Plant Responses to Insect Egg Deposition

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Monika Hilker1,∗ and Nina E. Fatouros1,2

1Institute of Biology, Dahlem Centre of Plant Sciences, Freie Universitat¨ Berlin, 12163 Berlin, Germany; email: [email protected] 2Laboratory of Entomology, Wageningen University, 6700 EH Wageningen, The Netherlands; email: [email protected]

Annu. Rev. Entomol. 2015. 60:493–515 Keywords First published online as a Review in Advance on oviposition, induced plant defense, parasitoids, plant volatiles, priming, October 20, 2014 bacterial symbiont The Annual Review of Entomology is online at ento.annualreviews.org Abstract This article’s doi: Plants can respond to insect egg deposition and thus resist attack by herbiv- 10.1146/annurev-ento-010814-020620 orous insects from the beginning of the attack, egg deposition. We review Copyright c 2015 by Annual Reviews.

Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org ecological effects of plant responses to insect eggs and differentiate between All rights reserved egg-induced plant defenses that directly harm the eggs and indirect defenses ∗ Corresponding author that involve egg parasitoids. Furthermore, we discuss the ability of plants to take insect eggs as warning signals; the eggs indicate future larval feeding damage and trigger plant changes that either directly impair larval performance or attract enemies of the larvae. We address the questions of how egg-associated cues elicit plant defenses, how the information that eggs have

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. been laid is transmitted within a plant, and which molecular and chemical plant responses are induced by egg deposition. Finally, we highlight evolutionary aspects of the interactions between plants and insect eggs and ask how the herbivorous insect copes with egg-induced plant defenses and may avoid them by counteradaptations.

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INTRODUCTION In most insect species, the egg is the first life stage that is directly exposed to the environment. Egg deposition liberates the female from hosting and nourishing the developing embryo inside her body. Nevertheless, the highly vulnerable egg stage needs to be protected from mortality risks to ensure successful reproduction. The risks to which eggs are exposed can be limited by the devices that insect parents transfer into or onto the eggs to protect them against predators, parasitoids, and abiotic stresses (10, 34, 35, 67, 93). Moreover, some insects show sophisticated parental care behavior and guard and shield their eggs with their bodies (63, 116, 126). The type of egg-laying behavior (e.g., egg clustering; 113) and the choice of oviposition site (47, 79) may further determine the chances of eggs surviving. Successful egg development requires a site that provides (a) appropriate abiotic conditions, (b) a low risk of predation, parasitism, and disease, and (c) sufficient food for the offspring (52). Herbivorous insects laying their eggs on plant tissue face the risk of aggressive plant responses that are detrimental to the eggs. To date, oviposition by more than 20 species from a wide range of insect taxa, including plant- and leafhoppers, beetles, sawflies, butterflies, moths, and flies, has been shown to induce plant responses that either have direct negative effects on eggs or inform parasitoids about the presence of eggs and thus indirectly harm the eggs by involving the third Supplemental Material trophic level (53–55, 99) (Supplemental Table 1; follow the Supplemental Materials link from the Annual Reviews home page at http://www.annualreviews.org). Some studies suggest that in addition to these egg-induced direct and indirect plant defenses, plants can take insect egg deposition as a warning signal of future larval herbivory. Plants warned by egg deposition start to prepare their defense against feeding larvae even before larval hatching (6, 40, 44, 68, 92) or accel- erate their growth and thus begin flowering and reproducing earlier than nonwarned plants (77, 92). One counteradaptation of insects to these plant responses would be to manipulate the plant’s reaction to eggs in such a way that plant defense against larvae would be suppressed (12). Hence, the interaction between plants and insect eggs may have very different ecological effects, ranging from egg-induced direct and indirect defenses to warning (priming) effects and possibly egg- induced suppression of plant antiherbivore defense (see Figure 1 and Supplemental Table 1). Furthermore, egg-induced plant responses have been described for more than 20 plant species that cover wide taxonomic and ecological spectra ranging from short-lived herbaceous species

to long-lived trees, from gymnosperms to angiosperms, from C3 plants to drought-adapted C4 plants (e.g., grasses, maize), from monocotyledon to dicotyledon plants (Supplemental Table 1). If one considers that egg deposition by numerous herbivorous insect species with very different egg-laying behaviors elicits responses in such a wide range of plant species, it is not surprising that the plant–insect egg dialogues result in a multitude of ecological effects and require sophisticated Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org molecular and chemical mechanisms that are ﬁne-tuned to the interacting species. In this context, we sort egg-induced plant responses by their ecological effects and consider them from a molecular, chemical, and evolutionary ecological perspective. We place special emphasis on ecological and evolutionary aspects of studies on plant–insect egg interactions that have been published during the last few years; thus, we aim to augment the existing framework of the complex pattern of plant responses to eggs outlined by previous reviews (53–55, 99). Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. ECOLOGICAL EFFECTS OF EGG-INDUCED PLANT RESPONSES Researchers have observed ecological effects of plant responses to both singly and gregariously laid eggs, as well as to eggs laid on undamaged leaf tissue or on ovipositionally damaged or feeding- damaged leaf tissue. Hence, whether egg-induced plant responses result in direct or indirect plant defense or have warning or suppressive effects (Figure 1) seems to be independent of the type

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Egg-larval parasitoids and larval parasitoids Egg parasitoids

Herbivore

OIPVs HIPVs

Eggs are taken as a warning signal and mediate direct Changes in plant VOCs and indirect defenses against larvae

Changes in internal plant secondary metabolites Direct anti-egg defenses: formation of plant neoplasms, egg-crushing plant tissue, leaf necrosis, and/or ovicidal substance

Phytochemical changes in leaf surface Attraction/arrestment Deterrence/avoidance Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org

Leaf waxes

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. Figure 1 Overview of plant responses to herbivorous insect egg deposition and their impact on interactions between plants, herbivores, and parasitoids. Abbreviations: HIPVs, herbivore-induced plant volatiles; OIPVs, oviposition-induced plant volatiles; VOCs, volatile organic compounds.

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of insect oviposition behavior. Nevertheless, the specialization of the egg-laying insect to a plant species may affect the plant response to eggs (40, 84, 87, 92); this is addressed below in the context of the evolutionary aspects of the interactions between plants and insect eggs. Hypersensitive response (HR): Egg-Induced Plant Defense Directly Targeting Egg-Laying Females or Eggs a plant’s response to phytopathogens results The first study indicating that insect egg deposition on plants can induce deterrence of further in the formation of egg deposition was conducted by Blaakmeer et al. (7, 8) when they investigated egg deposition necrotic plant tissue by the large cabbage white butterfly, Pieris brassicae, on cabbage plants (Brassica oleracea). Later that isolates the invader from healthy studies revealed that brassicaceous plants can indeed respond to Pieris egg deposition by changing tissue leaf odor or leaf surface chemistry, as outlined below (9, 37, 40, 41). Females of P. brassicae are repelled by the oviposition-induced odor of black mustard plants (Brassica nigra) (40). Egg-induced plant defense strategies directly targeting the eggs rather than the egg-laying female include plant-mediated desiccation of eggs, egg dropping, egg crushing, and egg killing Supplemental Material (Supplemental Table 1). Desiccation of eggs on plants that form necrotic leaf tissue where eggs are attached has been observed on black mustard leaves laden with Pieris eggs (40, 42, 110) (Figure 2a). Egg deposition by P. brassicae on host plant leaves induces production of reactive oxygen species, formation of callose (74), and death of plant cells. This egg-induced response is considered a hypersensitive response (HR)-like necrosis because it appears similar to HR induced by phytopathogens, but whether the mechanisms of a plant’s response to eggs are the same as those of HR to phytopathogens is unknown (40, 43, 72, 74, 88). Furthermore, plants can cast eggs off their leaves. When an insect deposits its eggs onto a plant, the plant may respond with growth of neoplastic tissue that loosens the interface between eggs and plant surface and finally results in detachment of eggs. Larvae hatching from eggs falling on the ground suffer greater mortality than larvae hatching from eggs on plants (5). Egg dropping by formation of plant neoplasms at the site of egg deposition is known to occur in several plant-insect systems; e.g., (a) certain lines of Pisum sativum grow neoplasms on the outside of pods where the eggs of Bruchus pisorum or Callosobruchus maculatus are attached (32), and (b) Physalis leaves grow neoplasms beneath the eggs of the moth Heliothis subflexa (96) (Figure 2b). Egg-induced growth of plant tissue may lead to not only detachment of eggs, but also egg crushing, as was shown for eggs laid on Viburnum twigs by the leaf beetle Pyrrhalta viburnum (27); for eggs laid on jarrah leaves (Eucalyptus marginata) by the jarrah leafminer moth, Perthida glyphopa (80); and for eggs laid on fruits of cultivated avocado (Persea americana)byAnastrepha fruit flies (4). The Pyrrhalta female deposits her eggs in little cavities that she gnaws into a Viburnum twig and covers the egg deposition site with fecal matter and twig snippets that deter egg predators with bitter triterpenes (50). When the Viburnum twigs grow wound tissue in response to the oviposition,

Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org the covered cavity becomes too small, and eggs will be either squeezed out of or squashed inside the cavity. The stronger the plant wound response is, the greater the mortality of Pyrrhalta eggs per cavity is (27) (Figure 2c). Furthermore, plants can kill eggs by producing ovicidal substances. Leaves of some rice varieties form watery lesions in response to egg deposition by the planthopper species Sogatella furcifera, Nilaparvata lugens,andLaodelphax striatellus. Eggs inside these lesions experience high mortality (109, 115). Eggs of S. furcifera are killed by an ovicidal compound in the watery lesion, benzyl

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. benzoate. Formation of watery lesions and egg mortality are independent of egg density per plant but dependent on plant age (115).

Indirect Plant Defense: Egg-Induced Plant Responses Inform Egg Parasitoids More than a decade ago, studies showed that insect eggs deposited on leaves induce the emission of leaf volatiles that attract parasitic wasps that kill the eggs (see sidebar, Herbivore-Induced

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a b

Neoplasm

Hypersensitive response–like necrosis

c Wound tissue d partially crushing the eggs EEgggg capcap wwithith eegggg mmassass uunderneathnderneath

VViburnumiburnum lleafeaf bbeetleeetle eegggg mmassass wwithith eegggg capcap rremovedemoved

e Bursa copulatrix f

Oviduct

Ovariole Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org

Accessory reproductive gland

Figure 2 Plant responses to insect eggs. (a) Egg of small cabbage white butterﬂy, also known as imported cabbageworm (Pieris rapae), inducing hypersensitive response–like necrosis in Brassica nigra.(b) Egg of Heliothis subﬂexa inducing neoplastic growth in Physalis angulata leaf. Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. (c) Viburnum leaf beetle (Pyrrhalta viburni ) egg mass laid in a cavity gnawed into a Viburnum twig with protective egg cap secretion covering egg mass (or with egg cap removed) (left); production of wound tissue crushing the eggs (right). (d ) Larval parasitoid Cotesia glomerata on Pieris brassicae egg mass, trying to parasitize neonates; parasitoids are attracted by OIPVs. (e) Dissected reproductive tract of a P. brassicae female; plant-defense-eliciting secretion in accessory reproductive gland. ( f ) Egg cluster of a Donacia leaf beetle species consisting of hundreds of eggs deposited on a reed; egg aggregation is discussed here as a counteradaptive strategy (see section Herbivore Offense Traits in Response to Egg-Induced Plant Defenses).

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HERBIVORE-INDUCED PLANT VOLATILES AND OVIPOSITION-INDUCED PLANT VOLATILES

Plant volatiles induced by feeding activity of herbivorous arthropods are referred to as herbivore-induced plant volatiles (HIPVs); the ﬁrst evidence that HIPVs can attract enemies of the feeding stages of herbivorous arthropods was provided by Dicke & Sabelis (31) and Turlings et al. (122). An overview of current knowledge of HIPVs in an evolutionary context is provided by Dicke & Baldwin (30). In this review, we refer to plant volatiles induced speciﬁcally by insect oviposition as oviposition-induced plant volatiles (OIPVs) and provide an overview of their effects on parasitoids killing the herbivore in either its egg stage or a later juvenile stage.

Supplemental Material Plant Volatiles and Oviposition-Induced Plant Volatiles, and Supplemental Table 1). These early studies demonstrated that oviposition by elm leaf beetles (Xanthogaleruca luteola)on elm leaves (Ulmus minor) (83, 125) and by pine sawflies (Diprion pini, Neodiprion sertifer)on pines (Pinus sylvestris) (51, 85, 87) induces emission of plant volatiles that attract females of specialist hymenopteran (Eulophidae) egg parasitoids, i.e., Oomyzus gallerucae and Closterocerus (formerly Chrysonotomyia) ruforum, respectively. These egg parasitoids are attracted to plant volatiles that are specifically induced by oviposition but not by plant damage associated with oviposition. Further studies revealed that oviposition by bugs and leafhoppers, which often damage leaves by their sucking-feeding activity close to the oviposition site, results in release of oviposition- induced plant volatiles (OIPVs) that attract egg parasitoids (17, 19, 54). However, the release of OIPVs by egg-laden plants is not dependent on damage associated with egg deposition. When butterflies or moths lay their eggs on leaves, no obvious leaf damage is observed. They often wipe their abdominal tip on the leaf surface or tap on the leaf with their legs prior to oviposition. The leaf epidermis may be scratched by these movements; however, in contrast to the above- described effects of behaviors linked with egg deposition by beetles, sawflies, bugs, and leafhoppers, no severe structural lesions of leaf tissue occur. Egg deposition by lepidopteran species on maize landraces and black mustard resulted in emission of OIPVs that attract Trichogramma egg parasitoids, which are often considered more habitat specific than host specific (42, 100, 117, 118). Attraction of egg parasitoids by OIPVs has usually been shown in laboratory olfactometer bioassays. However, one field study revealed that the eulophid wasp O. gallerucae is significantly

Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org attracted to traps baited with (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), a terpenoid volatile that is released from elm leaves with eggs and feeding damage (14; Supplemental Table 2). Hence, Egg parasitoids: a single volatile compound, a key component of the OIPV blend, can attract egg parasitoids even in insects that attack host the presence of numerous other habitat volatiles. Parasitoids attracted by OIPVs show surprisingly eggs and complete development inside ﬁned-tuned behavioral responses to the egg-induced changes in plant odor. Many egg parasitoids the host eggs respond innately to OIPVs without any prior occasion to associate successful location of host eggs Synomone: with egg-induced plant odor (38, 106).

