Abstract
Due to its fundamental role in shaping host selection behavior, we have analyzed the chemosensory repertoire of Chrysomela lapponica. This specialized leaf beetle evolved distinct populations which shifted from the ancestral host plant, willow (Salix sp., Salicaceae), to birch (Betula rotundifolia, Betulaceae). We identified 114 chemosensory candidate genes in adult C. lapponica: 41 olfactory receptors (ORs), eight gustatory receptors, 17 ionotropic receptors, four sensory neuron membrane proteins, 32 odorant binding proteins (OBPs), and 12 chemosensory proteins (CSP) by RNA‐seq. Differential expression analyses in the antennae revealed significant upregulation of one minus‐C OBP (Clap OBP27) and one CSP (Clap CSP12) in the willow feeders. In contrast, one OR (Clap OR17), four minus‐C OBPs (Clap OBP02, 07, 13, 20), and one plus‐C OBP (Clap OBP32) were significantly upregulated in birch feeders. The differential expression pattern in the legs was more complex. To narrow down putative ligands acting as cues for host discrimination, the relative abundance and diversity of volatiles of the two host plant species were analyzed. In addition to salicylaldehyde (willow‐specific), both plant species differed mainly in their emission rate of terpenoids such as (E,E)‐α‐farnesene (high in willow) or 4,8‐dimethylnona‐1,3,7‐triene (high in birch). Qualitatively, the volatiles were similar between willow and birch leaves constituting an “olfactory bridge” for the beetles. Subsequent structural modeling of the three most differentially expressed OBPs and docking studies using 22 host volatiles indicated that ligands bind with varying affinity. We suggest that the evolution of particularly minus‐C OBPs and ORs in C. lapponica facilitated its host plant shift via chemosensation of the phytochemicals from birch as novel host plant.
Highlights
Phytophagous beetles have undergone a 140 million years lasting period of coevolution and coadaptation with their host plants (Labandeira & Currano, 2013; Wang, Zhang, & Jarzembowski, 2013)
Within the peripheral chemosensory system, relatively minor and nonrandom changes in a subset of chemosensory genes contribute to population divergence in C. lapponica with respect to their two different hosts
Among the odorant binding proteins (OBPs) upregulated in the antennae of the birch-feeding population (BFP) compared to the antennae of the willow-feeding population (WFP), we found one classic, one plus-C, and three minus-C OBPs
Summary
Phytophagous beetles have undergone a 140 million years lasting period of coevolution and coadaptation with their host plants (Labandeira & Currano, 2013; Wang, Zhang, & Jarzembowski, 2013). The evolution of the sensory repertoire could provoke and reinforce adaptations of insects to new hosts Such host plant shifts have occurred during the evolutionary history of the leaf beetle subtribe Chrysomelina (Chrysomelidae, Chrysomeloidea). The populations of C. lapponica selecting different host plant families represent an excellent model system to investigate the role of the chemosensory system during and after host plant shifts by herbivorous insects. We test the hypothesis that the populations of C. lapponica which shifted their host plant species from willow to birch changed expression of components of the chemosensory repertoire in comparison to populations which kept their original host plant species, that is, willow. The chi-square test was used to test for significant differences between responses of the individuals from both populations
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