Hypermetamorphosis in a leaf-miner allows insects to cope with a confined nutritional space

Abstract

International audienceHypermetamorphosis has been described in several Lepidoptera leaf-miner species (mostly Gracillariidae, Epipyropidae, and Phyllocnistidae) and can be defined as a strong modification of the larval morphology associated with a switch in its feeding mode. Evolution of this larval feeding strategy presumably influences nutritional resources that can be exploited and has strong consequences for plant morphology. The following studyfocuses on Phyllonorycter blancardella (Lepidoptera: Gracillariidae), a leaf-miner developing on Malus domestica. We characterize the morphology of larval mouthparts and the resulting morphological impact on leaf tissues. Our results show that first instars do not strongly affect the leaf anatomy and leave most plant cells intact, while later instars significantly disrupt leaf tissues. Additionally, young larvae are ‘‘fluid-feeders’’ and feed on plant cell fluids resulting from the progression of the larvae through the lower layer of the leaf spongy parenchyma. They occupy a feeding niche clearly distinct from later instars that are ‘‘tissue-feeders’’. Hypermetamorphosis in P. blancardella most likely allows insects to cope with a confined nutritional space by partitioning the limited feeding resources, and may help leaf-miners to optimize their nutritio

Hypoxia and hypercarbia in endophagous insects: Larval position in the plant gas exchange network is key

“…This means that the CO 2 accumulated within a mine can diffuse out of the mine toward the adjacent photosynthesizing tissues, and vice versa for O 2 . Further, miner species with transitions in their feeding behavior along their ontogeny, including sap to tissue feeder (Body et al, 2015) or from miner to galler lifestyle (David Giron, personal communication), would be worth investigating in the context of the risk of hypoxia related to the dynamics of the mine structure. A similar lateral system may occur in leaf galls that are small enough to be aligned with leaf surface.…”

Leaf-mining by Phyllonorycter blancardella reprograms the host-leaf transcriptome to modulate phytohormones associated with nutrient mobilization and plant defense

“…They are also key players in the 107 interaction between leaf-miners and their host-plant with an intri-108 cate involvement of insect bacterial symbionts sometimes impli-109 cated (Connor and Taverner, 1997;Kaiser et al, 2010;Body et al, 110 2013; Giron and Glevarec, 2014;Gutzwiller et al, 2015). 111 Leaf-mining and gall-inducing insects likely took advantage of 112 their intimate relationship with their host-plant to manipulate 113 their microenvironment, thus creating insect-generated shelters 114 that avoid plant defenses, buffer against seasonal variations of leaf 115 nutritional quality, and/or allow the insect to consume high nutri-116 tious plant tissues leading to a higher feeding efficiency (Price 117 et al, 1987;Hespeinde, 1991;Connor and Taverner, 1997;Stone 118 and upper parenchyma (Body et al, 2015), resulting in the forma- 136 tion of feeding windows on a characteristic tentiform-shaped mine 137 (Pottinger and LeRoux, 1971;Djemai et al, 2000). As in other 138 leaf-miner systems, P. blancardella creates 'green-islands' around 139 mining caterpillars on yellow (but also green) leaves that provide 140 sugar-rich green tissues as well as creating an enhanced nutritional 141 microenvironment in an otherwise senescent context (Giron et al, 142 2007;Body et al, 2013).…”

Modulation of plant cytokinin levels in the Wolbachia‐free leaf‐mining species Phyllonorycter mespilella

“…The two species are morphologically cryptic (F Dedeine & D Giron, unpubl.). The development of larvae is similar to that of P. blancardella and divided into five instars (Pottinger & Leroux, 1971;Body et al, 2015). The development of larvae is similar to that of P. blancardella and divided into five instars (Pottinger & Leroux, 1971;Body et al, 2015).…”

“…Increased levels of iPR, tZR, and tZ in mines from yellow leaves can allow insects to induce a 'green island' and keep an appropriate nutritional supply in a degenerating context. However, the maintenance of functional green tissues on yellow leaves is of considerable ecological value to the development of the larvae as it allows the insect to maintain a favorable nutritional environment in an otherwise degenerating context providing the leaf-miners with the required nutrients for completing their development before winter (Body et al, 2013(Body et al, , 2015. First, P. blancardella larvae produce and deliver CKs to the plant, especially in yellow leaves, inducing an accumulation of CKs in mines (Zhang et al, 2017).…”

“…They share the same ecological niche and can often be found on the same trees, shoots, or even leaves. The last two instars that consume the lower and upper parenchyma are tissue-feeders, which result in the formation of feeding windows on a characteristic tentiform-shaped mine (Pottinger & Leroux, 1971;Djemai et al, 2000;Body et al, 2015). The first three instars (L1-3) that feed on interstitial fluids are fluid feeders.…”