorus (Mayr) (Hymenoptera: Encyrtidae) display a unique and atypical oviposition behaviour by attacking either primary parasitoid larvae in live aphids, or parasitoid pupae in dead, mummified aphids.
2. In the laboratory, the correlation between host suitability and host preference of S. aphidivorus on the host Aphidius nigripes Ashmead parasitising the aphid Macrosiphum euphorbiae (Thomas) was investigated.
3. The relative suitability of the two host stages was determined by measuring hyperparasitoid fitness parameters (survival, development time, fecundity, sex ratio, and adult size of progeny), and calculating the intrinsic rate of population increase ( r _m). Host preference by S. aphidivorus females and the influence of aphid defence behaviour on host selection was also examined.
4. Hyperparasitoid offspring performance was highest when developing from hosts in aphid mummies and females consistently preferred this host to hosts in parasitised aphids. Although aphid defensive behaviour may influence host selection, it was not a determining factor. Ecological and evolutionary processes that might have led to dual oviposition behaviour in S. aphidivorus are discussed.     

Patterns of diversity for aphidiine (Hymenoptera: Braconidae) parasitoid assemblages on aphids (Homoptera)

We used aphids (Aphidae) as a representative hemimetabolous host family to investigate patterns of parasitoid (Aphidiine) assemblage size. The aphidiine assemblages from 477 aphid species were used to estimate average assemblage size and the influence of eight ecological and taxonomic variables. Aphids species support an average of 1.7 aphidiine species. Aphid subfamily and invasion status (native or exotic) were the most important determinants of parasitoid richness, explaining 28% of the deviance in aphidiine assemblage size. Aphids within the largest aphid subfamily, the Aphidinae, support larger parasitoid assemblages than those in other subfamilies. Parasitoid diversity was also highest on exotic aphid hosts (within the Aphidinae) and on hosts in developed habitats (agricultural or urban), though the latter effect is weak. Patterns related to aphid food plant architecture were influenced by an interaction with aphid invasion status; parasitoid diversity drops with increasing architectural complexity on exotic aphids, whereas the diversities on native aphid hosts are similar on different plant types. Weak effects were also found for aphid food plant alternation (whether or not aphids switch hosts seasonally) and climate (annual range in temperature); alternating aphids support more parasitoids than non-alternating hosts, and parasitoid assemblage size is lowest in warm climates. Taxonomic isolation of aphids at the generic level showed no significant relationship with parasitoid diversity. Finally, in contrast to parasitoid assemblages on holometabolous hosts, sample size effects were weak for aphids, possibly due to the narrow host ranges of aphidiines. Received: 22 November 1997 / Accepted: 7 March 1998     

Herbivore-induced plant volatiles as cues for habitat assessment by a foraging parasitoid

1. Animals usually require information about the current state of their habitat to optimize their behaviour. For this, they can use a learning process through which their estimate is continually updated according to the cues they perceive. Identifying these cues is a long-standing but still inveterate challenge for ecologists. 2. The use of plant cues by aphid parasitoids for the assessment of habitat profitability and the adaptation of patch exploitation was studied. Grounding on predictions from optimal foraging theory, we tested whether parasitoids exploited host patches less intensively after visiting heavily infested plants than after visiting plants bearing fewer aphids. 3. As predicted, after visiting heavily infested plants parasitoids reduced their residence time and attacked fewer hosts in the next patch. This was the case regardless of whether the aphids were actually present on the first plant, indicating that the cue came from the plant. Moreover, the level of infestation of a plant at some distance from the first plant visited affected parasitoid patch exploitation on the second plant in a similar manner, indicating that the cue was volatile. 4. These results highlight a novel role of herbivore-induced volatiles in parasitoid foraging behaviour, different from the widely studied attraction at a distance.     

