Species swarms and their caterpillar colonisers: phylogeny and polyphenols determine host plant specificity in New Guinean Lepidoptera

Abstract

The majority of multi-cellular terrestrial life is found in tropical forests and is either an invertebrate or a plant: for decades ecologists have sought to understand why. As global change erodes the list of extant species on our planet quantifying what species remain, along with their origins and ecology, contributes to our ability to preserve ecosystem functioning and resilience. Here we study three feeding guilds of caterpillars (Lepidoptera) and seek to understand the drivers of their diet breadth across four diverse tropical plant genera in Papua New Guinea. Host specificity is central to biodiversity estimates and the resilience of ecological networks. Specifically, we calculate distance-based host specificity in relation to plant phylogenetic relationships alongside chemical and mechanical traits of leaves. In terms of chemical defenses, we focus on the major polyphenol groups, a compound class shared across many plant species. We refine our data exploration using food webs and ordinations to pick out specific traits of relevance to insect host specificity. Our results showed that the degree of specialization for caterpillars took the following order: phylogenetic>polyphenol>mechanical, such that insect specificity was explained best by host phylogeny and polyphenol chemistry in our study system. Leaf mining insects had higher host specificity than those feeding externally. Of the traits studied hexahydroxydiphenoyl derivatives, galloyl derivatives, trichome density, quinic acid derivatives, myricetins and successional index explained the most variation in overall insect community structure. Our findings build on earlier studies of New Guinean rainforest communities and add a mechanistic explanation to previous findings that host genera are functional islands for insect herbivores. Further, we demonstrate that different plant genera combine different defensive traits that appear to drive associated insect diversity. Our approach integrates trait data and phylogeny to explore dimensions of specialization and we welcome metabolomic studies that will provide more detailed explanations for insect-herbivore host use. Finally, chemical diversity is directly linked to organismal diversity and by studying a range of insect herbivore guilds we make a connection between feeding ecology and specialization that will help to predict species interactions and, potentially, the persistence of ecological networks.