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. a chemical that In addition to OIPVs, egg-induced changes in the plant’s surface chemistry can also inform egg interspeciﬁcally parasitoids and act as synomones (Supplemental Table 2). Several plants responded to insect egg mediates information deposition by changing leaf surface cues that tend to retain parasitoids on leaves with host eggs, that is beneﬁcial for e.g., the response of thale cress Arabidopsis thaliana and brussels sprouts B. oleracea var. gemmifera both the releaser and receiver organism to egg deposition by Pieris spp. (9, 37, 41, 91), and the response of tea plants Camellia sinensis to eggs laid by the tortricid moth Adoxophyes honmai (26). When parasitoids perceive this egg-induced

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information while walking on the leaf surface, they remain longer at this site. Thus, their chances of encountering host eggs increase. Further studies showed that parasitoid behavior is affected by a combination of egg-induced Kairomone: plant responses and host cues left by egg-laying herbivore females at the oviposition site (21, 102). a chemical that When insects lay their eggs on leaves, they often leave cues such as footprints; or, in the case interspecifically of egg-laying lepidopteran species, they shed wing scales at the oviposition site. Parasitic wasps mediates information may exploit footprints and scale chemicals as kairomonal cues for short-range orientation to their that is beneficial for hosts (38). When orientation by these kairomones is combined with orientation by egg-induced the receiver organism but costly for the plant cues, this dual-cue orientation might be a reliable host location strategy of parasitoids. The releaser orientation by egg-induced plant cues could serve as a backup when kairomonal cues from the Egg-mediated host have evaporated or have been oxidized, and the orientation by kairomonal cues could serve priming: priming of as a backup when egg-induced plant cues have not yet been produced or have not been produced antiherbivore plant in sufficient quantities (56). defense; eggs prepare the plant for more Insect Eggs Taken by Plants as Warning Signals of Future Larval Herbivory efficient defense against feeding A wide range of studies have shown that plants can respond to cues that indicate future herbivory. herbivores Odor released from feeding-damaged leaves may inform as yet undamaged parts of an herbivore- Egg-larval infested plant or even noninfested con- or heterospecific neighboring plants about the impending (egg-pupal) danger of herbivory (29, 49, 58, 66). The feeding-induced plant odor can prime defense in the parasitoids: insects noninfested plant and thus prepare it for upcoming danger from the imminent herbivores. The that oviposit into a successful evolution of a plant’s ability to take a cue as a warning of future herbivory requires that larva inside a host egg and develop further in the warning cue be very reliable. The plant would not benefit from a response to a cue that proves the hatched host larva to be a false warning (64). The more imminent the danger of herbivory is, the more reliable the (and pupa) warning cue should be. Larval parasitoids: Eggs laid by herbivorous insects on a plant indicate that larval feeding damage will soon insects that oviposit begin. Hence, insect eggs are expected to be highly reliable predictors of impending larval feeding into host larvae and damage. Egg-induced plant defenses targeting the egg might fail to completely repress the insect develop in them attack, e.g., because of limited success of direct defense or low parasitoid density in the case of indirect defense. If egg-induced plant responses could mediate defense that affects the hatching larvae, such defense strategies might significantly contribute to a plant’s defensive arsenal against feeding herbivores. Indeed, several studies suggest that egg-mediated plant reactions can target the larvae hatching from eggs by two strategies: (a) early attraction or arrestment of parasitoids that develop not inside the host egg but in later juvenile host stages (here considered egg-induced indirect defense against larval herbivory) and (b) activation of more efficient defense against feeding larvae by egg-laden plants than by egg-free ones (indicating egg-mediated priming of antiherbivore

Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org defense). Several studies have reported early attraction of egg-larval parasitoids, egg-pupal parasitoids (16, 26, 95, 97), or larval parasitoids (11, 40, 90, 98, 118) by egg-induced plant cues. Hence, in these cases, the plants do not attract egg parasitoids that kill the herbivore in its embryonic stage; instead, parasitoids of later juvenile herbivorous stages are attracted in a very timely manner, even prior to larval hatching (Figure 2d and Supplemental Table 1). Supplemental Material Oviposition-mediated higher efﬁciency of direct plant defense against feeding larvae has been

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. showninpine(P. sylvestris)–pine sawfly (D. pini ) interactions (6) and in Brassicaceae-Pieris interactions (44, 92). Sawfly and Pieris larvae have significantly worse performance if they start feeding on the same plant where they hatched from eggs, compared with larvae that are transferred to an egg-free plant after hatching from eggs. These results indicate that egg deposition can warn the plant of future larval herbivory and mediate a change in the plant’s nutritional quality, which in turn impairs larval performance.

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Furthermore, a study of interactions between tomato (Solanum lycopersicum) and the moth Helicoverpa zea, the corn earworm, indicated that oviposition mediated higher efficiency of direct plant defense against feeding larvae (68). Feeding-damaged tomato leaves with prior egg deposition Elicitor: microbial- (MAMPs), pathogen- show significantly higher transcript levels of proteinase inhibitor 2 ( pin2) than egg-free, but feeding- (PAMPs), or damaged, leaves. However, whether the differential expression of pin2 affects larval performance herbivore- (HAMPs) has not yet been studied (68). associated molecular patterns recognized by specific plant Eggs Suppressing Antiherbivore Plant Defense? receptors, which then initiate a plant In contrast to the above-mentioned examples wherein plants “anticipated” larval herbivory and response either responded to eggs by attracting parasitoids, which then developed in host larvae, or prepared improved defense against the feeding larvae, a few studies indicate that insect egg deposition may suppress a plant’s antiherbivore defense (Supplemental Table 1). Interestingly, when leaves of A. thaliana are treated with the supernatant of crushed eggs of Supplemental Material P. brassicae, freshly hatched, singly feeding larvae of the highly polyphagous moth Spodoptera littoralis gain more weight than larvae feeding on untreated leaves. In contrast, larval weight is unaffected when P. brassicae larvae feed singly on leaves with this treatment (12). The authors of the study that reported this finding concluded that insect egg deposition can suppress plant defense against generalist larvae, whereas they expected specialist larvae, such as P. brassicae,to be adapted to egg-mediated plant responses and thus unaffected when feeding on previously egg-laden plants. The difference between these results (12) and those mentioned above on the warning effects mediated by P. brassicae eggs on A. thaliana (44) may be due to (a)thetype of plant treatment (crushed eggs versus natural egg deposition), (b) the type of larval feeding [larvae placed singly onto a leaf versus gregariously feeding, young larvae (natural behavior)], or (c) differences between insect lines used by the laboratories. Suppression of plant defense by insect egg deposition was also suggested when a commercially available maize variety (cv. Delprim) laden with eggs of the moth Spodoptera frugiperda was found to show lower emission of leaf volatiles than egg-free plants. The egg-mediated suppression of emission of leaf volatiles is retained when S. frugiperda larvae start feeding (94); however, whether the reduced emission rates can indeed be linked to suppression of plant defense remains unclear. Although several other studies reported reduced emission of plant volatiles in response to insect egg deposition, no suppression of indirect defense was associated with this reduction (11, 40, 90). Indeed, plants with egg-induced lowered emission of certain volatiles are still attractive to parasitoids of the herbivores (11, 40, 90; Supplemental Table 2). Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org MECHANISMS OF PLANT RESPONSES TO INSECT EGGS To activate a defense response, a plant that receives insect eggs first has to detect the eggs. Because plants respond differently to eggs of different insect species (e.g., 40, 83, 87), species-specific, egg- associated cues are expected to elicit specific plant responses. Indeed, the very different types of egg- associated elicitors of plant defense known to date indicate high species specificity. Furthermore, in several plant–insect egg interactions, plants respond not only locally at the site of egg deposition,

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. but also systemically at egg-free sites adjacent to the egg-laden ones (e.g., 17, 40, 51, 83). Hence, the information about egg deposition has to be transmitted within the plant. In this context, we address the questions of how plant responses are elicited by eggs, which phytohormones are involved in intraplant transmission of information about egg deposition, what is known about the molecular basis of egg-induced plant responses, and which phytochemical changes are induced by egg deposition.

