While host switches can promote speciation in herbivorous insects, the benefits of switching hosts have only been ascribed to escaping competition and natural enemies. Herbivores might also escape from the defences of their ancestral host if their new host species lacks those defences, but 'defence-free space' has not been tested as a potential driver of host-associated speciation by increasing the likelihood of host shifts. We used field and laboratory experiments to test this hypothesis in goldenrod (Solidago spp.) and its gall fly (Eurosta solidaginis). The ancestral host (S. altissima) senses the volatile emissions (a putative sex pheromone) of male flies and increases its defences against both gall induction by the fly and chewing herbivory from co-occurring herbivore species, while the effect of exposure to this emission was unknown for the derived host (S. gigantea). In growth chamber experiments, we found that both host plant species responded similarly to fly pheromone in the levels of signalling phytohormones jasmonic acid and salicylic acid but that only S. altissima experienced reduced feeding by leaf beetles after pheromone exposure. In the field, S. altissima ramets were less preferred by ovipositing female gall flies after pheromone exposure, while there was no effect for S. gigantea. Conversely, pheromone exposure made S. gigantea ramets more susceptible to one type of herbivory: bunch galling by midge species. Our data show that the derived host, S. gigantea, does respond to the gall fly pheromone, but does so in a way that appears maladaptive for the plant, suggesting that escaping the defence of the ancestral host species provides an additional benefit to herbivores and an ecological mechanism for host switching and eventual speciation.Read the free Plain Language Summary for this article on the Journal blog.

Insect-derived molecular cues can prime plant defences against herbivore attack. The genes that are sensitive to priming, and how their expression changes on the scale of days, have not been fully resolved. Moreover, priming may affect interactions with insects that are not the source of the priming cue. We primed tall goldenrod (Solidago altissima) plants by exposure to the volatile emission of a specialist herbivore, the goldenrod gall fly (Eurosta solidaginis) then subjected the plants to 48 h of herbivory from an unrelated generalist, corn earworm (Helicoverpa zea). Using RNA sequencing, we identified transcriptome-wide gene expression patterns between exposed and unexposed plants. We identified biotic stress-associated genes that were more abundant during herbivory in primed plants, including defence-related transcription factors, thaumatin-like receptors and chitinases. We observed a surprising rise and fall in expression of hundreds of defence-related genes in a 48-h phase in primed damaged plants only. Our results support the hypothesis that primed defences are stronger than typical induced defences and suggest that primed defences target herbivores in the short term. We show that the threat cue from a specialist can affect plant defences against an unrelated herbivore.

Environmental cues that predict increased risk of herbivory can prime plant defenses; however, few studies have explored how such cues elicit broader plant responses, including potential effects on plant growth and other resource allocations that may affect tolerance to herbivore damage. We exposed goldenrod plants ( Solidago altissima ) to varying concentrations of the putative sex pheromone of a gall-inducing herbivore, which has previously been implicated in defense priming. In experiments with two plant genotypes and three herbivore populations, any level of exposure to the pheromone enhanced tolerance of galling, rescuing flower production to levels observed for ungalled plants. Exposure to low doses of the pheromone elicited greater resistance to galling than exposure to high doses, with unexposed plants exhibiting intermediate resistance, suggesting a nonlinear relationship between exposure and defense priming. These findings suggest plant responses to environmental cues associated with biotic stressors are broader and more complex than previously appreciated.

Data for "An insect pheromone primes tolerance of herbivory in goldenrod plants" Data include all raw data necessary for the analyses of the manuscript. These include data on the growth, flower production, rhizome production, and gall induction of goldenrod plants (Solidago altissima) after exposure to a priming cue gradient and a specialist herbivore that is the source of the priming cue. It also contains data on female herbivore oviposition preference. Description of the data and file structure The data are divided into four sheets. The first contains data necessary for analyses presented in the main text. The second contains data for analyses presented in the supplement. The third presents data from a separate experiment presented in the supplement, and the fourth contains R code for the analyses performed. Sharing/Access information These data are currently only available on Zenodo.

