Production Of Winged Offspring Research Articles

Fight or Flight? Alternative Defense of the Pea Aphids, Acyrthosiphon pisum on Different Host Plants.

Simple SummaryIn the event of a pathogen attack, fecundity compensation and production of winged offspring are critical in pea aphids. However, little is known about the effects of the host plant on these responses. The purpose of this study was to investigate the effects of host plant on these two alternative defenses in pea aphids. We took a single adult female from a pink colony of pea aphids that was originally from broad beans and allowed her to reproduce offspring in the laboratory. Some offspring were fed broad beans, while others were fed alfalfa for over 30 generations. We first investigated the backgrounds of their facultative symbionts before infecting them with pathogens and found that the composition of secondary symbionts in our aphid colony was not affected by the host plants. Broad bean reared pea aphids produced more offspring in infected and uninfected conditions, whereas alfalfa reared pea aphids produced more winged offspring when confronting challenges caused by Staphylococcus aureus and Beauveria bassiana. Our findings showed that the host plant influences the pea aphid’s alternative responses to mortality risks.Non-immunological responses are important alternative strategies for animals to deal with pathogens. It has long been recognized that fecundity compensation and production of winged offspring are two common non-immunological responses used by aphids when confronted with predators or pathogens. However, the effects of host plant on these responses have received little attention. This study investigated the effects of host plant on non-immunological defense in the pea aphids, Acyrthosiphon pisum, after bacterial and fungal infections. The aphids were raised in two groups, with one group being raised on broad beans and the other group being raised on alfalfa. The secondary symbiont background was examined, and the aphids were then infected with bacteria and fungus to assess fecundity and winged offspring production. We found that aphids that had been fed alfalfa had fewer offspring than those fed broad beans. Alfalfa-fed aphids produced more winged offspring in response to S. aureus and B. bassiana infections. Our findings suggest that the host plant plays a key role in fecundity and winged offspring production in pea aphid colony.

Secondary Symbionts Affect Foraging Capacities of Plant-Specialized Genotypes of the Pea Aphid.

Ecological specialization is widespread in animals, especially in phytophagous insects, which have often a limited range of host plant species. This host plant specialization results from divergent selection on insect populations, which differ consequently in traits like behaviors involved in plant use. Although recent studies highlighted the influence of symbionts on dietary breadth of their insect hosts, whether these microbial partners influence the foraging capacities of plant-specialized insects has received little attention. In this study, we used the pea aphid Acyrthosiphon pisum, which presents distinct plant-specialized lineages and several secondary bacterial symbionts, to examine the possible effects of symbionts on the different foraging steps from plant searching to host plant selection. In particular, we tested the effect of secondary symbionts on the aphid capacity (1) to explore habitat at long distance (estimated through the production of winged offspring), (2) to explore habitat at short distance, and (3) to select its host plant. We found that secondary symbionts had a variable influence on the production of winged offspring in some genotypes, with potential consequences on dispersal and survival. By contrast, symbionts influenced both short-distance exploration and host plant selection only marginally. The implication of symbionts' influence on insect foraging capacities is discussed.

Different phenotypic plastic responses to predators observed among aphid lineages specialized on different host plants

The role of intraspecific variation in the magnitude and direction of plastic responses in ecology and evolution is increasingly recognized. However, the factors underlying intraspecific variation in plastic responses remain largely unexplored, particularly for the hypothesis that the herbivores’ phenotypic response to predators might vary amongst lineages associated with different host plants. Here, we tested whether plant-specialized lineages of the pea aphid, Acyrthosiphon pisum, differed in their transgenerational phenotypic response to ladybird predators (i.e., the asexual production of winged offspring by wingless mothers). In a full factorial laboratory experiment, we found that six aphid clonal lineages each specialized either on alfalfa or clover significantly differed in their transgenerational phenotypic response to predators. Some lineages produced an increased number of winged aphids in predator presence while others did not respond. Aphid lineages specialized on alfalfa had stronger phenotypic responses to predators than those specialized on clover. Although we tested only six aphid lineages from two biotypes, our results imply that intraspecific variation in prey phenotypic response of herbivores to predators differs amongst lineages specialized on different host plants. Our findings therefore raise the question of the influence of plant specialization in shaping herbivore phenotypic responses, and highlight the need to consider multi-trophic interactions to understand the causes and consequences of intraspecific variation in complex phenotypic traits.