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Secretion: covering the eggs

Sources from which elicitors were isolated a. Female accessory reproductive glandular secretion (ARG) b. Male-derived anti-aphrodisiacs in female ARG c. Oviductus communis d. Extracts of females Secretion: filling the e. Crushed eggs interface between eggs and plant surface Source: a, b Source: d Bruchins Various phospholipids

Benzyl cyanide O O CH (CH ) (CH ) OH O 3 2 8 2 12 + 2 N CH3 C H2COR P O N CH O– 3 OH 2 RO CH R1 = -phosphocholine O O O OO H COR1 (CH2)8 (CH2)12 2 Indole C (CH2)7 (CH2)4 CH3 H N R2 = -linoleoyl OH OH O +NH O O OO 3 (CH ) (CH ) P O 2 8 2 14 H COR4,5 R3 -phosphoethanolamine 2 O– = Source: c 4,5RO CH OH OH O 3 R4 palmitoyl Small H2COR C (CH2)14 CH3 = - O O O O proteinaceous (CH2)8 (CH2)6 (CH2)6 compounds O C (CH ) (CH2)7 CH3 OH 2 7 OH R5 = -oleoyl

Figure 3 Elicitors of oviposition-induced plant defense. Sources a and b: Benzyl cyanide isolated from accessory reproductive glands (ARG) of mated Pieris brassicae females (36) induces indirect plant defense and arrestment of egg parasitoids. Sources a and b: Indole isolated from ARG of mated P. rapae (41) induces indirect plant defense and arrestment of egg parasitoids. Source c: Elicitor activity of a

Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org proteinaceous fraction of an oviduct secretion released with eggs of the sawﬂy Diprion pini (57), and eggs of the elm leaf beetle Xanthogaleruca luteola (55, 83), induces indirect plant defense and attraction of egg parasitoids. Source d: Bruchins isolated from extracts of thousands of Callosobruchus maculatus females (32) induce direct plant defense (growth of neoplasms). Phospholipids isolated from extracts of female Sogatella furcifera (128, 129) induce direct plant defense (ovicidal compound). Source e: Although crushed eggs show plant-response-eliciting activity, no chemical structure of an elicitor has been identiﬁed from crushed eggs.

Egg-Associated Secretions as Elicitors of Plant Responses

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. In several insect species, exocrine secretions coating the eggs elicit defensive plant responses. The response to application of these secretions onto plant tissue mimics the response to egg deposition. The secretions not only cover the eggs, but often ﬁll the interface between plant and insect egg and may contain elicitors of plant defense (Figure 3). In Pieris butterﬂies, secretions released from the female accessory reproductive glandular reservoir (Figure 2e) elicit a plant defense response and induce a change in leaf surface chemistry that arrests egg parasitoids (9, 36, 41). Similarly,

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application of a secretion of the accessory reproductive glands of Sesamia nonagrioides (stem borer moth) females onto Zea mays leaves elicits defensive plant responses that retain egg parasitoids on the treated leaves (102). In other insects, an egg-associated secretion that induces defensive plant responses is released from the oviductus communis, i.e., in the elm leaf beetle, X. luteola (83), and in the pine sawfly D. pini (51). A secretion associated with egg deposition by bruchid beetles onto pea pods induces growth of neoplasms. The exact morphological production site of the secretion is unknown; the secretion was squeezed out of the female abdominal tip (33). The production site of the secretion associated with eggs of the stem borer moth Chilo partellus is also unknown. However, ethanolic extracts of the secretion isolated from the eggs induced emission of OIPVs and thus mimicked C. partellus eggs on leaves of maize landraces (118). Secretions associated with eggs have various functions for insects: They may act as lubricants that facilitate gliding of eggs through the reproductive tract (1), as fertilization-supporting agents (73); as egg glue that attaches eggs tightly to plant tissue (124); or as material that protects eggs from environmental harm (e.g., desiccation, rainfall) (61), from microorganisms (78, 101), or from parasitoids and predators (10). Knowledge of the chemical composition of the secretions associated with insect eggs is very limited. The compound classes of female accessory reproductive glandular secretions range from peptides and proteins to polysaccharides and lipids (45). Species-specific compounds of the secretions may induce species-specific plant responses to eggs (e.g., 36, 41). For a few herbivorous insect species, the compounds eliciting plant defensive responses have been characterized or identified. In the elm leaf beetle, X. luteola, and the pine sawfly D. pini, the active principle of the oviduct secretion has been suggested to be a protein, because the OIPV-inducing activity of the secretion ceases after treatment of the secretion with a proteinase (55, 57, 83). The accessory reproductive glandular secretions of P. brassicae and Pieris rapae females only have a plant-defense-eliciting effect when females have already mated; the active elicitor compounds are antiaphrodisiacs received by the females from their males and released with the eggs onto the plants, i.e., benzyl cyanide in P. brassicae and indole in P. rapae (36, 41) (Figure 3). Further elicitors of plant defense against eggs were isolated not directly from the secretions associated with the eggs but from extracts of females producing the secretions. Thousands of female bruchid beetles (B. pisorum, C. maculatus) were used to extract the so-called bruchins, which elicit growth of neoplasms when applied to pods of certain pea lines (32). These bruchins

are long-chained α,ω-diols (C22 to C24) that are mono- or diesteriﬁed by 3-hydroxypropanoic acid (33) (Figure 3). Another novel elicitor of direct plant defense against eggs has been iden- tiﬁed from extracts of females of the planthopper S. furcifera. Application of this extract to rice plants induces the production of the ovicidal compound benzyl benzoate and thus mimics egg

Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org deposition. Application of extracts from males has no such effect (128). Yang et al. (129) reported that lipids identiﬁed from extracts of females induced the production of the ovicide in rice. The identiﬁed lipids are 1,2-dilinoleoyl-sn-glycero-3-phosphocholine, 1,2-dipalmitoyl-sn- glycero-3-phosphoethanolamine, 1-palmitoyl-2-oleoyl-X-glycero-3-phosphoethanolamine, and 1,2-dioleoyl-sn-glycero-3-phosphoethanolamine (127) (Figure 3). In addition to secretions associated with eggs and extracts from females, extracts of crushed eggs elicit plant defensive responses. Aqueous extracts of homogenized bruchid eggs have a

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. neoplasm-inducing effect on pea pods that is similar to the effect of egg-associated secretions or extracts from females (33). Application of homogenized eggs dissected from the ovaries of the stem borer moth S. nonagrioides on maize leaves elicits effects on egg parasitoid behavior similar to those caused by the application of secretions of the accessory reproductive glands and by natural egg deposition (102). Treatment of A. thaliana leaves with the supernatant of crushed eggs of P. brassicae can also mimic natural egg deposition with respect to HR-like necrosis and the strong

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expression of a pathogenesis-related gene (PR-1), a trypsin inhibitor gene (TI), a chitinase gene (CHIT ), and a senescence-associated gene (SAG13) in the immediate vicinity of the application site (99). Application of a lipid fraction of crushed P. brassicae eggs onto A. thaliana leaves has recently been shown to induce expression of PR-1 and pathogen-associated molecular pattern (PAMP)-responsive genes, thus indicating that the response of A. thaliana to P. brassicae eggs shares similarities with a plant’s response to phytopathogens (46). Since the early studies of plant responses to insect eggs, the possible involvement of egg-associated bacteria or fungi in eliciting plant defense has been discussed (5, 110). However, to date researchers have found no evidence that egg-associated microorganisms elicit plant defense against insect eggs (74). The isolation of plant-response-eliciting compounds from egg contents rather than from the outer surface of the egg raises the question as to whether and how internal egg compounds reach the responding plant cell, given that they would need to be transferred through the eggshell, the adhesive glue forming the interface between plant and egg, the lipophilic wax layer of leaves, and the leaf epidermal cell wall. This question was also discussed when high concentrations of jasmonic acid ( JA) were detected inside eggs of several lepidopteran species (121). Concentrations of JA in P. brassicae eggs were found to be similar to those present in untreated A. thaliana leaves, thus rendering JA an unlikely candidate for a plant-defense-eliciting compound of P. brassicae eggs (74). To date, no specific receptor of an egg-associated elicitor localized in a plant’s plasma membrane has been identified. However, an elegant study by Gouhier-Darimont et al. (46) provides the first evidence that an L-type lectin receptor kinase in A. thaliana leaves may be involved in perception of an elicitor derived from egg contents of P. brassicae. The experiments were conducted with extracts of crushed eggs. Further experiments are needed to show whether this receptor candidate also responds to natural egg deposition by P. brassicae.

