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Secondary plant compounds are strong deterrents of insect oviposition and feeding, but may also be attractants for specialist herbivores. These insect-plant interactions are mediated by insect gustatory receptors ( Grs ) and olfactory receptors ( Ors ). An analysis of the reference genome of the butterfly  Heliconius melpomene , which feeds on passion-flower vines ( Passiflora  spp.), together with whole-genome sequencing within the species and across the  Heliconius  phylogeny has permitted an unprecedented opportunity to study the patterns of gene duplication and copy-number variation (CNV) among these key sensory genes. We report  in silico  gene predictions of 73  Gr  genes in the  H. melpomene  reference genome, including putative CO 2 , sugar, sugar alcohol, fructose, and bitter receptors. The majority of these  Grs  are the result of gene duplications since  Heliconius  shared a common ancestor with the monarch butterfly or the silkmoth. Among  Grs  but not  Ors , CNVs are more common within species in those gene lineages that have also duplicated over this evolutionary time-scale, suggesting ongoing rapid gene family evolution. Deep sequencing (∼1 billion reads) of transcriptomes from proboscis and labial palps, antennae, and legs of adult  H. melpomene  males and females indicates that 67 of the predicted 73  Gr  genes and 67 of the 70 predicted  Or  genes are expressed in these three tissues. Intriguingly, we find that one-third of all  Grs  show female-biased gene expression (n = 26) and nearly all of these (n = 21) are  Heliconius -specific  Grs . In fact, a significant excess of  Grs  that are expressed in female legs but not male legs are the result of recent gene duplication. This difference in  Gr  gene expression diversity between the sexes is accompanied by a striking sexual dimorphism in the abundance of gustatory sensilla on the forelegs of  H. melpomene , suggesting that female oviposition behaviour drives the evolution of new gustatory receptors in butterfly genomes.

Female Behaviour Drives Expression and Evolution of Gustatory Receptors in Butterflies