Influence of cornicle droplet secretions of the cabbage aphid,Brevicoryne brassicae,on parasitism behavior of na＇fve and experienced Diaeretiella rapae

Insects have evolved amazing methods of defense to ward off enemies. Many aphids release cornicle secretions when attacked by predators and parasitoids. These se cretions contain an alarm pheromone that alerts other colony members of danger, thereby providing indirect fitness benefits to the releaser. In addition, contact with cornicle se cretions could also threaten an attacker and could provide direct fitness to the releaser. However, cornicle secretions may also be recruited as a kairomonal cue by aphid natural enemies. In this study, we investigated the effect of the cornicle droplet volatiles of the cabbage aphid, Brevicoryne brassicae （L.）, on the hostsearching behavior of naive and experienced female Diaeretiella rapae （M＇Intosh） parasitoids in olfactometer studies. In addition, we evaluated the role ofB. brassicae cornicle droplets on the oviposition prefer ence of the parasitoid in a twochoice bioassay. Naive females did not exhibit any preference between volatiles from aphids secreting cornicle droplets over nonsecreting aphids, while experienced parasitoids exploited the secretions in their host location. Experienced females were also able to choose volatiles from both secreting and nonsecreting aphids over clean air, while this ability was not observed in naive females. Although secretion of cornicle droplets did not influence the percentage of first attack in either naive or experienced females, the success of attack （i.e. resulting in a larva） was significantly different between secreting and nonsecreting aphids in the case of experienced parasitoids.     

Soybean Aphid Response to their Alarm Pheromone E-ß-Farnesene (EBF)

When attacked by natural enemies some insect pests, including many aphid species, alert neighboring conspecifics with alarm pheromones. Cornicle secretions with pheromones benefit the attacked aphid but are costly to produce, while alarm pheromone benefits probably fall largely on alerted conspecifics. Given these variable benefits, the likelihood of a secretion may change depending on aphid density. Thus, we first hypothesized that the common alarm pheromone in aphids, E-ß-farnesene (EBF), was present in soybean aphid (Aphis glycines Matsumura) cornicle secretions and would elicit an alarm response in aphids exposed to it. Second, since aphids other than the secretor also benefit from cornicle secretions, we hypothesized that the likelihood of secretion would increase concurrently with the density of neighboring clonal conspecifics. Third, because alarm reaction behavior (e.g. feeding cessation) is probably costly, we hypothesized that alarm reaction behavior would decrease as conspecific density (i.e. alternative prey for an attacking natural enemy) increased. We found that soybean aphids 1) produce cornicle secretions using EBF as an alarm pheromone, 2) are less likely to release cornicle secretions when alone than in a small group (~10 individuals), but that the rate of secretion does not increase further with additional conspecific density, and 3) also exhibit alarm reaction behavior in response to cornicle secretions independent of aphid density. We show that soybean aphids can use their cornicle secretions to warn their neighbors of probable attack by natural enemies, but that both secretion and alarm reaction behavior does not change as density of nearby conspecifics rises above a few individuals.     

Direct vs. inclusive fitness in the evolution of aphid cornicle length

By comparing the relative sizes of anatomical structures among phenotypes, selective pressures that shape species' morphologies can be evaluated. Aphids emit droplets containing an alarm pheromone/defensive secretion from unique anatomical structures called cornicles, upon being attacked. As aphids live in colonies of high relatedness, it is uncertain whether direct or inclusive fitness benefits have chiefly promoted cornicle evolution. Morphological measurements for apterous parthenogen, alate parthenogen, female sexual and male sexual morphs of 43 species (21 genera, one subfamily) were assessed to distinguish between the hypotheses that: (1) cornicles evolved for mechanical defence against natural enemies (direct fitness); (2) cornicles evolved for alarm signalling (inclusive fitness); or (3) cornicle length has been largely constrained by flight aerodynamics. Our results generally support the inclusive fitness hypothesis; cornicle length decreases as the relative number and relatedness of offspring decreases. As cornicle length is greatest in apterous parthenogenetic morphs, inclusive fitness benefits of protecting highly related kin may have been a key factor selecting for cornicles, and increased cornicle length, in aphids.     