Plant Hormonal and Molecular Responses to Insect Egg Deposition Both the phytohormone JA and salicylic acid (SA) are known to play a role in mediating plant responses to insect egg deposition (54, 55, 99). JA is involved in egg-induced responses of very different plant species. Enhanced levels of JA or induction of transcription of JA-responsive defensive genes seems to be independent of the mode of egg deposition on the plant. JA is involved in plant responses to eggs laid on unwounded leaves (e.g., eggs of the moth H. zea on tomato; 68), eggs laid on leaf tissue that experienced ovipositional wounding (by, e.g., sawﬂies on pine; 51), or feeding damage by gravid females [e.g., leaf beetles on elm (15, 83), planthoppers on rice (75, 76, 120)].

Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org In addition to JA, SA plays a major role in egg-induced plant responses. It accumulates beneath the eggs of P. brassicae laid on A. thaliana leaves (12). Furthermore, expression of several SA- responsive genes is inducible by P. brassicae and P. rapae egg deposition; expression of PR1 is signiﬁcantly enhanced in leaf tissue beneath the eggs and in close proximity to them (74). Similarly, P. rapae egg deposition enhanced expression of PR1 in B. nigra plants, but only when an HR-like necrosis was visible (42). A defense-suppression effect due to plant treatment with crushed eggs of P. brassicae has been attributed to negative interference of the JA pathway with treatment-induced

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. SA accumulation (12). Further studies are needed to show how JA, SA, and other phytohormones interact in response to insect egg deposition (99). Insect egg deposition changes the expression of genes involved in numerous plant primary and secondary metabolic processes. The ﬁrst insights into how broadly the plant’s transcriptome is affected by insect egg deposition were provided by microarray studies on the interactions between Pieris spp. eggs and Arabidopsis spp. (13, 74) and between Pieris spp. eggs and brussels sprouts

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(B. oleracea var. gemmifera; 36). Later, a large-scale study of egg-induced changes in the transcriptome of elm leaves resulted in a huge database with more than 350,000 expressed sequence tags (ESTs) and showed the enormous range of genes responding to elm leaf beetle egg deposition (15). Other more candidate-gene-approach-oriented studies revealed that insect egg deposition can affect expression of genes involved in, e.g., phytoalexin biosynthesis (23), glucosinolate biosynthesis (44), production of a proteinase inhibitor (68), or terpenoid biosynthesis (6, 70, 71).

Egg-Induced Changes in Phytochemistry Several chemical analyses addressed the question as to which egg-induced changes in phytochemistry contribute to direct defense against the eggs, to priming of defense against hatching larvae, and to indirect defense against the eggs (by affecting egg parasitoid behavior). The most promi- nent example of egg-induced phytochemical changes that directly affect the eggs is the ovicidal compound benzyl benzoate, which is produced by rice plants (Oryza sativa) in response to planthopper (S. furcifera) eggs (109, 115). A concentration of 15.6 ppm benzyl benzoate was found at the oviposition site (108). A few recent studies have addressed the question as to which egg-mediated phytochemical changes affect plant defense against hatching larvae (6, 44). To date, the decrease in larval performance on previously egg-laden plants cannot be explained by phytochemical changes. Prior egg deposition on A. thaliana attenuates the increase in total glucosinolate levels that is induced by P. brassicae larval herbivory. However, these changes probably do not contribute to the impaired performance of P. brassicae larvae on previously egg-laden plants compared with larvae on egg-free plants (44) because a specialized herbivore like P. brassicae is well adapted to the range of glucosinolate levels in its host plants (44, 112). Needles of P. sylvestris did not respond to pine sawfly egg deposition with changes in C:N ratios or changes in the content of water, terpenoids, or phenolic compounds. However, Schroder¨ et al. (105) showed reduced photosynthetic activity of pine in response to pine sawfly egg deposition. Nevertheless, the finding that pine sawfly larvae perform worse on previously egg-laden pine compared with egg-free pine cannot yet be attributed to expected differences in the nutritional quality of egg-laden and egg-free pine (6). Further studies are needed to close this gap in knowledge and to determine which phytochemical changes cause the impaired performance of insect larvae on egg-primed plants. Egg-induced phytochemical changes that result in indirect plant defense by release of OIPVs that attract egg parasitoids have been studied most intensively. Egg-induced changes in plant volatile emissions are primarily quantitative changes that vary after egg deposition (e.g., 22, 40) and with the type of plant and insect species studied (40, 86, 117). Studies on egg-induced changes

Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org in plant odor have revealed that the release of numerous volatile leaf compounds, ranging from terpenoids to green leaf volatiles and isothiocyanates, is affected by egg deposition. Both enhanced and reduced emission of plant volatiles after insect egg deposition have been detected, but to date the pattern of egg-induced odor is not attributable to distinct oviposition behaviors or species (6, 11, 19, 20, 22, 40, 85, 97, 104, 118, 125; Supplemental Table 2). Several studies have shown that egg parasitoids respond positively to egg-induced changes in the leaf surface (9, 26, 36, 41, 91), but so far only one study has addressed the question of how the

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. pattern of leaf surface chemicals changes in response to egg deposition (9). The total quantities of epicuticular waxes in A. thaliana leaves do not change in response to egg deposition by

P. brassicae. However, the fatty acid tetratriacontanoic acid (C34H68O2) occurs in higher quantities and tetracosanoic acid (C24H48O2) in lower quantities on the surface of egg-laden A. thaliana leaves. Hence, insect egg deposition causes a change in the ratio of leaf wax components, which informs parasitoids that host eggs are nearby (9).

