Neurotranscriptomic signatures of natural variation in mate preference learning in two subspecies of Heliconius melpomene butterflies

Many animals change their behavior in response to social experiences by learning. Although social learning is adaptive, not all individuals learn. In Heliconius melpomene, H. m. malleti males respond to 2-day prior failed copulation experience by decreasing courtship, whereas H. m. rosina males do not. Here, we explore the transcriptomic differences in both the neural (brain) and sensory (eyes, antennae) tissues underlying this natural diversity in male aversive mate-preference learning. While the transcriptomic profiles of the two subspecies are inherently different across all three tissues, we found the greatest difference between the good (H. m. malleti), and bad (H. m. rosina) mate-preference learners in the brain, followed by the sensory tissues. Known learning genes and Gene Ontology terms were associated with differences in mate-preference learning, suggesting conserved learning pathways across animals. Genes within putative magic loci associated with colors, odors, and locomotion, were also differentially expressed between H. m. malleti and H. m. rosina, suggesting multimodal sensory processing may drive behavioral variance in these two subspecies. Overall, our study identifies genetic underpinnings for differences in preference learning, both in neural processing and sensory tissues. Selection on these genes/networks could result in preference learning-induced reinforcement, leading to reproductive isolation and speciation.