The influence of symbiotic bacteria on reproductive strategies and wing polyphenism in pea aphids responding to stress.

Environmental stressors can be key drivers of phenotypes, including reproductive strategies and morphological traits. The response to stress may be altered by the presence of microbial associates. For example, in aphids, facultative (secondary) bacterial symbionts can provide protection against natural enemies and stress induced by elevated temperatures. Furthermore, aphids exhibit phenotypic plasticity, producing winged (rather than wingless) progeny that may be better able to escape danger, and the combination of these factors improves the response to stress. How symbionts and phenotypic plasticity, both of which shape aphids' stress response, influence one another, and together influence host fitness, remains unclear. In this study, we investigate how environmental stressors drive shifts in fecundity and winged/wingless offspring production, and how secondary symbionts influence the process. We induced production of winged offspring through distinct environmental stressors, including exposure to aphid alarm pheromone and crowding, and, in one experiment, we assessed whether the aphid response is influenced by host plant. In the winged morph, energy needed for wing maintenance may lead to trade-offs with other traits, such as reproduction or symbiont maintenance. Potential trade-offs between symbiont maintenance and fitness have been proposed but have not been tested. Thus, beyond studying the production of offspring of alternative morphs, we also explore the influence of symbionts across wing/wingless polyphenism as well as symbiont interaction with cross-generational impacts of environmental stress on reproductive output. All environmental stressors resulted in increased production of winged offspring and shifts in fecundity rates. Additionally, in some cases, aphid host-by-symbiont interactions influenced fecundity. Stress on first-generation aphids had cross-generational impacts on second-generation adults, and the impact on fecundity was further influenced by the presence of secondary symbionts and presence/absence of wings. Our study suggests a complex interaction between beneficial symbionts and environmental stressors. Winged aphids have the advantage of being able to migrate out of danger with more ease, but energy needed for wing production and maintenance may come with reproductive costs for their mothers and for themselves, where in certain cases, these costs are altered by secondary symbionts.

Evolution without standing genetic variation: change in transgenerational plastic response under persistent predation pressure.

Transgenerational phenotypic plasticity is a fast non-genetic response to environmental modifications that can buffer the effects of environmental stresses on populations. However, little is known about the evolution of plasticity in the absence of standing genetic variation although several non-genetic inheritance mechanisms have now been identified. Here we monitored the pea aphid transgenerational phenotypic response to ladybird predators (production of winged offspring) during 27 generations of experimental evolution in the absence of initial genetic variation (clonal multiplication starting from a single individual). We found that the frequency of winged aphids first increased rapidly in response to predators and then remained stable over 25 generations, implying a stable phenotypic reconstruction at each generation. We also found that the high frequency of winged aphids persisted for one generation after removing predators. Winged aphid frequency then entered a refractory phase during which it dropped below the level of control lines for at least two generations before returning to it. Interestingly, the persistence of the winged phenotype decreased and the refractory phase lasted longer with the increasing number of generations of exposure to predators. Finally, we found that aphids continuously exposed to predators for 22 generations evolved a significantly weaker plastic response than aphids never exposed to predators, which, in turn, increased their fitness in presence of predators. Our findings therefore showcased an example of experimental evolution of plasticity in the absence of initial genetic variation and highlight the importance of integrating several components of non-genetic inheritance to detect evolutionary responses to environmental changes.

Non-additive effects of simulated heat waves and predators on prey phenotype and transgenerational phenotypic plasticity.

Understanding the effects of extreme climatic events on species and their interactions is of paramount importance for predicting and mitigating the impacts of climate change on communities and ecosystems. However, the joint effects of extreme climatic events and species interactions on the behaviour and phenotype of organisms remain poorly understood, leaving a substantial gap in our knowledge on the impacts of climatic change on ecological communities. Using an aphid-ladybeetle system, we experimentally investigated the effects of predators and heat shocks on prey body size, microhabitat use, and transgenerational phenotypic plasticity (i.e., the asexual production of winged offspring by unwinged mothers). We found that (i) aphids were smaller in the presence of predators but larger when exposed to frequent heat shocks; (ii) frequent heat shocks shifted aphid distribution towards the plant's apex, but the presence of predators had the opposite effect and dampened the heat-shock effects; and (iii) aphids responded to predators by producing winged offspring, but heat shocks strongly inhibited this transgenerational response to predation. Overall, our experimental results show that heat shocks inhibit phenotypic and behavioural responses to predation (and vice versa) and that such changes may alter trophic interactions, and have important consequences on the dynamics and stability of ecological communities. We conclude that the effects of extreme climatic events on the phenotype and behaviour of interacting species should be considered to understand the effects of climate change on species interactions and communities.