Foraging behaviour at the fourth trophic level: a comparative study of host location in aphid hyperparasitoids

In studies of foraging behaviour in a multitrophic context, the fourth trophic level has generally been ignored. We used four aphid hyperparasitoid species: Dendrocerus carpenteri (Curtis) (Hymenoptera: Megaspilidae), Asaphes suspensus Walker (Hymenoptera: Pteromalidae), Alloxysta victrix (Westwood) (Hymenoptera: Alloxystidae) and Syrphophagus aphidivorus (Mayr) (Hymenoptera: Encyrtidae), to correlate their response to different cues with their ecological attributes such as host range and host stage. In addition, we compared our results with studies of primary parasitoids on the same plant–herbivore system. First, the olfactory response of females was tested in a Y‐tube olfactometer (single choice: plant, aphid, honeydew, parasitised aphid, aphid mummy, or virgin female parasitoid; dual choice: clean plant, plant with aphids, or plant–host complex). Second, their foraging behaviour was described on plants with different stimuli (honeydew, aphids, parasitised aphids, and aphid mummies). The results indicated that olfactory cues are probably not essential cues for hyperparasitoid females. In foraging behaviour on the plant, all species prolonged their total visit time and search time as compared to the control treatment (clean plant). Only A. victrix did not react to the honeydew. Oviposition in mummies prolonged the total visit time because of the long handling time, but the effect of this behaviour on search time could not be determined. No clear correlation between foraging behaviour and host stage or host range was found. In contrast to specialised primary aphid parasitoids that have strong fixed responses to specific kairomones and herbivore‐induced synomones, more generalist aphid hyperparasitoids seem to depend less on volatile olfactory stimuli, but show similarities with primary parasitoids in their use of contact cues while searching on a plant.     

Females of Cotesia vestalis,a parasitoid of diamondback moth larvae,learn to recognise cues from aphid‐infested plants to exploit honeydew

1. To maximise their reproductive success, the females of most parasitoids must not only forage for hosts but must also find suitable food sources. These may be nectar and pollen from plants, heamolymph from hosts and/or honeydew from homopterous insects such as aphids. 2. Under laboratory conditions, females of Cotesia vestalis, a larval parasitoid of the diamondback moth (Plutella xylostella) which does not feed on host blood, survived significantly longer when held with cruciferous plants infested with non‐host green peach aphids (Myzus persicae) than when held with only uninfested plants. 3. Naïve parasitoids exhibited no preference between aphid‐infested and uninfested plants in a dual‐choice test, but those that had been previously fed aphid honeydew significantly preferred aphid‐infested plants to uninfested ones. 4. These results suggest that parasitoids that do not use aphids as hosts have the potential ability to learn cues from aphid‐infested plants when foraging for food. This flexible foraging behaviour could allow them to increase their lifetime reproductive success.     

The use of general foraging kairomones in a generalist parasitoid

Almost no comparative studies are available on the use of general and specific infochemical cues by generalist parasitoids with hosts from different families feeding on host plants also from different families. Based on literature, two hypotheses were developed and tested with host recognition cues used by the larval parasitoid Lariophagus distinguendus . This generalist parasitizes beetle species from different families developing in seeds of plant species from the Poaceae and Fabaceae. The first hypothesis predicts that for initial encounters with host species, natural enemies should innately use general cues, which are common to all hosts and their food plants. The second hypothesis predicts that natural enemies should learn specific cues from host plant and host after experience with a host species. The first hypothesis was partly confirmed. L. distinguendus innately reacted to faecal cues from several host species and chemical analyses of faeces from these hosts revealed the common occurrence of chemicals that are used for host recognition by L. distinguendus . In disagreement with the first hypothesis, parasitoids did not innately respond to cues from plant seeds. Preference experiments on the influence of experience demonstrated an increased host recognition response towards a host after experience with it. In support of the second hypothesis, L. distinguendus females learned specific cues from herbivore-damaged wheat, rice and cowpea seeds and from the faeces of the bean weevil Callosobruchus maculatus .     