Because the diet of many herbivorous insects is restricted to closely related taxa with similar chemistry, intercropping with diverse plant communities may reduce both pest populations and reliance on chemical pesticides in agroecosystems. We tested whether the effectiveness of intercropping against herbivorous insects depends on the phylogenetic relatedness of neighboring crops, using butternut squash (Cucurbita moschata) as a focal crop species in a series of different intercropping combinations. We found that increased phylogenetic divergence of neighboring plants could reduce abundance of herbivorous insects, but the effect was only detectable mid-season. In addition, we tested two hypothesized mechanisms for a negative association between phylogenetic distance of neighboring plants and reduced herbivore populations: one, we tested using Y-tube olfactometer and choice cage trials whether diverse volatile cues impede host-plant location by the dominant pest of butternut squash in our experiment, striped cucumber beetle Acalymma vittatum. Two, we recorded predator and parasitoid abundance relative to crop phylodiversity to test whether diverse crops support larger natural-enemy populations that can better control pest species. Our results, however, did not support either hypothesis. Striped cucumber beetles preferentially oriented toward non-host-plant volatiles, and predator populations more often decreased with phylodiversity than increased. Thus, the mechanisms driving associations in the field between phylogenetic divergence and herbivore populations remain unclear.

Social animals are expected to experience a positive effect of conspecific number or density on fitness (an Allee effect) because of the benefits of group living. However, social animals also often disperse to live either solitarily or in small groups, so to understand why social animals leave their groups it is necessary to understand how group size affects both average fitness and the expected fitness outcomes of individuals. We examined the relationships between group size and fitness in the colonial spider Cyrtophora citricola using long-term observations of colony demographics. We censused colonies, recording the number of juveniles, large females, and egg sacs, approximately every 2 months for 2 years. We also recorded the substrates supporting colony webs, including plant species and size, and the azimuth the colony occupied on the plant. Colonies in all regions showed cyclical patterns of growth and decline; however, regions were not synchronized, and seasonal effects differed between years. Colonies with fewer individuals at the initial observation were less likely to survive over the course of observations, and extinction rates were also influenced by an interaction between region and plant substrate. Small colonies were more likely to be extinct by the next census, but if they survived, they were more likely to have high growth rates compared to larger colonies. Despite the potential for high growth rates, high extinction rates depressed the average fitness of small colonies so that population growth rates peaked at intermediate colony sizes. Variance in egg sac production also peaked at intermediate colony sizes, suggesting that competitive interactions may increase the uneven distribution of resources in larger groups. Even if average fitness is high, if spiders can anticipate poor outcomes in large colonies, they may disperse to live solitarily or in smaller, less competitive groups.

Tall goldenrod plants Solidago altissima appear to eavesdrop on the communication of a specialist gall-inducing fly Eurosta solidaginis by detecting the volatile emissions of male flies and priming anti-herbivore defences. However, the effects of defence priming on fly fitness have not previously been demonstrated, despite some evidence that female flies avoid ovipositing on primed plants in the field. To explore how priming affects female preferences and galling success, we manipulated exposure to the priming cue in multiple genotypes of S. altissima and assessed rates of oviposition and gall development. Priming reduced gall formation overall; however, its effect varied across plant genotypes, as well as by the age of the male flies used for priming, possibly reflecting dosage effects (older flies produce lower emissions). Priming by younger males significantly reduced galling success, while priming by older males slightly improved it. Remarkably, female flies accurately assessed host-plant quality by avoiding plants primed by young males while preferring those primed by older males. Synthesis. Our results suggest that defence priming in S. altissima in response to the volatile emissions of E. solidaginis males does affect fly fitness; however, the effect of priming varied by plant genotype, suggesting that there may be variation in defensive strategies against the fly. Female flies have, in response to this defence, evolved a sophisticated ability to evaluate the quality of primed plants.

