Divergent sensory transcriptomic profiles in positive and negative learning in a butterfly

Mate preference learning, where individuals learn to prefer or avoid specific phenotypes during mate selection, is pervasive across animal taxa and influences reproductive isolation and trait evolution. Despite its significance, the genetic basis underlying the associated valence attribution (whether to prefer or avoid) remains largely unclear. Both in terms of what genes are associated with attributing valence, and whether valence attribution is associated with transcriptional changes in both sensory and higher cognitive tissues, or is restricted to the brain. Here, we investigate the neurogenomic basis of positive and negative mate preference learning using Bicyclus anynana butterflies. We put females in positive or negative learning scenarios, as well as a naive control, and compared their transcriptomic profiles across three sensory and cognitive tissues: antennae, eyes, and brain using RNA-sequencing. Our results reveal tissue-specific transcriptional responses, with the antennae showing higher transcriptomic changes during negative learning and the eyes showing higher transcriptomic changes during positive learning, relative to the naive control, indicating that valence attribution during learning may not be restricted to transcriptional changes in the brain. We identified a subset of genes in each tissue whose expression patterns changed with valence, as well as genes linked to classical conditioning pathways, supporting the hypothesis that imprinting-like learning and classical conditioning share molecular mechanisms. Our findings suggest that valence attribution in mate preference learning involves tissue-specific transcriptional responses in sensory and cognitive tissues, emphasising the role of peripheral sensory systems in modulating learned mate preferences.