Ecdysone signaling underlies the pea aphid transgenerational wing polyphenism

The wing polyphenism of pea aphids is a compelling laboratory model with which to study the molecular mechanisms underlying phenotypic plasticity. In this polyphenism, environmental stressors such as high aphid density cause asexual, viviparous adult female aphids to alter the developmental fate of their embryos from wingless to winged morphs. This polyphenism is transgenerational, in that the pea aphid mother experiences the environmental signals, but it is her offspring that are affected. Previous research suggested that the steroid hormone ecdysone may play a role in this polyphenism. Here, we analyzed ecdysone-related gene expression patterns and found that they were consistent with a down-regulation of the ecdysone pathway being involved in the production of winged offspring. We therefore predicted that reduced ecdysone signaling would result in more winged offspring. Experimental injections of ecdysone or its analog resulted in a decreased production of winged offspring. Conversely, interfering with ecdysone signaling using an ecdysone receptor antagonist or knocking down the ecdysone receptor gene with RNAi resulted in an increased production of winged offspring. Our results are therefore consistent with the idea that ecdysone plays a causative role in the regulation of the proportion of winged offspring produced in response to crowding in this polyphenism. Our results also show that an environmentally regulated maternal hormone can mediate phenotype production in the next generation, as well as provide significant insight into the molecular mechanisms underlying the functioning of transgenerational phenotypic plasticity.

Mechanisms of species‐sorting: effect of habitat occupancy on aphids' host plant selection

Interspecific interactions such as competition are important factors affecting insect herbivore fitness. Host choice in herbivorous insects including aphids has largely been studied with respect to host plant condition, while the role of competition is also very important. Tansy (Tanacetum vulgare L.) hosts three specialised aphids, Macrosiphoniella tanacetaria (Kaltenbach), Metopeurum fuscoviride Stroyan and Uroleucon tanaceti (L.) (Hemiptera: Aphididae). In this study, a set of greenhouse and field experiments were carried out to investigate whether aphid host plant choice was affected by the presence of the other aphid species. When winged individuals were given the choice between unoccupied plants and plants occupied by the same or another aphid species, choices generally reflected the outcome of competitive interactions among aphids. Colonisation of plants by winged individuals was influenced not only by the presence of other aphids on the host plant but also by previous infestation. The host choice of winged individuals basically reflected competitive hierarchies, i.e. aphids in most cases selected plants where future competition was less likely. By contrast, unwinged aphids did not show any host plant preference. For M. tanacetaria previously infested plants promoted the production of winged offspring. Our results show that competitive interactions could affect host selection behaviour by aphids. In a metacommunity context, such preferences in colonising different habitats leads to species‐sorting through habitat heterogeneity.

Exposure to Bacterial Signals Does Not Alter Pea Aphids’ Survival upon a Second Challenge or Investment in Production of Winged Offspring

Pea aphids have an obligate nutritional symbiosis with the bacteria Buchnera aphidicola and frequently also harbor one or more facultative symbionts. Aphids are also susceptible to bacterial pathogen infections, and it has been suggested that aphids have a limited immune response towards such pathogen infections compared to other, more well-studied insects. However, aphids do possess at least some of the genes known to be involved in bacterial immune responses in other insects, and immune-competent hemocytes. One possibility is that immune priming with microbial elicitors could stimulate immune protection against subsequent bacterial infections, as has been observed in several other insect systems. To address this hypothesis we challenged aphids with bacterial immune elicitors twenty-four hours prior to live bacterial pathogen infections and then compared their survival rates to aphids that were not pre-exposed to bacterial signals. Using two aphid genotypes, we found no evidence for immune protection conferred by immune priming during infections with either Serratia marcescens or with Escherichia coli. Immune priming was not altered by the presence of facultative, beneficial symbionts in the aphids. In the absence of inducible immune protection, aphids may allocate energy towards other defense traits, including production of offspring with wings that could escape deteriorating conditions. To test this, we monitored the ratio of winged to unwinged offspring produced by adult mothers of a single clone that had been exposed to bacterial immune elicitors, to live E. coli infections or to no challenge. We found no correlation between immune challenge and winged offspring production, suggesting that this mechanism of defense, which functions upon exposure to fungal pathogens, is not central to aphid responses to bacterial infections.