Within animal populations, behaviour often varies consistently among individuals, yet it remains unclear what generates and maintains this variation in ?animal personality?. To understand how multiple sources of variation might combine to promote interindividual differences in behaviour, we examined dispersal behaviour in a colonial spider, Cyrtophora citricola. We measured the repeatability of two behaviours in the laboratory that are associated with dispersal: latency to tiptoe (a dispersal behaviour in spiders) and latency to explore a new environment. We then tested five hypothesized sources of consistent variation across two generations of spiders: sex, food resources, transient internal states, heritability and parental effects. Spiders were modestly consistent in both latency to tiptoe and latency to explore. Males behaved similarly to females of the same size; however, males mature at a smaller size than females, and females became much more hesitant to tiptoe and explore as they grew. Food availability had no effect on either behaviour. Repeatability of exploration was higher within an instar than across instars, suggesting that some aspect of spiders' internal state, other than food, maintained relatively high repeatability over short periods. Tiptoe behaviour was significantly heritable for female relatives, but not for male relatives. For exploratory behaviour, siblings showed significant heritability, while parents and offspring did not, suggesting that early natal environments shared by siblings, rather than genes, might account for their similar behaviour. Finally, although food had no effect on the generation of spiders to which the diet was applied, poorly fed fathers had offspring that tiptoed more readily than well-fed fathers, suggesting paternal effects potentially transmitted through epigenetics. Tiptoe and exploratory behaviours were correlated within individuals, yet the overall modest interindividual variation in these two dispersal behaviours was maintained by disparate effects of different sources of variation. (c)& nbsp;2021 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Eurosta solidaginis males produce large amounts of putative sex pheromone compared to other insect species; however, neither the site of pheromone production nor the release mechanism has been characterized. We compared E. solidaginis males and females, focusing on sexually dimorphic structures that are known to be involved in pheromone production in other tephritid species. Morphological and chemical analyses indicated that the rectum and pleural epidermis are involved in male E. solidaginis pheromone production, storage, or emission. We detected large quantities of pheromone in the enlarged rectum, suggesting that it stores pheromone for subsequent release through the anus. However, pheromone might also discharge through the pleural cuticle with the involvement of unusual pleural attachments of the tergosternal muscles, which, when contracted in males, realign specialized cuticular surface elements and expose less-sclerotized areas of cuticle. In males, pheromone components were also detected in epidermal cells of the pleuron. These cells were 60-100 times larger in mature males than in females and, to our knowledge, are the largest animal epithelial cells ever recorded. Furthermore, because these large cells in males are multinucleated, we presume that they develop through somatic polyploidization by endomitosis. Consequently, the pheromone-associated multinuclear pleural epidermal cells of Eurosta solidaginis may provide an interesting new system for understanding polyploidization.

Proximate cues for animal dispersal are complex and varied. Multiple cues may provide information about different aspects of habitat quality, and these aspects may interact with each other, as well as with population density in different ways. We examined how individuals incorporate multiple cues in their decisions to emigrate and immigrate in the colonial orb‐weaving spider, Cyrtophora citricola . We manipulated maternal feeding as a cue for prey abundance and measured the size of the maternal web, which provides a limited space for philopatric offspring and a second potential dispersal cue. In addition, we recorded all immigration events to determine dispersal distances and the cues juveniles may use in settlement. Dispersal increased when mothers were poorly fed, web sizes were small and clutch sizes were large. In addition to these overall effects, maternal feeding also interacted with web size, indicating that offspring from well‐fed mothers were more tolerant of high sibling densities. We also detected a threshold for the effect of clutch size on dispersal for the first egg sac: below 20 offspring, there was no effect of clutch size, but dispersal increased with clutch size for larger clutches. Dispersal distances were often short, and immigrants preferred sheltered trees and those occupied by adult females. Dispersal not only depended on multiple cues, but these cues interacted, and the importance of web size suggested that saturation of the natal web might force dispersal, at least for spiders with poorly‐fed mothers. How one aspect of habitat quality influences dispersal can therefore depend on the state of other aspects of habitat quality. In particular, some natal resources, such as a nest or territory, may become saturated and limit group size, but this limit will also depend on other factors, such as prey availability.