Cornicle length in Macrosiphini aphids: a comparison of ecological traits

Abstract 1. Aphids often emit cornicle droplets when attacked by predators. While the function of cornicle droplets has long been debated (i.e. mechanical protection vs. chemical signalling), it is not understood why aphid species have cornicles of different lengths.
2. It was hypothesised that aphids living in more scattered colonies have longer cornicles to scent-mark predators with cornicle droplets containing alarm pheromone, so that clone-mates are provided with advanced warning of a threat, even if not at the predation site. To test this hypothesis, multiple regression analyses were used, due to a lack of phylogenetic information on these taxa, to address which ecological traits (amount of wax on an aphid, degree of colony aggregation, feeding shelter, ant attendance) are correlated with cornicle length.
3. Aphids living in dense colonies tended to have shorter cornicles than aphids living in more scattered colonies. Also, aphids with more protection (i.e. wax) on their bodies had shorter cornicles. Aphids also tended to have shorter cornicles when tended by ants. The presence of a feeding shelter was not a good predictor of cornicle length.
4. It is suggested that longer cornicles function to scent-mark predators with alarm pheromone to increase the inclusive fitness of a clone; however the negative correlation between the amount of individual protection, and also ant attendance, and cornicle length argues for a trade-off between different forms of defence.     

Has the Attraction of Predatory Coccinellids to Cornicle Droplets Constrained Aphid Alarm Signaling Behavior?

When attacked by a predator, aphids of many species secrete cornicle droplets, containing an alarm pheromone, that results in the dispersal of nearby conspecifics. As females are parthenogenetic, alarm signaling functions to enhance the survival of clone-mates. Enigmatically, however, aphids are physically able to, but usually do not emit alarm pheromone when initially detecting a predator, but rather signal only when captured by a predator. We hypothesized that cornicle droplets may be attractive to natural enemies and result in an increased risk of predation for the signaler, thereby selecting for prudent alarm signalers. We tested this hypothesis by investigating the olfactory cues that the multicolored Asian ladybird beetle, Harmonia axyridis Pallas, uses to locate pea aphids, Acyrthosiphon pisum. In choice tests, H. axyridis were attracted to odors from pea aphid colonies, whether feeding or not feeding on a host plant leaf, but were not attracted to cornicle droplets containing alarm pheromone. Further, individual pea aphids emitting cornicle droplets were not located more often or in a shorter period of time by beetles than aphids not emitting cornicle droplets. Thus, the cost of emitting early alarm signals is not prohibitively high in regards to the attraction of predators such as H. axyridis.     

Body size affects host defensive behavior and progeny fitness in a parasitoid wasp,Lysiphlebus fabarum

This study tested effects of maternal body size on foraging behavior and progeny development in a thelytokous population of Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae). Small and large wasps were reared from first and second instar hosts [black bean aphid, Aphis fabae Scopoli (Hemiptera: Aphididae)], respectively, and each was provided with a patch (bean leaf disk) containing either 15 small (second instar) or 15 large (fourth instar) hosts for a 30‐min foraging period. Neither body size nor host size affected time allocation to various behaviors within a patch, but second instar aphids produced significantly more mummies than fourth instars. The preferred attack orientation was from the side of the aphid, suggesting wasps were sensitive to the risk of smearing with cornicle secretions. Few wasps developed in fourth instar hosts, suggesting later host instars were somewhat resistant to parasitism. Second instar hosts, the most suitable stage for L. fabarum development, relied more on defensive behavior, specifically kicking and secreting cornicle droplets. Large wasps were more likely to elicit a double cornicle secretion, indicating that aphids graded their response to the size of the attacker. Larger wasps were also more likely to be smeared with cornicle secretion, suggesting they were more vulnerable than small wasps. Although small wasps had smaller eggs than large wasps, there was no effect of maternal egg size on the size of progeny. However, daughters of small females emerged with larger egg loads than daughters of large mothers, and their eggs tended to be slightly smaller, although not significantly. Regression analysis revealed a positive correlation between maternal egg size and progeny developmental time for small and large wasps, and between maternal egg size and progeny egg load for small wasps. These results confirm maternal effects of body size in an aphid parasitoid, and reveal that vulnerability to host behavioral defenses is also body size dependent.     

Symbiont infection affects aphid defensive behaviours

Aphids harbour both an obligate bacterial symbiont, Buchnera aphidicola, and a wide range of facultative ones. Facultative symbionts can modify morphological, developmental and physiological host traits that favour their spread within aphid populations. We experimentally investigated the idea that symbionts may also modify aphid behavioural traits to enhance their transmission. Aphids exhibit many behavioural defences against enemies. Despite their benefits, these behaviours have some associated costs leading to reduction in aphid reproduction. Some aphid individuals harbour a facultative symbiont Hamiltonella defensa that provides protection against parasitoids. By analysing aphid behaviours in the presence of parasitoids, we showed that aphids infected with H. defensa exhibited reduced aggressiveness and escape reactions compared with uninfected aphids. The aphid and the symbiont have both benefited from these behavioural changes: both partners reduced the fitness decrements associated with the behavioural defences. Such symbiont-induced changes of behavioural defences may have consequences for coevolutionary processes between host organisms and their enemies.     

