Host-specific leaf-mining behaviour of holometabolous insect larvae in the early Permian

Abstract

Leaf-mining is a complex insect feeding behaviour that provides various advantages for reproduction success. The evolutionary origin within the holometabolan clade was hypothesised to have first occurred in the early Mesozoic. We re-examined the controversial feeding trace of Asteronomus maeandriformis, which is abundant in an early Permian plant fossil assemblage from central Germany. We applied multiple optical and chemical analysis techniques to unravel the distinctive morphological patterns of these insect traces. The feeding traces represent tunnels within the leaf laminae, pointing to an endophytic feeding style. In addition, we found numerous oviposition sites that exhibit a direct association with the tunnels and were most likely produced by the same organisms. At the investigated locality, more than 80% of the abundant foliage of Autunia conferta (Peltaspermales) was affected, indicating a host-specific mass infestation by the producer. Our results unequivocally show that endophytic feeding behaviour evolved in the holometabolan clade at least by the earliest Permian and, therefore, more than 40 Ma earlier than hypothesised. The findings reveal complex organism interactions in late Palaeozoic ecosystems that may have evolved in response to global environmental change, leading to drier conditions in the palaeotropics.