Insect egg-killing: a new front on the evolutionary arms-race between Brassicaceae plants and Pierid butterflies

Abstract

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

Priming by Timing: Arabidopsis thaliana Adjusts Its Priming Response to Lepidoptera Eggs to the Time of Larval Hatching

“…These plant responses to insect eggs are known to be associated with increased egg mortality, as has been shown for B. nigra responding to Pieris rapae and Pieris napi eggs ( Shapiro and DeVay, 1987 ; Fatouros et al, 2014 ), P. sylvestris responding to sawfly eggs ( Bittner et al, 2017 ), and S. dulcamara responding to eggs of a moth ( Geuss et al, 2017 ). While also A. thaliana Col-0 ecotype shows HR-like symptoms (chlorosis; Reymond, 2013 ) and ROS accumulation ( Gouhier-Darimont et al, 2013 ), no detrimental effects of these responses to P. brassicae eggs are known ( Griese et al, 2019 ). The increase of SA levels in response to eggs also mediates the plant’s protection from phytopathogens ( Hilfiker et al, 2014 ).…”

Plant responses to butterfly oviposition partly explain preference–performance relationships on different brassicaceous species

“…Furthermore, future studies need to explore whether clustering of eggs by P. brassicae and a high number of singly laid eggs for P. rapae may evolved as counter adaptations against the egg-killing leaf necrosis. Other countermeasures of pierid butterflies against egg-induced plant defenses include oviposition on inflorescence stems instead of leaves, as occurs in some other pierid species feeding on Brassicaceae (P. napi and Anthocharis cardamines) (Griese et al 2019) and feeding preference for flowers when they are available (A. cardamines and P. brassicae) (Wiklund and Åhrberg 1978;Smallegange et al 2007).…”

Great chemistry between us: The link between plant chemical defenses and butterfly evolution

“…Recent studies on this group have shown that Brassicaceae have evolved diverse antiherbivore defense traits against pierid herbivores, including the attraction of butterfly-parasitoids and eggkilling necrosis reactions (Fatouros et al, 2014;Griese et al, 2019).…”