Griese, E. | Search bioRxiv

bioRxiv2019

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

Evolutionary arms-races between plants and herbivores have been proposed to generate key innovations that can drive diversification of the interacting species. Recent studies reveal that plant traits that target herbivore insect eggs are widespread throughout the plant kingdom. Within the Brassicaceae family, some plants express a hypersensitive response (HR)-like necrosis underneath the eggs of specialist cabbage white butterflies (Pieridae) that leads to eggs desiccating or dropping of the leaf. Here, we studied the evolutionary basis of this trait, its egg-killing effect on and elicitation by specialist butterflies, by screening 31 Brassicaceae species and nine Pieridae species. We show that induction of HR-like necrosis by pierid egg deposition is clade-specific in the economically important Brassiceae tribe (Brassica crops and close-relatives) and in the first-branching genus Aethionema. The necrosis is elicited only by pierid butterflies that feed on Brassicaceae plants; four Pieris and Anthocharis cardamines butterflies, of which the larvae are specialists on Brassicaceae, elicited a HR-like necrosis. Eggs of pierid butterflies that feed on Rhamnaceae (Gonepteryx rhamni) or Fabaceae (Colias spp.) however, did not elicit such a leaf necrosis. Finally, eggs of Aglais io, a species of the sister group Nymphalidae, did not elicit any visible response. Counter-adaptations to HR-like necrosis might have evolved by insect deposition of eggs in clusters or on inflorescences. 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 chemical defence traits against caterpillars.

evolutionary biology↗

bioRxiv2019

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

According to the preference-performance hypothesis (PPH), also known as mother-knows-best hypothesis, herbivorous insects prefer those plants for oviposition, which yield the best offspring performance. Yet, most studies testing the PPH neglect the possibility that plant responses to insect eggs may affect both egg survival and larval performance. Here, we tested the PPH by studying responses of seven Brassicaceae plant species to oviposition by two cabbage white species. When including the egg phase, our study supports the mother-knows-best hypothesis: larvae of Pieris rapae (solitary) or P. brassicae (gregarious) gained most weight on those plant species which had received most eggs (B. nigra or B. montana, respectively). However, our experiments did not reveal any relationship between oviposition preference and egg survival. Brassicaceous species are known to respond to these butterfly eggs with a hypersensitive response (HR)-like necrosis, which can lower egg survival. Pieris eggs frequently induced necrosis in five of the tested plant species. Survival of clustered P. brassicae eggs was unaffected by HR-like in four of the five species. Therefore, our experiments did not reveal any relationship between P. brassicae egg survival and oviposition preference. Females of P. rapae preferred oviposition on plant species which most frequently showed HR-like necrosis. Remarkably, although egg survival was lower on HR-like plants, larval biomass was higher compared to plants without a necrosis. We conclude that egg survival does not seem to be a deciding factor for oviposition choices. However, egg-mediated plant responses might be important to explain the PPH of the two Pieris species.\n\nLay summaryEgg-laying preferences of herbivorous insects can often be linked to offspring performance. Commonly, the fate of insect eggs and the plant responses to the eggs have been ignored when studying the link between preference and performance. By including the egg phase, our study supports the mother-knows-best hypothesis, explained by butterfly oviposition and associated egg and larval performances on different plant species. We especially found that egg-mediated responses seem a deciding factor for butterfly oviposition choices.

ecology↗