In the goldenrod Solidago altissima, most stems are erect, but "ducking" genotypes bend the tip of the apical stem downward for much of the growing season, and this morphology protects against at least two gall-forming herbivore species. Despite this advantage to defense, ducking remains a rare strategy in goldenrod, yet the costs that prevent ducking genotypes from outcompeting erect genotypes remain unclear. We tested whether ducking (an architectural defense) trades off with chemical defense against aphids (Uroleucon nigrotuberculatum). We hypothesized that signaling related to the ducking defense might interfere with investment in chemical defenses, making ducking plants more susceptible to some herbivores. To test this hypothesis, we compared aphid survival and preference on ducking and erect genotypes. We also measured terpenoid concentration in S. altissima leaf tissue to determine whether plant investment in these compounds correlated with either ducking or aphid performance. Aphids had higher survival on all three ducking genotypes than their erect counterparts and preferred ducking to erect plants in two of three genotype pairings. However, terpenoid concentrations did not track with either ducking or aphid performance and cannot therefore explain the differences between ducking and erect host-plants. Although the mechanism remains unknown, the data supported the predicted trade-off in defenses against different herbivores, which may contribute to the distribution and abundance of these two defensive strategies.

BACKGROUND:By sensing environmental cues indicative of pathogens or herbivores, plants can "prime" appropriate defenses and deploy faster, stronger responses to subsequent attack. Such priming presumably entails costs-else the primed state should be constitutively expressed-yet those costs remain poorly documented, in part due to a lack of studies conducted under realistic ecological conditions. We explored how defence priming in goldenrod (Solidago altissima) influenced growth and reproduction under semi-natural field conditions by manipulating exposure to priming cues (volatile emissions of a specialist herbivore, Eurosta solidaginis), competition between neighbouring plants, and herbivory (via insecticide application).RESULTS:We found that primed plants grew faster than unprimed plants, but produced fewer rhizomes, suggesting reduced capacity for clonal reproduction. Unexpectedly, this effect was apparent only in the absence of insecticide, prompting a follow-up experiment that revealed direct effects of the pesticide esfenvalerate on plant growth (contrary to previous reports from goldenrod). Meanwhile, even in the absence of pesticide, priming had little effect on herbivore damage levels, likely because herbivores susceptible to the primed defences were rare or absent due to seasonality.CONCLUSIONS:Reduced clonal reproduction in primed plants suggest that priming can entail significant costs for plants. These costs, however, may only become apparent when priming cues fail to provide accurate information about prevailing threats, as was the case in this study. Additionally, our insecticide data indicate that pesticides or their carrier compounds can subtly, but significantly, affect plant physiology and may interact with plant defences.