Effect of synthetic and plant‐extracted aphid pheromones on the behaviour of Aphidius colemani

Parasitoid females use several chemical cues to locate hosts. A better knowledge of how they respond to a complex of these cues in a small range may help us to understand how to manipulate the parasitoids in the field. Here, the response of the aphid parasitoid Aphidius colemani to a mixture of odours of synthetic and plant‐extracted nepetalactone (a component of aphid sex pheromone) and to (E)‐β‐farnesene (aphid alarm pheromone) was investigated. The behavioural responses of A. colemani to three semiochemical groups with different concentrations were studied in a square arena. Parasitoid females were significantly attracted by the semiochemicals, when their concentrations were high, in which case the females spent more time in squares with semiochemicals. The majority of females preferred plant‐extracted nepetalactone, when it was in high concentration, but they consistently did not respond to (E)‐β‐farnesene.     

Host age and fitness-related traits in a koinobiont aphid parasitoid

Abstract.  1. Trade-offs play a key role in species evolution and should be found in host–parasitoid interactions where the host quality may differ between host age categories.
2. The braconid wasp, Aphidius ervi , is a solitary endoparasitoid that allows its aphid hosts to continue to feed and grow after parasitisation. The hypotheses that host age influences their quality and that female parasitoids exploit their hosts based on that quality were tested under laboratory conditions using no-choice tests.
3.  Aphidius ervi females accepted the aphid Myzus persicae for oviposition and their progeny developed successfully in all host ages. The fitness-related traits of parasitoids did not increase linearly with the host age in which they developed. Host quality was found to be optimal at intermediate host ages and the females preferred to parasitise these hosts. The shortest progeny development time and a more female-biased sex ratio were observed in hosts of intermediate age.
4. This study suggests the existence of multiple interactive trade-offs occurring during host–parasitoid interactions according to host age related quality.     

The role of plant chemical cues in determining host preference in the generalist aphid parasitoid Aphidius colemani

The host preference behaviour of the generalist aphid parasitoid Aphidius colemaniwas investigated using a Y-tube olfactometer. Female A. colemanishowed a preference for the host-plant complex on which they had been reared, even though the same aphid host was involved, demonstrating a host plant preference. This preference was not evident when the parasitoids were dissected from their mummies prior to adult emergence. Host plant preference exhibited during host selection appeared to be induced by chemical cues encountered on the mummy case at the time of emergence, but preferences could be changed by subsequent foraging experiences. It is concluded that plant chemical cues play a major role in determining initial preferences through a process of emergence conditioning but that learning processes, involving cues encountered during oviposition in or contact with the host, can modify these initial preferences.     

Within-patch foraging behaviour of the aphid parasitoidAphidius funebris: plant architecture, host behaviour, and individual variation

The influence of plant architecture, host colony size, and host colony structure on the foraging behaviour of the aphid parasitoidAphidius funebris Mackauer (Hymenoptera: Aphidiidae) was investigated using a factorial experimental design. The factorial design involved releasing individual parasitoid females in aphid colonies consisting of either 10 or 20 individuals ofUroleucon jaceae L. (Homoptera: Aphididae) of either only larval instar L3 or a mixture of host instars, both on unmanipulated plants and on plants that had all leaves adjacent to the colony removed. Interactions between the parasitoid and its host were recorded until the parasitoid had left the plant. The time females spent on the host plant and the number of eggs laid varied greatly among females. Host colony size significantly affected patch residence time and the number of contacts between parasitoids and aphids. Plant architecture influenced the time-budget of the parasitoids which used leaves adjacent to the aphid colony for attacking aphids. Female oviposition rate was higher on unmanipulated plants than on manipulated plants. No further significant treatment effects on patch residence time, the number of contacts, attacks or ovipositions were found. Oviposition success ofA. funebris was influenced by instar-specific host behaviour. Several rules-of-thumb proposed by foraging theory did not account for parasitoid patch-leaving behaviour.     