Transduction of high‐density signals across generations in aphid wing polyphenism

AbstractWing polyphenism in aphids represents an outstanding example of adaptive phenotypic plasticity. During summer, parthenogenic mother aphids alter the developmental fate of their embryos to produce wingless or winged adult forms in response to high population density (i.e. crowded conditions). Although this maternal effect is well known, the mechanisms underlying transgenerational winged‐morph determination remain largely unresolved. In the present study, the effects of different high‐density treatment durations are tested on the vetch aphid Megoura crassicauda Mordvilko aiming to investigate how and when the density signals detected by mothers are transmitted to embryos. The duration of density treatment shows additive effects on both the number of crowded females producing winged aphids (winged‐producers) and the number of winged progeny. In addition, even when high‐density treatment is stopped, the production of winged offspring continues for several days and depends on the duration of treatment. The results indicate that mother aphids retain high‐density signals for a period after removal of the stimulus. Furthermore, observations of the progeny sequence (i.e. the order in which the offspring are born) and the embryonic stages developing in the mothers reveal that high‐density information may affect embryonic fate at the late embryonic stage immediately before cuticle formation.

Multiple Cues for Winged Morph Production in an Aphid Metacommunity

Environmental factors can lead individuals down different developmental pathways giving rise to distinct phenotypes (phenotypic plasticity). The production of winged or unwinged morphs in aphids is an example of two alternative developmental pathways. Dispersal is paramount in aphids that often have a metapopulation structure, where local subpopulations frequently go extinct, such as the specialized aphids on tansy (Tanacetum vulgare). We conducted various experiments to further understand the cues involved in the production of winged dispersal morphs by the two dominant species of the tansy aphid metacommunity, Metopeurum fuscoviride and Macrosiphoniella tanacetaria. We found that the ant-tended M. fuscoviride produced winged individuals predominantly at the beginning of the season while the untended M. tanacetaria produced winged individuals throughout the season. Winged mothers of both species produced winged offspring, although in both species winged offspring were mainly produced by unwinged females. Crowding and the presence of predators, effects already known to influence wing production in other aphid species, increased the percentage of winged offspring in M. tanacetaria, but not in M. fuscoviride. We find there are also other factors (i.e. temporal effects) inducing the production of winged offspring for natural aphid populations. Our results show that the responses of each aphid species are due to multiple wing induction cues.

Predator‐Induced Dispersal and the Evolution of Conditional Dispersal in Correlated Environments

It is widely accepted that organisms adjust their dispersal propensity to local population density, but there has been no analysis of how they should react to changes in environmental conditions that reduce local density. We take the case of delayed predator-induced dispersal (PID) in aphids to explore in which way current environmental conditions may be utilized as an appropriate signal for dispersal decisions. In aphids, the presence of predators triggers the production of winged offspring that may later leave the plant and shift their center of activity permanently. Using individual-based simulations as well as analytical approximations, we explore under which conditions PID is likely to evolve. We demonstrate that this requires substantial temporal correlation in predation risk and weak competition among prey; these conditions may be fulfilled in the aphid system. We discuss the analogy between the specific case of PID and the evolution of conditional emigration in the face of spatiotemporally correlated deterioration in reproduction or survival.

