Inside the horn of plenty: Leaf-mining micromoth manipulates its host plant to obtain unending food provisioning

Abstract

Leaves represent the main resource for herbivorous insects and their performances are mainly a function of leaf nutritional quality. Two feeding strategies are known to optimize the exploitation of leaf resources: leaf-miners that selectively feed on tissues of high nutritional quality and gall-inducers that induce the development of a new tissue showing an enhanced nutritional value. Some leaf-miners are known to also manipulate their nutritional environment, but do not affect plant development. Cases of callus proliferation in leaf-mines have been reported, however, the direct role of the insect in the formation of additional plant cells and the nutritional function of this tissue have never been established. Using an experimental approach, we show that leaf-mining larvae of micromoth, Borboryctis euryae (Lepidoptera: Gracillariidae), that grow on Eurya japonica (Pentaphylacaceae), actively induce callus proliferation within their leaf-mine at the fourth instar. We experimentally demonstrated that, at this developmental stage, the larva feeds exclusively on this newly formed tissue and feeding of the tissue is essential for completing larval stage. Phenological census revealed considerable expansion and variation of fourth instar duration caused by the continuous production of callus. We propose here the “cornucopia” hypothesis which states that the newly produced callus induced by the leaf-mining larvae provides virtually unending nourishment, which in turn allows flexible larval development time. This represents the first example of a leaf-miner manipulating plant development to its benefit, like a gall-inducer. We propose to name this life style “mine-galler”.

The Evolution of Endophagy in Herbivorous Insects

“…We propose that when the influence of gall insects reaches farther from the local vicinity of the gall that competition becomes increasingly relevant as a selective force that can shape the strength and direction of interactions with other herbivorous species. It is likely that revisiting nutrient allocation between various sinks through mass spectrometry imaging (Kaspar et al, 2011), tracing experiments, and manipulating sink strength with transplantation experiments and killing (Guiguet et al, 2018) will provide insight on the role of competition in the ecology and evolution of the endophagous lifestyle.…”

“…Species in the genus Buccalatrix (Bucculatricidae) move from leaf miners to external leaf feeders, while some gracilariids combine two different endophytic habits ( Caloptilia , Parornix ), feeding as miners for the first few instars and then become leaf folders ( Hering, 1951 ; Nakadai and Kawakita, 2016 ). Other gracilariids first feed as leaf miners and then become gall inducers, and this transition involves hypermetamorphosis of mouthparts ( Guiguet et al, 2018 , 2019 ; Guiguet, 2019 ).…”

Volatile production differs between oak leaves infested by leaf-miner Phyllonorycter harrisella (Lepidoptera: Gracillariidae) and galler Neuroterus quercusbaccarum (Hymenoptera: Cynipidae)

“…This includes changes in biosynthesis of jasmonic acid, salicylic acid, abscisic acid or cytokinins (Giron et al, 2016;Zhang, 2017). Such changes can positively affect the nutritive value of the tissue the leaf-miner feeds on and can hamper the direct and indirect chemical defences of the host (Zhang et al, 2016;Guiguet et al, 2018). For example, apple plants infested with Phyllonorycter blancardella emit less sesquiterpenes than healthy ones (Vogler et al, 2010).…”

“…Leaf-miners induce cytokinins (CKs), phytohormones that regulate plant growth and affect senescence (Zhang et al, 2018). Recently, it was shown that a certain leaf-mining species (Borboryctis euryae: Gracillariidae) is able to actively induce callus proliferation (Guiguet et al, 2018). Consequently, such a manipulation can hamper direct and indirect chemical defences of the plant (Giron et al, 2007).…”

Plants make galls to accommodate foreigners: some are friends, most are foes

“…The R. fascians pathosystem is a model for the interplay between plant-and antagonist-produced molecules. The R. fascians strain D188 has a number of essential Virulence genes, which are typically (Schultz et al, 2019) Establish the boundaries of the galler's zone of influence on plant cell growth and development Compare processes plants use to make galls vs callus tissue (Sugiyama, 2018;Guiguet et al, 2018) Compare processes plants use to enhance localized growth (e.g. galls) vs overall growth Compare the plant's style of defense against gallers vs necrotrophs or other biotrophs Are plants really better at suppressing de novo growth than animals?…”