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SPECIES SPECIFICITY OF PLANT RESPONSES TO EGGS IN A BI- AND TRITROPHIC CONTEXT To understand the evolutionary ecology of induced plant defenses, it is necessary to study specificity of induction and effects. From a bitrophic perspective, specificity of induction refers to whether various herbivores induce the same response in a plant, whereas specificity of effects per- tains to whether the induced plant response has the same consequences for different herbivores (114). Especially for pathogen-induced defenses, the differential steps from elicitor recognition to signaling pathways have been elucidated and depend on the type and species of attacker (114). Several studies on plant defenses induced by egg deposition have addressed whether the observed responses are specific to the plant and/or herbivore species, as outlined below. In general, this specificity might be due to individual intraspecific as well as typical species- specific plant and insect traits. Plants may vary with respect to inducibility of defense or capacity to perceive defense-eliciting, egg-associated compounds that may be dependent on thickness of leaf epicuticle or on leaf toughness (see Egg-Associated Secretions as Elicitors of Plant Responses, above). Insect traits contributing to the specificity of plant-egg interactions may vary with respect to the egg-specific elicitors of plant defense or the mode of egg deposition (singly or gregariously laid eggs, egg deposition associated with plant damage or not). For bitrophic interactions between plants and eggs of lepidopteran species, plant responses are specific to the interacting organisms, both the plant and the herbivore species. Specificity of both induction and effects was investigated in black mustard, B. nigra, laden with eggs of two lepidopteran species, the specialist butterfly P. brassicae and the generalist moth Mamestra brassicae (92). Both insect species lay their eggs gregariously. Egg deposition by P. brassicae, but not by M. brassicae, induces a plant response (specificity of induction) that impairs subsequent performance of feeding larvae of both species (no specificity of effect on the herbivore) (92). Likewise, HR-like necrosis is induced by egg deposition of only two specialist Pieris species (P. brassicae and P. rapae, the latter with singly laid eggs), not by eggs of the generalist moth M. brassicae laid on the same plant (herbivore specificity, or specificity of induction) (40, 42). Moreover, HR-like necrosis mediated by singly laid H. subflexa eggs is induced in Physalis hosts but not in nonhost plants (e.g., cotton) (plant-species specificity) (96). Because lepidopteran species do not damage plants when laying eggs on them and because similar effects of plant responses were shown for species with gregariously and singly laid eggs, the herbivore specificity of plant–lepidopteran egg interactions is expected to be the result of species-specific elicitors associated with the eggs or their secretions. Suppression of direct antiherbivore plant defense by application of egg extracts on A. thaliana leaves is specific to the feeding insect species. Plant treatment with egg extracts of P. brassicae or the generalist S. littoralis (gregarious species) increases local levels of SA and surprisingly Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org enhances the performance of subsequently feeding larvae of S. littoralis, but not larvae of the specialist P. brassicae (specificity of effect) (12). Specificity of oviposition-induced plant responses has also been observed in tritrophic contexts. Only oviposition by a specialist herbivore (the elm leaf beetle, X. luteola) on elm induces egg parasitoid–attracting OIPVs in the preferred host plant species U. minor. When freshly laid eggs of a generalist (the leaf beetle Galeruca tanaceti ) are transferred onto elm leaves, they do not induce OIPVs attracting egg parasitoids (82–84). Similarly, oviposition by only the most abundant Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. herbivores (the pine sawflies D. pini and N. sertifer)ononlyP. sylvestris, but not on Pinus nigra, induces OIPVs that attract egg parasitoids (herbivore and plant-species specificity) (87). Feeding sawfly larvae do not induce egg parasitoid–attracting volatiles in P. sylvestris (developmental-stage specificity) (87). Oviposition by the specialist P. brassicae induces OIPVs in B. nigra that attract Trichogramma brassicae wasps, whereas oviposition by the generalist moth M. brassicae does not

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(40). Hence, egg-mediated, tritrophic effects are specific to (highly abundant) specialist herbivore species and the plant species. One possible explanation for the observed distinct interactions between egg deposition by specialist herbivores and plants is that plants have developed a counteradaptation to specialized insects that are able to cope with the plant’s secondary metabolites in the feeding stage. Yet, all specificity studies on egg-mediated plant responses that affect larval performance have thus far been conducted with leaf-chewing (lepidopteran or sawfly) larvae. Future studies including specialist and generalist leaf-sucking herbivores should reveal whether indeed specialization and not feeding guilds, as suggested by Ali & Agrawal (3), is predictive for the differential plant responses.

HERBIVORE OFFENSE TRAITS IN RESPONSE TO EGG-INDUCED PLANT DEFENSES Herbivores can avoid or counteract plant defenses, and plants under attack can even become more susceptible to subsequent attackers (e.g., 18, 89, 103, 107). Such counteradaptations of herbivores to plant defenses include behavioral traits of the herbivores (e.g., feeding and oviposition choices and aggregation), morphological characters (e.g., formation of an almost-lighttight insect cuticle when feeding on plants with phototoxins), and chemical traits of the herbivore (e.g., manipulation or suppression of plant metabolites by release of insect enzymes, or sequestration of plant toxins). Nevertheless, herbivore offense traits, which beneﬁt the herbivore, are far less frequently described than plant defense traits (65).

Behavioral Adaptations of the Egg-Laying Female Egg clustering used by the egg-laying female is a common strategy, but its adaptive value is poorly understood (Figure 2f ). It may be advantageous when food plants are patchily distributed or risks of predation or parasitism are high. The probability of each egg being parasitized decreases with increasing number of eggs in an egg clutch (48). Egg parasitoids might be driving forces for egg clustering. On the one hand, most egg parasitoids that were found to use the adult host as a transport vehicle to obtain access to freshly laid eggs attack gregarious hosts because the reward is much greater than the reward for attacking eggs laid singly by a solitary host (39, 60). On the other hand, in a group of eggs or when eggs are stacked, the vulnerability of the inner eggs is reduced, and the female wasp will not parasitize all of the eggs (123). The solitary seed beetle Mimosestes amicus reduces the risk of parasitism by Uscana semifumipennis wasps in a

Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org sophisticated way: It covers a viable egg with inviable ones. This egg-stacking behavior reduces the mortality of the protected eggs (25). However, studies have not provided any indications that egg clustering reduces the risks of parasitoid attraction by OIPVs. In black mustard, B. nigra, both single eggs of P. rapae and egg clutches of P. brassicae induce Trichogramma-attracting OIPVs (40, 42). Although egg aggregation or clustering might not help to reduce indirect, egg-induced plant defenses, it might lower a plant’s direct anti-egg defense. This was shown for the set of interac-

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. tions between Viburnum plants and viburnum leaf beetle (Pyrrhalta viburni ) eggs. This leaf beetle species prefers to deposit eggs on already-egg-infested Viburnum shrubs, an aggregative oviposition behavior. Egg survival increases and twig wound response (i.e., egg crushing; see Egg-Induced Plant Defense Directly Targeting Egg-Laying Females or Eggs) decreases with increasing levels of infestation (27). This behavior is also beneﬁcial for P. viburni because larval performance is positively density-dependent (28).

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Herbivorous insects can even exploit plant defensive responses to avoid intraspeciﬁc competi- tion or assess risk. Female insects can perceive OIPVs and adjust their egg deposition according to the infestation rate and parasitization risk. Indeed, volatiles of noninfested or egg-infested twigs with low egg density attract more elm leaf beetles than volatiles of twigs with high egg densities and severe feeding damage by conspeciﬁcs. Bioassays indicate that female beetles can respond to both egg- and feeding-induced plant volatiles. However, attraction to plant volatiles induced by low egg densities is not correlated to oviposition preference, as more eggs are laid on noninfested twigs (81). Two other studies also found that egg-laying herbivores avoid heavily egg infested plants: Ovipositing spotted stem borer (C. partellus) females avoid egg-infested African forage grass (Brachiaria brizantha), probably owing to egg-induced changes in the emission of plant volatiles (11). P. brassicae females prefer volatiles of noninfested, rather than egg-infested, OIPV-emitting B. nigra plants and lay eggs on the former. Neither egg age nor the occurrence of HR-like necrosis has an effect on these preferences (40).