Survival to Parasitoids in an Insect Hosting Defensive Symbionts: A Multivariate Approach to Polymorphic Traits Affecting Host Use by Its Natural Enemy

Insect parasitoids and their insect hosts represent a wide range of parasitic trophic relations that can be used to understand the evolution of biotic diversity on earth. Testing theories of coevolution between hosts and parasites is based on factors directly involved in host susceptibility and parasitoid virulence. We used controlled encounters with potential hosts of the Aphidius ervi wasp to elucidate behavioral and other phenotypic traits of host Acyrthosiphon pisum that most contribute to success or failure of parasitism. The host aphid is at an advanced stage of specialization on different crop plants, and exhibits intra-population polymorphism for traits of parasitoid avoidance and resistance based on clonal variation of color morph and anti-parasitoid bacterial symbionts. Randomly selected aphid clones from alfalfa and clover were matched in 5 minute encounters with wasps of two parasitoid lineages deriving from hosts of each plant biotype in a replicated transplant experimental design. In addition to crop plant affiliation (alfalfa, clover), aphid clones were characterized for color morph (green, pink), Hamiltonella defensa and Regiella insecticola symbionts, and frequently used behaviors in encounters with A. ervi wasps. A total of 12 explanatory variables were examined using redundancy analysis (RDA) to predict host survival or failure to A. ervi parasitism. Aphid color was the best univariate predictor, but was poorly predictive in the RDA model. In contrast, aphid host plant and symbionts were not significant univariate predictors, but significant predictors in the multivariate model. Aphid susceptibility to wasp acceptance as reflected in host attacks and oviposition clearly differed from its suitability to parasitism and progeny development. Parasitoid progeny were three times more likely to survive on clover than alfalfa host aphids, which was compensated by behaviorally adjusting eggs invested per host. Strong variation of the predictive power of intrinsic (body color) and extrinsic traits (symbionts, host plant), indicate that host variables considered as key predictors of outcomes strongly interact and cannot be considered in isolation.     

Influence of aphid size,age and behaviour on host choice by the parasitoid wasp Ephedrus californicus: a test of host-size models

Summary When host quality varies, parasitoid wasps are expected to oviposit selectively in high-quality hosts. We tested the assumption underlying host-size models that, for solitary species of wasps, quality is based on host size. Using Ephedrus californicus, a solitary endoparasitoid of the pea aphid, we evaluated the influence of aphid size (= mass), age and defensive behaviours on host selection. Experienced parasitoid females were given a choice among three classes of 5-day-old apterous nymphs: small aphids that had been starved daily for 4 h (S4) and 6 h (S6) respectively, and large aphids permitted to feed (F) normally. Wasps attacked more, and laid more eggs in, small than large aphids (S6>S4>F). This rank-order for attack did not change when females could choose among aphids of the same size that differed in age; however, wasps oviposited in all attacked aphids with equal probability. Host size did not influence parasitoid attack rates when aphids were anaesthetized so that they could not escape or defend themselves. As predicted by host-size models, wasp size increased with host size (F>S4; S6), but large wasps required longer to complete development than their smaller counterparts (S4E. californicus reflects a trade-off between maximization of fitness gains per egg and the economics of search-time allocation. Because large aphids are more likely to escape parasitization, a wasp must balance her potential gain in fitness by ovipositinng in a high-quality (large) aphid against her potential cost in terms of lost opportunity time if the attack fails.     

Beneficial arthropod behavior mediated by airborne semiochemicals. VIII. Learning of host-related odors induced by a brief contact experience with host by-products inCotesia marginiventris (Cresson), a generalist larval parasitoid

Females of Cotesia marginiventris(Cresson), a generalist larval parasitoid, were observed to respond to host related odors in a four-arm olfactometer. The females were significantly more responsive to the odors after a brief contact experience with host-damaged leaves contaminated with host by products. During the experience, actual encounters with hosts were not required to improve subsequent responses to host-related odors. The response to odors of the plant-host complex with which parasitoids had experience was significantly higher than the response to odors of an alternative plant-host complex. This suggests that the experience effect is due, at least partly, to associative learning. We suspect that females of this generalist parasitoid, as was recently found for those of a specialist, recognize specific semiochemicals when they contact frass of suitable host larvae. The parasitoids, subsequently, associate the surrounding odors with the possible presence of hosts, and use these odors as cues in their search for more hosts. This could be an important component in the host-searching behavior of many parasitoids.Mention of a proprietary product does not constitute an endorsement or the recommendation for its use by the USDA.     

