Abstract
Many herbivorous insects are mono- or oligophagous, having evolved to select a limited range of host plants. They specifically identify host-plant leaves using their keen sense of taste. Plant secondary metabolites and sugars are thought to be key chemical cues that enable insects to identify host plants and evaluate their quality as food. However, the neuronal and behavioral mechanisms of host-plant recognition are poorly understood. Here, we report a two-factor host acceptance system in larvae of the silkworm Bombyx mori, a specialist on several mulberry species. The first step is controlled by a chemosensory organ, the maxillary palp (MP). During palpation at the leaf edge, the MP detects trace amounts of leaf-surface compounds, which enables host-plant recognition without biting. Chemosensory neurons in the MP are tuned with ultrahigh sensitivity (thresholds of attomolar to femtomolar) to chlorogenic acid (CGA), quercetin glycosides, and β-sitosterol (βsito). Only if these 3 compounds are detected does the larva make a test bite, which is evaluated in the second step. Low-sensitivity neurons in another chemosensory organ, the maxillary galea (MG), mainly detect sucrose in the leaf sap exuded by test biting, allowing larvae to accept the leaf and proceed to persistent biting (feeding). The two-factor host acceptance system reported here may commonly underlie stereotyped feeding behavior in many phytophagous insects and determine their feeding habits.
Highlights
Diet choice is essential for survival in all organisms
We found that ultrasensitive chemosensory neurons in the maxillary palp (MP) of silkworm larvae detect a set of key mulberry compounds, including chlorogenic acid (CGA), quercetin glycosides, and βsito, inducing a test bite
When a silkworm encounters a leaf, it first palpates the leaf edge using a peripheral chemosensory organ known as the maxilla, intermittently bites the edge several times, and engages in continuous biting (2–3 times per second) with its head shaking in the dorsoventral direction along the leaf edge (Fig 1A; S1 Movie)
Summary
Diet choice is essential for survival in all organisms. Many herbivorous insects have adapted to a limited range of host plants by overcoming plant defenses against insect herbivory, resulting in mono- and oligophagous insects (so-called specialist insects) [1]. Specialists are able to precisely distinguish their host plants from other nonhost plants in their ecosystem using chemical senses, including gustation and olfaction [2]. Gustation is important in determining the acceptance or rejection of a potential food source, whereas olfaction is required when searching for host plants from a distance [3].
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