Summary Plants frequently employ induced, rather than constitutive, defences against herbivores and pathogens, presumably as an adaptive response to the unpredictability of attack by particular antagonists. Plants may further accelerate defence deployment by ‘priming’ appropriate defences in response to environmental cues that reliably predict impending attack. However, the population‐ and community‐level ecological consequences of such priming remain relatively unexplored. We recently discovered that the volatile emissions of male Eurosta solidaginis prime the antiherbivore defences of its host plant, tall goldenrod (Solidago altissima). This co‐evolved system provides a unique opportunity to study the ecological consequences of priming in a natural system. We explored effects of the priming cue on neighbouring ramets at varying distances from the emission source by quantifying subsequent levels of foliar herbivory, as well as plant growth and flower production (which might reveal trade‐offs between investment in growth or reproduction and defence). We observed a linear increase in leaf damage with distance from the emission source (up to our maximal distance of 1 m), consistent with the hypothesis that the intensity of priming corresponds to the intensity of exposure to the fly emission. Unexpectedly, ramets nearest the emission source also exhibited a short‐term increase in growth‐rate; however, this effect did not persist to the end of the season or increase flower production. Instead, ramet's mid‐distance from the emission source exhibited reduced growth and flower production compared to those nearer or farther away. Synthesis. The responsiveness of Solidago altissima ramets to herbivore‐associated cues across a distance of 1 m or more is highly relevant in this system, where individual ramets frequently grow within a few cm of one another. Furthermore, the resulting mosaic of ramets primed to varying degrees might influence herbivore (and consequently predator) distributions. The unexpected decline in flower production by mid‐distance ramets suggests that the effects of plant priming on ecological interactions among plants and other organisms (such as tritrophic interactions and competition) may feed back onto plant fitness in complex, and as yet unexplored, ways. A lay summary is available for this article.

The costs and benefits of group living can vary among group members depending on their physical location within the group. If individuals can anticipate poor positions and leave the group, the society may dissolve. Therefore, understanding the geometry of social groups is critical to understanding their stability. We examined social geometry in the colonial spider, Cyrtophora citricola (Araneidae), which builds long-lasting individual webs within a shared colony framework. Group foraging benefits are thought to be an ultimate cause for the evolution of colonial living in spiders, but conflict often arises over food and territory. To understand how foraging benefits of grouping interact with inter-individual conflict to shape group geometry, we examined the effects of feeding history and body size on inter-individual spacing in the laboratory. We also examined the effect of spider density and body size on individual position within colonies in a semi-natural setting. We found that spiders with prior food stress increased their inter-individual spacing, suggesting that competition for prey may override group foraging benefits. Larger spiders built their webs first, relegating smaller spiders to the margins of the space and sometimes preventing them from completing web construction. In a semi-natural setting, spiders did not maintain close spacing, but rather spread themselves out over the substrate, and larger spiders occupied the preferred side of the substrate to the exclusion of smaller spiders. Contrary to the hypothesis that foraging advantages to group living promote greater cohesion under food stress, food competition appeared to promote group instability, and exclusion of small spiders by larger and more dominant individuals seemed to determine position in the colony.

Diet restriction increases longevity while reducing fecundity in a broad range of organisms. However, there are exceptions to this rule, and the causes of these exceptions remain unclear. One hypothesis is that short-lived, semelparous organisms gain no benefit from increased longevity regardless of nutritional resources. Another hypothesis is that organisms may alter their behaviour to compensate for nutrient deficiencies. We examined these hypotheses in the colonial orb-weaving spider Cyrtophora citricola. Sexual cannibalism is frequent in this species so that females are long lived and interoparous while males are semelparous. Because of these differing sexual strategies, we predicted that the common pattern of increased longevity under diet restriction would hold for females but not for males. We also investigated in a semi-natural setting whether spiders could compensate for diet restriction by altering their feeding behaviour. Diet-restricted females produced fewer offspring but lived longer than well-fed females, while diet had no effect on male longevity. Despite being semelparous, virgin males were quite long-lived, suggesting that potential lifespan is relatively unimportant in determining the effects of diet restriction. Contrary to our predictions, females were unable to compensate for their restricted diet by altering their foraging behaviour. Instead, semi-natural conditions increased the differences between spiders on high and low diets, suggesting that the effects of diet restriction can be pervasive under natural conditions.