Alarm pheromone emission by pea aphid, Acyrthosiphon pisum, clones under predation by lacewing larvae

AbstractGenetic variation in anti‐predator traits has been shown for a variety of species. Aphid alarm pheromone, (E)‐β‐farnesene, is released by attacked aphids and causes a variety of behavioral defense reactions in the signal receivers. In pea aphids, Acyrthosiphon pisum Harris (Homoptera: Aphididae), (E)‐β‐farnesene mediates the production of winged offspring in the presence of natural enemies. While variation in the propensity for pea aphids to produce winged offspring is well‐documented, little quantitative information is available about clonal differences in (E)‐β‐farnesene emission or the amount of alarm pheromone released in aphid colonies. We tested the wing induction response of four clones when attacked by a predatory lacewing larva, Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae), and found that three of the four clones increased the proportion of winged offspring under predator attack. We then investigated the emission of aphid alarm pheromone of these clones of pea aphid under attack. Alarm pheromone emission in aphid colonies of initially 25 adults varied from 81.2 to 10 851.0 ng per aphid colony over 24 h. There were no differences between clones in total emission or in emission per consumption event. These results show that there is substantial variability in alarm pheromone emission within clones and that the propensity to produce winged offspring in some clones is not a simple function of the propensity of alarm pheromone production in these clones.

Alarm pheromone induces a transgenerational wing polyphenism in the pea aphid, Acyrthosiphon pisum

In response to increased predation risk, many organisms exhibit transgenerational polyphenisms whereby offspring have behavioural and (or) morphological adaptations to avoid natural enemies. The mechanisms underlying altered phenotypic expression, however, are not well understood. Aphids commonly exhibit a transgenerational wing-induction polyphenism in response to predators and parasitoids, but the stimuli inducing winged offspring production have not yet been identified. As aphids commonly emit the alarm pheromone (E)-β-farnesene (EBF) when physically attacked, this compound is a reliable signal of increased predation risk for asexual conspecifics. Here we show that maternal detection of EBF induces a transgenerational wing polyphenism in offspring of the pea aphid, Acyrthosiphon pisum (Harris, 1776). In response to 50, 500, or 5000 ng of EBF vapor, aphids responded with 2.5-, 5.0-, and 6.0-fold increases in winged offspring production, respectively. Thus, alarm pheromone may alter aphid transgenerational phenotypic expression, thereby influencing aphid – natural enemy dynamics.

Transgenerational phenotypic plasticity under future atmospheric conditions

AbstractOrganisms often exhibit transgenerational phenotypic changes in response to an increased risk of parasitism or predation. Shifts in global atmospheric composition could modify these phenotypic effects through changes in either nutrient quantity/quality or altered interactions with higher trophic levels. Here we show that future atmospheric conditions alter a natural enemy‐induced wing polyphenism in aphids. Winged offspring production by Uroleucon nigrotuberculatum aphids on goldenrod (Solidago canadensis var. scabra) does not differ in enriched CO2 and/or O3 atmospheres. However, proportionally more winged offspring are produced in response to search cues from both coccinellid predators (Coccinella septempunctata) and hymenopteran parasitoids (Aphidius polygonaphis) relative to plants not searched by natural enemies. Moreover, the magnitude of this response differs under enriched CO2 and O3 environments. Aphids produce more winged offspring in response to predators under elevated CO2, but produce more winged offspring in response to parasitoids under elevated O3. Thus, global atmospheric changes influence natural enemy‐mediated phenotypic expression, with potentially far‐reaching consequences for trophic dynamics.

How predictable are aphid population responses to elevated CO2?

Experiments investigating the population responses of aphids to CO2 enrichment have yielded results suggesting that aphid populations will be both larger under elevated CO2 and that they will be smaller under elevated CO2. Most studies have failed to reject the null hypothesis of no difference in population sizes due to atmospheric CO2 concentration. This diversity of results has led some investigators to conclude that aphid responses are not general, and that every aphid-plant interaction may be unique and unpredictable a priori. We use a single, general, mathematical model to consider the population responses of cereal aphids to grass grown under different CO2 concentrations. The model shows that it is possible to explain any of the three observed results: larger populations, smaller populations, or no difference, and that which of these three outcomes arises may depend critically on the interaction between aphid nitrogen requirements and the nitrogen fertility of the soil. The model also shows that the qualitative results will depend on how sensitive the aphid species is to increases in its own density. Past studies have shown that aphids increase their production of winged offspring in response to increasing aphid density. The model predicts that, in general, aphid species that have lower nitrogen requirements and that are less sensitive to their own density will be more likely to have larger populations in elevated CO2 compared to ambient CO2. Differences between aphid species (and clones) in their nitrogen requirements and the strength of their density-dependent response have not been widely reported in the literature. Also, the nitrogen fertility of the soil has rarely been manipulated in experiments on aphid responses to rising CO2 levels. The model suggests that the diversity of population responses of aphids may be both understandable and predictable in the context of such an interaction.