Wingless virgin queens assume helper roles in Acromyrmex leaf-cutting ants

Division of labour is the hallmark of advanced societies, because specialization carries major efficiency benefits in spite of costs owing to reduced individual flexibility [1]. The trade-off between efficiency and flexibility is expressed throughout the social insects, where facultative social species have small colonies and reversible caste roles and advanced eusocial species have permanently fixed queen and worker castes. This usually implies that queens irreversibly specialize on reproductive tasks [2]. Here, we report an exception to this rule by showing that virgin queens (gynes) of the advanced eusocial leaf-cutting ant Acromyrmex echinatior switch to carrying out worker tasks such as brood care and colony defence when they fail to mate and disperse. These behaviours allow them to obtain indirect fitness benefits (through assisting the reproduction of their mother) after their direct fitness options (their own reproduction) have become moot. We hypothesize that this flexibility could (re-)evolve secondarily because these ants only feed on fungal mycelium and thus could not benefit from cannibalising redundant gynes, and because queens have retained behavioural repertoires for foraging, nursing, and defense, which they naturally express during colony founding.     

A comparison of triglycerides from aphids and their cornicle secretions

Direct mass spectrometry of extracts showed that body triglycerides from 30 species of aphids contained the same fatty acid radicals, C₆ (hexanoyl), C_6:2 (sorboyl), C₁₄ (myristoyl), and C₁₆ (palmitoyl) as did the cornicle secretions, but in many species the proportions of hexanoyl and/or palmitoyl triglycerides were greater in the body. When cornicle secretions were collected progressively so as to draw increasingly upon body fat reserves, their composition changed gradually towards that of the body extracts.All summer forms of Myzus persicae had similar body triglycerides, even when selected for resistance to organophosphorus insecticides, or bred for 3 months on an artificial diet. The composition of body triglycerides was also independent of colour in two aphid species in which pink and green forms were compared.Body extracts contain enough triglycerides for their composition to be determined in single aphids and the use of body extracts allows examination of aphids lacking cornicles and of specimens that do not give cornicle secretion because of low body turgor. Although, as in the case of cornicle secretions, the triglyceride composition of body extracts was not well correlated with taxonomic position, body extracts provide a second chemical characteristic that can be used to define a particular species.     

Greenbugs [Hom.: Aphididae] forced from host plants byLysiphlebus Testaceipes [Hym.; Braconidae]

In a laboratory study 150 sorghum plants were infested with greenbugs,Schizaphis graminum (Rondani), of ages 1, 3, and 5 days in densities of 5, 10, and 20 aphids per plant. Seventy-five of these infested plants were exposed to mated femaleLysiphlebus testaceipes (Cresson), and the number of aphids leaving each plant in a 4-hr period was recorded. Of the 75 plants exposed to parasitoids, an average of 41.0% of the aphids left the plants, compared to 0.9% from the 75 control plants. Twenty-six of the 75 parasitoids used in the experiment were inactive in the presence of aphids, showing no interest in searching for hosts. The number of inactive parasitoids was inversely related to the number of aphids per plant. When only those plants exposed to active parasitoids were considered, an average of 62.8% of the aphids left. To determine the fate of greenbugs leaving plants on hot, sunny, summer days, a small field test was performed in which greenbugs were knocked from plants onto soil exposed to direct sunlight. Air temperature was ca. 29°C and soil temperatures ranged from 45°C to 54°C. Twenty-four greenbugs were knocked to the soil, and all of them ceased activity within 10 seconds and were apparently dead.     

Specialised placement of morphs within the gall of the social aphid <Emphasis Type="Italic">Pemphigus spyrothecae</Emphasis>

Background  

The strategic placement and aggregation of certain castes within the nests of eusocial insects such as bees and ants results in complex colonies that enjoy increased fitness through improved efficiency of social tasks. To examine if this advanced social phenomenon might apply to social aphids, the location of the numerous morphs within the nests (plant galls) of the aphid species Pemphigus spyrothecae was examined.     