The abundance of sperm relative to eggs selects for males that maximize their number of mates and for females that choose high quality males. However, in many species, males exercise mate choice, even when they invest little in their offspring. Sexual cannibalism may promote male choosiness by limiting the number of females a male can inseminate and by biasing the sex ratio toward females because, while females can reenter the mating pool, cannibalized males cannot. These effects may be insufficient for male choosiness to evolve, however, if males face low sequential encounter rates with females. We hypothesized that sexual cannibalism should facilitate the evolution of male choosiness in group living species because a male is likely to encounter multiple receptive females simultaneously. We tested this hypothesis in a colonial orb-weaving spider, Cyrtophora citricola, with a high rate of sexual cannibalism. We tested whether mated females would mate with multiple males, and thereby shift the operational sex ratio toward females. We also investigated whether either sex chooses mates based on nutritional state and age, and whether males choose females based on reproductive state. We found that females are readily polyandrous and exhibit no mate choice related to male feeding or age. Males courted more often when the male was older and the female was younger, and males copulated more often with well-fed females. The data show that males are choosier than females for the traits we measured, supporting our hypothesis that group living and sexual cannibalism may together promote the evolution of male mate choice.

Interference competition can profoundly influence the outcome of species interactions and may lead to either coexistence or exclusion. Our understanding of how interference can lead to coexistence remains incomplete, particularly when interference fails to result in resource partitioning. I document a novel form of interference competition between an ant (Myrmecia pyriformis) and a social spider (Delena cancerides) with similar foraging patterns. Of 120 nest boxes occupied by D. cancerides in the field, 7 (6 %) were invaded by M. pyriformis ants over a 2-month period. After eliminating spiders from the nest boxes, the ants proceeded to fill the boxes with debris, rendering them useless to the spiders. The ants do not occupy the nest boxes; thus, interference occurs at a resource that is necessary to one species, but not the other. I discuss how further research into this system may improve our understanding of how interference competition can support coexistence. I also suggest modeling exploitation and interference competition on multiple resources to align with this and other empirical examples where different forms of competition occur for different resources.

While most spiders are solitary and opportunistically cannibalistic, a variety of social organisations has evolved in a minority of spider species. One form of social organisation is subsociality, in which siblings remain together with their parent for some period of time but disperse prior to independent reproduction. We review the literature on subsocial and maternal behaviour in spiders to highlight areas in which subsocial spiders have informed our understanding of social evolution and to identify promising areas of future research. We show that subsocial behaviour has evolved independently at least 18 times in spiders, across a wide phylogenetic distribution. Subsocial behaviour is diverse in terms of the form of care provided by the mother, the duration of care and sibling association, the degree of interaction and cooperation among siblings, and the use of vibratory and chemical communication. Subsocial spiders are useful model organisms to study various topics in ecology, such as kin recognition and the evolution of cheating and its impact on societies. Further, why social behaviour evolved in some lineages and not others is currently a topic of debate in behavioural ecology, and we argue that spiders offer an opportunity to untangle the ecological causes of parental care, which forms the basis of many other animal societies.

Siblings living together compete with each other for resources, yet they may also cooperate to maximize their inclusive fitness. In social spiders, siblings share prey and may both compete and cooperate to obtain this resource. In the laboratory, the social huntsman spider, Delena cancerides, readily shares prey captured by other colony members; however, these spiders only occasionally share prey in the field, making the importance of prey sharing to their social system difficult to assess directly. We examined the importance of prey sharing indirectly by measuring the body condition of spiders from 90 colonies at the time of collection. We compared body condition to colony demographics to determine whether the patterns were consistent with the hypothesis that younger spiders benefit from sharing prey captured by older siblings. We tested several alternative hypotheses that might also explain associations between condition and the presence of siblings. We further conducted a laboratory experiment to directly determine whether feeding on prey captured by older siblings improves the condition of younger spiders. Younger spiders collected from the field were heavier in the presence of older siblings, but there was no effect for older spiders or for any spider with younger siblings. Laboratory spiders gained access to additional prey captured by older siblings. We rejected the alternative hypotheses and concluded that younger spiders indeed benefit from the presence of older siblings. This system provides evidence that the exploitation of others' resources can provide a benefit of group living and act as a form of cooperation. (C) 2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.