Manipulation of Plant Defenses by Egg Deposition Extreme cases of plant manipulations by egg deposition are those involving gall insects, which even beneﬁt from the ability of their eggs to induce growth of plant tissue. Most plant galls are caused by insect feeding activity; however, many plant galls in which hymenopterans develop result from egg deposition, which induces limited growth of plant structures for shelter and food provision. Overviews of mechanisms involved in oviposition-induced growth of galls are given by Hilker et al. (56) and Shorthouse & Rohfritsch (111). In gall wasps (Cynipidae) components of the egg in combination with ovipositional wounding cause galls to form (56). Apart from investigations of plant response to manipulations by ovipositing gall insects, a few studies suggest that insect egg deposition may suppress a plant’s antiherbivore defense, as mentioned above. Further studies are needed to elucidate the conditions that favor the insect’s capability to suppress a plant’s antiherbivore defense (12, 94, 99). A highly exciting, but almost unexplored, hypothesis is that an herbivorous insect species that varies its egg-associated, plant-defense-eliciting traits plays a moving-target game. The moving- target strategy has been suggested for plants that vary their phenotypes in response to biotic stress; the model postulates that variability in itself is defensive (2). We suggest that the insect moving target in this context might be due to varying genotypes or phenotypes of eggs. Such variability might counteract the development of efﬁcient plant defensive responses. The variability of HR-like plant responses to eggs gave rise to this hypothesis. Within a plant population, the HR-like necrosis induced by egg deposition varies considerably, even with

Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org identical conditions for plant growth (40, 42, 96). Variation in plant traits might signiﬁcantly contribute to variation in egg-induced HR-like necrosis. However, variation may, of course, also occur in insects. Field studies of both Physalis shrubs (96) and B. nigra (42) found that when multiple eggs were deposited on the same leaf, one egg induced necrosis and another did not. This suggests that the egg-laying female either releases varying amounts of egg-associated secretion or deposits eggs with varying leaf-necrosis-eliciting activity as a result of genetic variation of the lepidopteran eggs and/or varying egg phenotypes. The different egg phenotypes might be due

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. to varying egg-associated microfauna vertically transferred by the mother to her offspring, as suggested by Petzold-Maxwell et al. (96). Indeed, the pest status of an insect can be determined according to different bacterial symbiont genotypes rather than the insect genotype. Hatching rates of eggs laid by a stink bug (Megacopta punctatissima) feeding on crop legumes are higher when the bug harbors the right gut symbiotic bacteria but lower when the latter are exchanged with the wrong gut symbiotic bacteria (59).

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AN EVOLUTIONARY PERSPECTIVE ON PLANT–INSECT EGG INTERACTIONS Central to an understanding of the evolution of associations between herbivorous insects and plants is the debate on host selection by an ovipositing female and whether it is influenced by the relationship between the female’s oviposition preference for certain plant species and performance of the offspring (preference-performance hypothesis, PPH) (e.g., 24, 62, 119). A wide range of theories have been proposed to explain the often-observed mismatches between female choice and offspring performance. A meta-analysis by Gripenberg et al. (47) offered support for the PPH and found an effect of diet breadth on host choice. Preference for good-quality plants is stronger in oligophagous than in monophagous or polyphagous herbivorous insects. Tested variables other than diet breadth, e.g., offspring mobility, pattern of egg distribution, feeding by adults, and type of host plant (woody or herbaceous), have no detectable influence on the positive link between preference and performance (47). Insects with similar diet breadth (feeding niche) and a close phylogenetic relationship are expected to show similar links between oviposition preference and larval performance (24). To the best of our knowledge, the vast majority of the innumerable laboratory studies testing the “mother knows best” principle (79) and linkages between oviposition preference and offspring performance have not included the question as to how the egg stage performed. This phase, between the oviposition event and the larval feeding period, has been almost completely neglected in these types of studies (69). Oviposition preference studies should link not only preference of host plants with performance of larvae, but also females’ preference of plants with survival of eggs. Furthermore, to test for offspring performance, leaves of egg-free plants have usually been offered to larvae after hatching. However, as highlighted in this review, egg deposition can strongly affect plant quality and, subsequently, the performance of the developing larvae. We therefore hypothesize that induction or manipulation of plant defenses by herbivore egg deposition influences the preference-performance relationship. We expect egg deposition to affect the preference-performance relationship especially when oviposition is not preceded or accompanied by feeding activity of adults, i.e., in sawflies, butterflies, and moths. Hence, egg-mediated plant responses might play an important role in the evolution of herbivorous insects and their host plants and might affect host preferences, host shifts, host specificity, and speciation. We recommend including the egg phase and the effects of egg-mediated plant changes on egg survival and larval performance when testing the PPH.

CONCLUSIONS AND FUTURE DIRECTIONS Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org Plants apply a wide repertoire of responses to insect egg deposition. The response is often specific to the herbivore and the plant species. Nevertheless, different types of oviposition behaviors may result in similar ecological effects of plant responses: Both singly and gregariously laid eggs induce direct and indirect plant defense, and both oviposition associated with and oviposition independent of plant damage can induce plant responses with similar ecological effects. We suggest that the specificity of plant responses to eggs is due to species-specific egg-associated elicitor cues, to the

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. quality of plant tissue, and/or to the type of plant cells that receive the cues. However, to test this hypothesis, more egg-associated elicitors of plant defense and more plant receptors of the eliciting compounds have to be identiﬁed. The range of ecological effects mediated by plant responses to eggs is not limited to effects on eggs but extends also to effects on later insect herbivore stages. Results of future studies on performance of herbivorous larvae may depend on whether larval performance is tested under natural conditions (i.e., on plants where larvae hatch from eggs) or

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artiﬁcial conditions (i.e., on egg-free plants where neonates are placed). Despite growing evidence that direct and indirect plant defense against feeding herbivores may be primed by prior egg deposition, further studies are needed to elucidate the mechanisms of this egg-mediated priming of plant antiherbivore defense. Insects that have developed counteradaptations to egg-induced plant defense are expected to release egg-associated cues (effectors) that suppress plant defense or cues that are highly variable; high variability might impede development of targeted plant defense against eggs. More research is needed to further elucidate how insects cope with egg-mediated plant responses that defend against the eggs or warn the plant of upcoming larval feeding damage. The hypothesized intraspeciﬁc variability of egg-associated elicitors of plant defense that might counteract targeted plant defense requires detailed analyses. Furthermore, it will be a challenge to ascertain whether symbiotic bacteria vertically transferred through the egg contribute to insect strategies that circumvent plant defense induced by egg deposition. Finally, additional studies are necessary to elucidate the impact of plant responses to insect egg deposition on colonization of plants by insects and, thus, lay the foundation for the community ecology level of studies on plant–insect egg interactions.

SUMMARY POINTS 1. Insect eggs induce plant responses that can harm the eggs directly and/or inform parasitoids about the presence of host eggs. 2. Several studies indicate that egg deposition can warn a plant of larval herbivory; in these studies, larvae developing on plants with previous egg deposition had impaired performance compared with larvae on egg-free plants, an ecological effect that is suggested to be a priming effect of eggs on antiherbivore plant defense. 3. Performance of herbivorous larvae depends on whether they start their development on plants where they hatched from eggs (the natural condition) or on egg-free plants. 4. Investigators studying oviposition preference–larval performance associations in herbivorous insects should consider that females might choose host plants that have weak defense against the eggs (rather than selecting hosts that will favor optimal larval performance) or plants where eggs will have attenuated or no priming effects on antilarval defense. 5. Several elicitors of plant defense induced by egg deposition are located in secretions released with the eggs.

Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org 6. Different types of egg deposition behavior (singly or gregariously laid eggs, egg deposition associated with or unrelated to plant damage) can induce direct and indirect plant defense as well as plant responses affecting the larvae. 7. Egg-induced plant responses that attract or arrest egg parasitoids are often highly speciﬁc with respect to the plant and herbivore species. 8. Possible counteradaptations of insects to aggressive egg-induced plant responses range from avoidance of egg-laden plants to suppression of egg-induced plant defense to vari- Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. ation of egg-associated elicitors. Some gall insects can even exploit a plant’s ability to respond to egg deposition and use growth of plant tissue around their eggs to shelter their offspring.