Parasitoids induce production of the dispersal morph of the pea aphid, Acyrthosiphon pisum

In animals, inducible morphological defences against natural enemies mostly involve structures that are protective or make the individual invulnerable to future attack. In the majority of such examples, predators are the selecting agent while examples involving parasites are much less common. Aphids produce a winged dispersal morph under adverse conditions, such as crowding or poor plant quality. It has recently been demonstrated that pea aphids, Acyrthosiphon pisum, also produce winged offspring when exposed to predatory ladybirds, the first example of an enemy‐induced morphological change facilitating dispersal. We examined the response of A. pisum to another important natural enemy, the parasitoid Aphidius ervi, in two sets of experiments. In the first set of experiments, two aphid clones both produced the highest proportion of winged offspring when exposed as colonies on plants to parasitoid females. In all cases, aphids exposed to male parasitoids produced a higher mean proportion of winged offspring than controls, but not significantly so. Aphid disturbance by parasitoids was greatest in female treatments, much less in male treatments and least in controls, tending to match the pattern of winged offspring production. In a second set of experiments, directly parasitised aphids produced no greater proportion of winged offspring than unparasitised controls, thus being parasitised itself is not used by aphids for induction of the winged morph. The induction of wing development by parasitoids shows that host defences against parasites may also include an increased rate of dispersal away from infected habitats. While previous work has shown that parasitism suppresses wing development in parasitised individuals, our experiments are the first to demonstrate a more indirect influence of parasites on insect polyphenism. Because predators and parasites differ fundamentally in a variety of attributes, our finding suggests that the wing production in response to natural enemies is of general occurrence in A. pisum and, perhaps, in other aphids.

Apparent competition between two species of aphid via the fungal pathogen Erynia neoaphidis and its interaction with the aphid parasitoid Aphidius ervi

Abstract 1. Motivated by a community study on aphids and their fungal pathogens, three hypotheses were tested experimentally to investigate the influence of the fungal pathogen, Erynia neoaphidis Remaudière and Hennebert, on aphid population and community ecology.2. Field experiments were performed in 2 years to test whether two susceptible aphid species on different host plants might interact through the shared fungal pathogen. No strong pathogen‐mediated indirect interactions (apparent competition) between populations of pea aphid Acyrthosiphon pisum Harris and nettle aphid Microlophium carnosum Buckton were detected.3. In the first of the field experiments, pea aphids exposed to the fungus showed a weak tendency to produce more winged dispersal morphs than control populations not exposed to the fungus. In a laboratory test, however, no support was found for the hypothesis that the presence of volatiles from fungus‐infected cadavers promotes production of winged offspring.4. The response of the pea aphid parasitoid Aphidius ervi Halliday to colonies containing hosts infected 1 and 3 days previously was assessed. Wasps initiated fewer attacks on 1‐day‐old infected colonies than on healthy colonies, with the numbers on 3‐day‐old fungus‐infected colonies intermediate.

Predator-induced morphological shift in the pea aphid

Aphids exhibit a polymorphism whereby individual aphids are either winged or unwinged. The winged dispersal morph is mainly responsible for the colonization of new plants and, in many species, is produced in response to adverse environmental conditions. Aphids are attacked by a wide range of specialized predators and predation has been shown to strongly influence the growth and persistence of aphid colonies. In two experiments, we reared two clones of pea aphid ( Acyrthosiphon pisum ) in the presence and absence of predatory ladybirds ( Coccinella septempunctata or Adalia bipunctata ). In both experiments, the presence of a predator enhanced the proportion of winged morphs among the offspring produced by the aphids. The aphid clones differed in their reaction to the presence of a ladybird, suggesting the presence of genetic variation for this trait. A treatment that simulated disturbance caused by predators did not enhance winged offspring production. The experiments indicate that aphids respond to the presence of a predator by producing the dispersal morph which can escape by flight to colonize other plants. In contrast to previous examples of predator-induced defence this shift in prey morphology does not lead to better protection against predator attack, but enables aphids to leave plants when mortality risks are high.