Plants employ various defences killing the insect attacker in an early stage. Oviposition by cabbage white butterflies (Pieris spp.) on brassicaceous plants, including Brassica nigra, induces a hypersensitive response (HR) - like leaf necrosis promoting desiccation of eggs. To gain a deeper insight into the arms race between butterflies and plants, we conducted field and greenhouse experiments using different B. nigra genotypes. We investigated variation in HR and consequent survival of P. brassicae egg clusters. Impact of egg density, distribution type and humidity on HR formation and egg survival was tested. HR differed among plant genotypes as well as plant individuals. Egg density per plant did not affect HR formation. Remarkably, egg survival did not depend on the formation of HR, unless butterflies were forced to lay single eggs. Larval hatching success from single eggs was lower on plants expressing HR. This may be due to increased vulnerability of single eggs to low humidity conditions at necrotic leaf sites. We conclude that effectiveness of HR-like necrosis in B. nigra varies with plant genotype, plant individual and the type of egg laying behaviour (singly or clustered). By clustering eggs, cabbage white butterflies can escape the egg-killing, direct plant defence trait.
Induction of plant defences, specifically in response to herbivore attack, can save costs that would otherwise be needed to maintain defences even in the absence of herbivores. However, plants may suffer considerable damage during the time required to mount these defences against an attacker. This could be resolved if plants could respond to early cues, such as egg deposition, that reliably indicate future herbivory. We tested this hypothesis in a field experiment and found that egg deposition by the butterfly Pieris brassicae on black mustard (Brassica nigra) induced a plant response that negatively affected feeding caterpillars. The effect cascaded up to the third and fourth trophic levels (larval parasitoids and hyperparasitoids) by affecting the parasitisation rate and parasitoid performance. Overall, the defences induced by egg deposition had a positive effect on plant seed production and may therefore play an important role in the evolution of plant resistance to herbivores.
Summary Evolutionary arms‐races between plants and insect herbivores have long been proposed to generate key innovations such as plant toxins and detoxification mechanisms that can drive diversification of the interacting species. A novel front‐line of plant defence is the killing of herbivorous insect eggs. We test whether an egg‐killing plant trait has an evolutionary basis in such a plant–insect arms‐race. Within the crucifer family (Brassicaceae), some species express a hypersensitive response (HR)‐like necrosis underneath butterfly eggs (Pieridae) that leads to eggs desiccating or falling off the plant. We studied the phylogenetic distribution of this trait, its egg‐killing effect on and elicitation by butterflies, by screening 31 Brassicales species, and nine Pieridae species. We show a clade‐specific induction of strong, egg‐killing HR‐like necrosis mainly in species of the Brassiceae tribe including Brassica crops and close relatives. The necrosis is strongly elicited by pierid butterflies that are specialists of crucifers. Furthermore, HR‐like necrosis is linked to PR1 defence gene expression, accumulation of reactive oxygen species and cell death, eventually leading to egg‐killing. Our findings suggest that the plants’ egg‐killing trait is a new front on the evolutionary arms‐race between Brassicaceae and pierid butterflies beyond the well‐studied plant toxins that have evolved against their caterpillars.
The preference-performance hypothesis (PPH) states that herbivorous female insects prefer to oviposit on those host plants that are best for their offspring. Yet, past attempts to show the adaptiveness of host selection decisions by herbivores often failed. Here, we tested the PPH by including often neglected oviposition-induced plant responses, and how they may affect both egg survival and larval weight. We used seven Brassicaceae species of which most are common hosts of two cabbage white butterfly species, the solitary Pieris rapae and gregarious P. brassicae. Brassicaceous species can respond to Pieris eggs with leaf necrosis, which can lower egg survival. Moreover, plant-mediated responses to eggs can affect larval performance. We show a positive correlation between P. brassicae preference and performance only when including the egg phase: 7-dayold caterpillars gained higher weight on those plant species which had received most eggs. Pieris eggs frequently induced necrosis in the tested plant species. Survival of clustered P. brassicae eggs was unaffected by the necrosis in most tested species and no relationship between P. brassicae egg survival and oviposition preference was found. Pieris rapae preferred to oviposit on plant species most frequently expressing necrosis although egg survival was lower on those plants. In contrast to the lower egg survival on plants expressing necrosis, larval biomass on these plants was higher than on plants without a necrosis. We conclude that egg survival is not a crucial factor for oviposition choices but rather egg-mediated responses affecting larval performance explained the preference-performance relationship of the two butterfly species.
18According to the preference-performance hypothesis (PPH), also known as 'mother-knows-best 19 hypothesis', herbivorous insects prefer those plants for oviposition, which yield the best offspring 20 performance. Yet, most studies testing the PPH neglect the possibility that plant responses to insect 21 eggs may affect both egg survival and larval performance. Here, we tested the PPH by studying 22 36 37 Keywords: Preference-performance hypothesis, Hypersensitive response, Brassicaceae, Pieridae, 38 egg-killing, priming 39 40Lay summary: 41 Egg-laying preferences of herbivorous insects can often be linked to offspring performance. 42 Commonly, the fate of insect eggs and the plant responses to the eggs have been ignored when 43 3 studying the link between preference and performance. By including the egg phase, our study 44 supports the 'mother-knows-best hypothesis', explained by butterfly oviposition and associated egg 45 and larval performances on different plant species. We especially found that egg-mediated 46 responses seem a deciding factor for butterfly oviposition choices. 47 48 4 49
13Evolutionary arms-races between plants and herbivores have been proposed to generate key 14 innovations that can drive diversification of the interacting species. Recent studies reveal that plant 15 traits that target herbivore insect eggs are widespread throughout the plant kingdom. Within the 16 Brassicaceae family, some plants express a hypersensitive response (HR)-like necrosis underneath 17 the eggs of specialist cabbage white butterflies (Pieridae) that leads to eggs desiccating or dropping 18 of the leaf. Here, we studied the evolutionary basis of this trait, its egg-killing effect on and 19 elicitation by specialist butterflies, by screening 31 Brassicaceae species and nine Pieridae species. 20We show that induction of HR-like necrosis by pierid egg deposition is clade-specific in the 21 economically important Brassiceae tribe (Brassica crops and close-relatives) and in the first-22 branching genus Aethionema. The necrosis is elicited only by pierid butterflies that feed on 23 Brassicaceae plants; four Pieris and Anthocharis cardamines butterflies, of which the larvae are 24 specialists on Brassicaceae, elicited a HR-like necrosis. Eggs of pierid butterflies that feed on 25 well-studied chemical defence traits against caterpillars. 31 32 Key words: induced plant defences, counter adaptation, coevolution, plant-insect interaction, egg 33 deposition, hypersensitive response 34 35 36 37
Plant response to butterfly eggs: inducibility, severity and success of egg-killing leaf necrosis depends on plant genotype and egg clustering
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