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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 (ClapOBP27) and one CSP (ClapCSP12) in the willow
feeders. In contrast, one OR (ClapOR17), four minus-C
OBPs (ClapOBP02, 07, 13, 20),
and one plus-C
OBP (ClapOBP32) 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.