Infection with an insect virus affects olfactory behaviour and interactions with host plant and natural enemies in an aphid

Aphid ecology and population dynamics are affected by a series of factors including behavioural responses to ecologically relevant chemical cues, capacity for population growth, and interactions with host plants and natural enemies. Using the aphid Rhopalosiphum padi (L.) (Homoptera: Aphididae), we showed that these factors were affected by infection with Rhopalosiphum padi virus (RhPV). Uninfected aphids were attracted to odour of uninfected aphids on the host plant, an aggregation mechanism. However, infected aphids were not attracted, and neither infected nor uninfected aphids were attracted to infected aphids on the plant. Infected aphids did not respond to methyl salicylate, a cue denoting host suitability. Infected aphids were more behaviourally sensitive to aphid alarm pheromone, and left the host plant more readily in response to it. RhPV reduced the lifespan and population growth rate of the aphid. The predacious ladybird, Coccinella septempunctata (L.) (Coleoptera: Coccinellidae), consumed more infected aphids than uninfected aphids in a 24‐h period, and the aphid parasitoid Aphidius ervi Haliday (Hymenoptera: Aphidiidae) attacked more infected than uninfected aphids. However, the proportion of mummies formed was lower with infected aphids. The results represent further evidence that associated organisms can affect the behaviour and ecology of their aphid hosts.     

Quality of different aphids species as hosts for the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae)

The suitability of Macrosiphum euphorbiae (Thomas), Aulacorthum solani (Kaltenbach) and Acyrthosiphon kondoi Shinji (Hemiptera: Aphididae) as hosts for the aphid parasitoid Aphidius ervi Haliday was evaluated by assessing host size, host preference, and host quality. Tests were carried out in an environmental chamber at 22±1oC, 70±10% RH and 12h photophase. Replicates (11) consisted of one 24h-old mated female of A. ervi without a previous oviposition experience. Female was released into a Petri dish (5 cm) with 20 2nd and 3rd instars of one of each aphid species tested on a leaf disc of the host plant onto a 1% water-agar layer. Parasitoid emergency was lower in A. kondoi (78.7%) compared to M. euphorbiae (92.2%) and A. solani (91.7%). Acyrthosiphon kondoi (0.36 mm) was the smallest host. The parasitoid showed preference (74.0% parasitism) for M. euphorbiae, the largest host (hind tibia length=0.73 mm), which in turn yielded larger A. ervi females (0.75 mm).     

Development of the aphid parasitoid,Aphidius ervi, in asexual and sexual females of the pea aphid,Acyrthosiphon pisum, and the blackberry-cereal aphid,Sitobion fragariae

The aphid parasitoid,Aphidius ervi Haliday, overwinters in larval diapause. The possibility that the parasitoid might prefer sexual (oviparae) rather than asexual females (virginoparae) as overwintering hosts (oviparae predominate in autumn when host numbers are generally declining) was tested by comparing these aphid morphs as potential hosts. Two host species were also examined, the pea aphid,Acyrthosiphon pisum (Harris), and the blackberry aphid,Sitobion fragariae (Walker). The parasitoids took longer to develop inS. fragariae than inA. pisum but the development of non-diapausingA. ervi was similar in sexual and asexual females. This observation, together with the greater variation in the duration of the different parasitoid stadia inS. fragariae, indicated that the parasitoid is specialized on the pea aphid. In photophases of 12 h and longer, the proportion ofA. ervi entering diapause inA. pisum oviparae was higher than in virginoparae. The critical daylength (where 50% of parasitoids entered diapause) was therefore longer in oviparae (12.6 h) than in virginoparae (11.7 h) with the inference that parasitoids developing in the oviparae would enter diapause earlier in the field. InS. fragariae, critical day-lengths were similar in both aphid morphs. The duration of diapause was unaffected by host morph and emergence in short days (10:14 L:D) occurred over a long period (c. 60 days).     