Direct and indirect interactions involving ants, insect herbivores, parasitoids, and the host plant Baccharis dracunculifolia (Asteraceae)

Abstract.  1. The relative importance of direct and indirect interactions in controlling organism abundance is still an unresolved question. This study investigated the role of the direct and indirect interactions involving ants, aphids, parasitoids, and the host plant Baccharis dracunculifolia (Asteraceae) on a galling herbivore Baccharopelma dracunculifoliae (Homoptera: Psyllidae).
2. The effects of these interactions on the galling herbivore's performance were evaluated by an exclusion experiment during two consecutive generations of the galling insect.
3. Ants had a direct negative effect on the performance of the galling herbivore by reducing the number of nymphs per gall. In contrast, ants had no indirect effects on gall mortality through the associated parasitoids.
4. Aphids negatively affected gall development, suggesting that galls and aphids might be partitioning photoassimilates and nutrients moving throughout host-plant tissues.
5. In addition, galls that developed during the rainy season were heavier, indicating that variation in the host plant, due to weather changes, can affect the development of B. dracunculifoliae galls. However, variation in the development of B. dracunculifoliae galls due to presence of aphids or the weather changes did not affect parasitoid attack.
6. These results suggest that direct interactions between ants and galls influenced galling insect abundance, whereas numerical indirect effects involving galling insects, ants, aphids, and host plants were less conspicuous.     

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.     

Prosocial primates: selfish and unselfish motivations

Non-human primates are marked by well-developed prosocial and cooperative tendencies as reflected in the way they support each other in fights, hunt together, share food and console victims of aggression. The proximate motivation behind such behaviour is not to be confused with the ultimate reasons for its evolution. Even if a behaviour is ultimately self-serving, the motivation behind it may be genuinely unselfish. A sharp distinction needs to be drawn, therefore, between (i) altruistic and cooperative behaviour with knowable benefits to the actor, which may lead actors aware of these benefits to seek them by acting cooperatively or altruistically and (ii) altruistic behaviour that offers the actor no knowable rewards. The latter is the case if return benefits occur too unpredictably, too distantly in time or are of an indirect nature, such as increased inclusive fitness. The second category of behaviour can be explained only by assuming an altruistic impulse, which—as in humans—may be born from empathy with the recipient''s need, pain or distress. Empathy, a proximate mechanism for prosocial behaviour that makes one individual share another''s emotional state, is biased the way one would predict from evolutionary theories of cooperation (i.e. by kinship, social closeness and reciprocation). There is increasing evidence in non-human primates (and other mammals) for this proximate mechanism as well as for the unselfish, spontaneous nature of the resulting prosocial tendencies. This paper further reviews observational and experimental evidence for the reciprocity mechanisms that underlie cooperation among non-relatives, for inequity aversion as a constraint on cooperation and on the way defection is dealt with.     

Chemical defence,offence and alliance in ants–aphids–ladybirds relationships

Chemicals, which mediate the interactions between aphids, ladybirds and ants, are reviewed. Special emphasis is laid on autogenous and plant-derived chemical defence in aphids and ladybirds. Evidences for chemical cues used during foraging and oviposition in ladybirds are assessed. Possible mutualistic interaction between plants and the third trophic level is illustrated by the as yet few reports of indirect plant-defence volatiles induced by aphids or coccids attracting parasitoids or ladybirds. The use of chemical signals allowing aphid parasitoids or ladybirds to squeeze into ant–aphid mutualistic association is briefly described. Questions are raised and hypotheses suggested which could stimulate further research on aphid host-plant influence on ladybird foraging behaviour and fitness, and on the cues used by aphid-web partners for their mutual recognition.     

Ploidy of the eusocial beetle Austroplatypus incompertus (Schedl) (Coleoptera, Curculionidae) and implications for the evolution of eusociality

In the hymenopterans, haplodiploidy, leading to high-genetic relatedness amongst full sisters has been regarded as critical to kin selection and inclusive fitness hypotheses that explain the evolution of eusociality and altruistic behaviours. Recent evidence for independent origins of eusociality in phylogenetically diverse taxa has led to the controversy regarding the general importance of relatedness to eusociality and its evolution. Here, we developed a highly polymorphic microsatellite marker to test whether the eusocial ambrosia beetle Austroplatypus incompertus (Schedl) is haplodiploid or diplodiploid. We found that both males and females of A. incompertus are diploid, signifying that altruistic behaviour resulting from relatedness asymmetries did not play a role in the evolution of eusocialty in this species. This provides additional evidence against the haplodiploidy hypothesis and implicates alternative hypotheses for the evolution of eusociality.     