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DISCLOSURE STATEMENT The authors are not aware of any afﬁliations, memberships, funding, or ﬁnancial holdings that might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS The authors are supported by grants from the German Research Foundation for funding CRC 973 (M.H. and N.E.F.) and the Netherlands Organisation for Scientific Research (NWO/ALW Veni grant 863.09.002 to N.E.F.). We are very grateful to Marcel Dicke, Wageningen University, and Torsten Meiners, Freie Universitat¨ (FU) Berlin, for helpful comments on an earlier draft of the manuscript, and to Daniel F. Whybrew, Gottingen,¨ for his linguistic corrections. Furthermore, we thank all those who helped designing the figures: Camille Ponzio, Wageningen University, for providing the plant and insect drawings shown in Figure 1; Jennifer Petzold-Maxwell, Wart- burg College, for providing the Heliothis subflexa egg picture (Figure 2b); Ken Loeffler, Cornell University, for providing the viburnum leaf beetle egg pictures (Figure 2c); and Tobias Otte and Elisabeth Eilers, FU Berlin, for their support in preparing Figure 3.

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Annual Review of Entomology Contents Volume 60, 2015

Breaking Good: A Chemist Wanders into Entomology John H. Law pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp1 Multiorganismal Insects: Diversity and Function of Resident Microorganisms Angela E. Douglas ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp17 Crop Domestication and Its Impact on Naturally Selected Trophic Interactions Yolanda H. Chen, Rieta Gols, and Betty Benrey ppppppppppppppppppppppppppppppppppppppppppppp35 Insect Heat Shock Proteins During Stress and Diapause Allison M. King and Thomas H. MacRae pppppppppppppppppppppppppppppppppppppppppppppppppppp59 Termites as Targets and Models for Biotechnology Michael E. Scharf ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp77 Small Is Beautiful: Features of the Smallest Insects and Limits to Miniaturization Alexey A. Polilov ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp103 Insects in Fluctuating Thermal Environments Herv´e Colinet, Brent J. Sinclair, Philippe Vernon, and David Renault ppppppppppppppppp123 Developmental Mechanisms of Body Size and Wing-Body Scaling in Insects pppppppppppppppppppppppppppppppppppppppppppppppppp

Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org H. Frederik Nijhout and Viviane Callier 141 Evolutionary Biology of Harvestmen (Arachnida, Opiliones) Gonzalo Giribet and Prashant P. Sharma ppppppppppppppppppppppppppppppppppppppppppppppppp157 Chorion Genes: A Landscape of Their Evolution, Structure, and Regulation Argyris Papantonis, Luc Swevers, and Kostas Iatrou pppppppppppppppppppppppppppppppppppppp177 Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. Encyrtid Parasitoids of Soft Scale Insects: Biology, Behavior, and Their Use in Biological Control Apostolos Kapranas and Alejandro Tena ppppppppppppppppppppppppppppppppppppppppppppppppppp195

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Extrafloral Nectar at the Plant-Insect Interface: A Spotlight on Chemical Ecology, Phenotypic Plasticity, and Food Webs Martin Heil pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp213 Insect Response to Plant Defensive Protease Inhibitors Keyan Zhu-Salzman and Rensen Zeng pppppppppppppppppppppppppppppppppppppppppppppppppppp233 Origin, Development, and Evolution of Butterfly Eyespots Antónia Monteiro pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp253 Whitefly Parasitoids: Distribution, Life History, Bionomics, and Utilization Tong-Xian Liu, Philip A. Stansly, and Dan Gerling ppppppppppppppppppppppppppppppppppppp273 Recent Advances in the Integrative Nutrition of Arthropods Stephen J. Simpson, Fiona J. Clissold, Mathieu Lihoreau, Fleur Ponton, Shawn M. Wilder, and David Raubenheimer pppppppppppppppppppppppppppppppppppppppppp293 Biology, Ecology, and Control of Elaterid Beetles in Agricultural Land Michael Traugott, Carly M. Benefer, Rod P. Blackshaw, Willem G. van Herk, and Robert S. Vernon ppppppppppppppppppppppppppppppppppppppppppp313 Anopheles punctulatus Group: Evolution, Distribution, and Control Nigel W. Beebe, Tanya Russell, Thomas R. Burkot, and Robert D. Cooper pppppppppppppp335 Adenotrophic Viviparity in Tsetse Flies: Potential for Population Control and as an Insect Model for Lactation Joshua B. Benoit, Geoffrey M. Attardo, Aaron A. Baumann, Veronika Michalkova, and Serap Aksoy ppppppppppppppppppppppppppppppppppppppppppppppppp351 Bionomics of Temperate and Tropical Culicoides Midges: Knowledge Gaps and Consequences for Transmission of Culicoides-Borne Viruses B.V. Purse, S. Carpenter, G.J. Venter, G. Bellis, and B.A. Mullens pppppppppppppppppppp373 Mirid (Hemiptera: Heteroptera) Specialists of Sticky Plants: Adaptations, Interactions, and Ecological Implications Alfred G. Wheeler Jr. and Billy A. Krimmel pppppppppppppppppppppppppppppppppppppppppppppp393 Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org Honey Bee Toxicology Reed M. Johnson ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp415 DNA Methylation in Social Insects: How Epigenetics Can Control Behavior and Longevity Hua Yan, Roberto Bonasio, Daniel F. Simola, Jürgen Liebig, Shelley L. Berger, and Danny Reinberg ppppppppppppppppppppppppppppppppppppppppppppppppp435 Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. Exaggerated Trait Growth in Insects Laura Lavine, Hiroki Gotoh, Colin S. Brent, Ian Dworkin, and Douglas J. Emlen pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp453

viii Contents EN60-FrontMatter ARI 9 December 2014 14:16

Physiology of Environmental Adaptations and Resource Acquisition in Cockroaches Donald E. Mullins ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp473 Plant Responses to Insect Egg Deposition Monika Hilker and Nina E. Fatouros pppppppppppppppppppppppppppppppppppppppppppppppppppppp493 Root-Feeding Insects and Their Interactions with Organisms in the Rhizosphere Scott N. Johnson and Sergio Rasmann ppppppppppppppppppppppppppppppppppppppppppppppppppppp517 Insecticide Resistance in Mosquitoes: Impact, Mechanisms, and Research Directions Nannan Liu pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp537 Vector Ecology of Equine Piroplasmosis Glen A. Scoles and Massaro W. Ueti ppppppppppppppppppppppppppppppppppppppppppppppppppppppp561 Trail Pheromones: An Integrative View of Their Role in Social Insect Colony Organization Tomer J. Czaczkes, Christoph Gr¨uter, and Francis L.W. Ratnieks pppppppppppppppppppppp581 Sirex Woodwasp: A Model for Evolving Management Paradigms of Invasive Forest Pests Bernard Slippers, Brett P. Hurley, and Michael J. Wingﬁeld pppppppppppppppppppppppppppp601 Economic Value of Biological Control in Integrated Pest Management of Managed Plant Systems Steven E. Naranjo, Peter C. Ellsworth, and George B. Frisvold ppppppppppppppppppppppppp621

Indexes

Cumulative Index of Contributing Authors, Volumes 51–60 ppppppppppppppppppppppppppp647 Cumulative Index of Article Titles, Volumes 51–60 ppppppppppppppppppppppppppppppppppppp652

Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org Errata

An online log of corrections to Annual Review of Entomology articles may be found at http://www.annualreviews.org/errata/ento Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only.

Contents ix