Superparasitism limitation in an aphid parasitoid: cornicle secretion avoidance and host discrimination ability

Superparasitism avoidance by the endoparasitoid Aphidius rhopalosiphi De Stefani Perez on the grain aphid, Sitobion avenae was studied. Experiments were carried out in which aphids were exposed to two consecutive attacks by parasitoids. Results showed that superparasitism avoidance in A. rhopalosiphi was mediated by two successive stimuli whose effectiveness depended on the time interval between attacks. For short time intervals (<16 h), host rejections were mainly associated with the presence of dried cornicle secretion on the host's body which was exuded during the first attack. The repellency of this secretion declined with the time interval between attacks, becoming ineffective 2 days after the first parasitization, and allowed females to reject up to 30% of parasitized hosts. For longer time intervals (>/=16 h), host rejection behavior was a response of parasitoid females to internal changes in host quality associated with parasite development. This response gradually increased with an increase in time interval, reaching no more than 60%, 96 h after initial parasitization. This host discrimination ability did not allow females to distinguish between hosts parasitized by themselves or by conspecifics. Consequently, these findings suggest that superparasitism is a common event in A. rhopalosiphi and especially on recently parasitized hosts.     

Volatile cues used by the parasitoid, Aphytis melinus, for host location: California red scale revisited

Aphytis melinus DeBach (Hymenoptera: Aphelinidae) is a biological control agent of diaspidid scale insects. The parasitoid has a narrow host range but its hosts are polyphagous. We determined the source of volatile cues the wasp uses to locate its few host species when those hosts occur on more than one host plant species. We addressed four questions in regard to the use of volatile cues in host location of California red scale, Aonidiella aurantii (Maskell) (Homoptera: Diaspididae): (1) Does A. melinus use volatile cues to assist in host location? (2) Are these cues innately recognized or learned? (3) Are cues produced by female California red scale, or from other sources? (4) Are the cues specific to the host or host plant? These questions were tested through the use of a Y-tube olfactometer. Female A. melinus used volatile cues to orient toward both infested and uninfested host plant material. Wasps learned these cues by associating odors from the host plant with host presence. They had no innate preferences for scale insect or host plant volatile stimuli. Contrary to previous studies, we found no evidence of orientation toward the female-produced sex pheromone of California red scale, nor to volatile cues from the attacked host stage. Wasps given experience with scale insects growing on lemon fruit subsequently oriented toward lemon and orange fruit and leaves. The scale species with which the wasp was given experience did not affect this preference. Wasps given experience with California red scale growing on squash did not orient toward infested lemon fruit. The host ranges of the parasitoid and its hosts are used to explain the adaptive value for the evolution of learned rather than fixed responses to cues used in foraging behavior.     

Asymmetry in host and parasitoid diffuse coevolution: when the red queen has to keep a finger in more than one pie

BACKGROUND: Coevolution between pairs of antagonistic species is generally considered an endless "arms race" between attack and defense traits to counteract the adaptive responses of the other species. PRESENTATION OF THE HYPOTHESIS: When more than two species are involved, diffuse coevolution of hosts and parasitoids could be asymmetric because consumers can choose their prey whereas preys do not choose their predator. This asymmetry may lead to differences in the rate of evolution of the antagonistic species in response to selection. The more long-standing the coevolution of a given pair of antagonistic populations, the higher should be the fitness advantage for the consumer. Therefore, the main prediction of the hypothesis is that the consumer trophic level is more likely to win the coevolution race. TESTING THE HYPOTHESIS: We propose testing the asymmetry hypothesis by focusing on the tritrophic system plant/aphid/aphid parasitoid. The analysis of the genetic variability in the virulence of several parasitoid populations and in the defenses of several aphid species or several clones of the same aphid species could be compared. Moreover, the analysis of the neutral population genetic structure of the parasitoid as a function of the aphid host, the plant host and geographic isolation may complement the detection of differences between host and parasitoid trophic specialization. IMPLICATIONS OF THE HYPOTHESIS: Genetic structures induced by the arms race between antagonistic species may be disturbed by asymmetry in coevolution, producing neither rare genotype advantages nor coevolutionary hotspots. Thus this hypothesis profoundly changes our understanding of coevolution and may have important implications in terms of pest management.