Beyond promiscuity: mate-choice commitments in social breeding

Obligate eusociality with distinct caste phenotypes has evolved from strictly monogamous sub-social ancestors in ants, some bees, some wasps and some termites. This implies that no lineage reached the most advanced form of social breeding, unless helpers at the nest gained indirect fitness values via siblings that were identical to direct fitness via offspring. The complete lack of re-mating promiscuity equalizes sex-specific variances in reproductive success. Later, evolutionary developments towards multiple queen-mating retained lifetime commitment between sexual partners, but reduced male variance in reproductive success relative to female''s, similar to the most advanced vertebrate cooperative breeders. Here, I (i) discuss some of the unique and highly peculiar mating system adaptations of eusocial insects; (ii) address ambiguities that remained after earlier reviews and extend the monogamy logic to the evolution of soldier castes; (iii) evaluate the evidence for indirect fitness benefits driving the dynamics of (in)vertebrate cooperative breeding, while emphasizing the fundamental differences between obligate eusociality and cooperative breeding; (iv) infer that lifetime commitment is a major driver towards higher levels of organization in bodies, colonies and mutualisms. I argue that evolutionary informative definitions of social systems that separate direct and indirect fitness benefits facilitate transparency when testing inclusive fitness theory.     

When is bigger better? The effects of group size on the evolution of helping behaviours

Understanding the evolution of sociality in humans and other species requires understanding how selection on social behaviour varies with group size. However, the effects of group size are frequently obscured in the theoretical literature, which often makes assumptions that are at odds with empirical findings. In particular, mechanisms are suggested as supporting large‐scale cooperation when they would in fact rapidly become ineffective with increasing group size. Here we review the literature on the evolution of helping behaviours (cooperation and altruism), and frame it using a simple synthetic model that allows us to delineate how the three main components of the selection pressure on helping must vary with increasing group size. The first component is the marginal benefit of helping to group members, which determines both direct fitness benefits to the actor and indirect fitness benefits to recipients. While this is often assumed to be independent of group size, marginal benefits are in practice likely to be maximal at intermediate group sizes for many types of collective action problems, and will eventually become very small in large groups due to the law of decreasing marginal returns. The second component is the response of social partners on the past play of an actor, which underlies conditional behaviour under repeated social interactions. We argue that under realistic conditions on the transmission of information in a population, this response on past play decreases rapidly with increasing group size so that reciprocity alone (whether direct, indirect, or generalised) cannot sustain cooperation in very large groups. The final component is the relatedness between actor and recipient, which, according to the rules of inheritance, again decreases rapidly with increasing group size. These results explain why helping behaviours in very large social groups are limited to cases where the number of reproducing individuals is small, as in social insects, or where there are social institutions that can promote (possibly through sanctioning) large‐scale cooperation, as in human societies. Finally, we discuss how individually devised institutions can foster the transition from small‐scale to large‐scale cooperative groups in human evolution.     

The evolution of trans-generational altruism: kin selection meets niche construction

A cornerstone result of sociobiology states that limited dispersal can induce kin competition to offset the kin selected benefits of altruism. Several mechanisms have been proposed to circumvent this dilemma but all assume that actors and recipients of altruism interact during the same time period. Here, this assumption is relaxed and a model is developed where individuals express an altruistic act, which results in posthumously helping relatives living in the future. The analysis of this model suggests that kin selected benefits can then feedback on the evolution of the trait in a way that promotes altruistic helping at high rates under limited dispersal. The decoupling of kin competition and kin selected benefits results from the fact that by helping relatives living in the future, an actor is helping individuals that are not in direct competition with itself. A direct consequence is that behaviours which actors gain by reducing the common good of present and future generations can be opposed by kin selection. The present model integrates niche-constructing traits with kin selection theory and delineates demographic and ecological conditions under which altruism can be selected for; and conditions where the 'tragedy of the commons' can be reduced.     

Radio-tagging technology reveals extreme nest-drifting behavior in a eusocial insect

Kin-selection theory underlies our basic understanding of social evolution [1, 2]. Nest drifting in eusocial insects (where workers move between nests) presents a challenge to this paradigm, since a worker should remain as a helper on her natal colony, rather than visit other colonies to which she is less closely related. Here we reveal nest drifting as a strategy by which workers may maximize their indirect fitness by helping on several related nests, preferring those where the marginal return from their help is greatest. By using a novel monitoring technique, radio frequency identification (RFID) tagging, we provide the first accurate estimate of drifting in a eusocial insect: 56% of females drifted in a natural population of the eusocial paper wasp Polistes canadensis, exceeding previous records of drifting in natural populations by more than 30-fold. We demonstrate that drifting cannot be explained through social parasitism, queen succession, mistakes in nest identity, or methodological bias. Instead, workers appear to gain indirect fitness benefits by helping on several related colonies in a viscous population structure. The potential importance of this strategy as a component of the kin-selected benefits for a social insect worker has previously been overlooked because of methodological difficulties in quantifying and studying drifting.