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Dietary shifts may act to ease energetic constraints and allow organisms to optimise life-history traits.Heliconiusbutterflies differ from other nectar-feeders due to their unique ability to digest pollen, which provides a reliable source of amino acids to adults. Pollen-feeding has been associated with prolonged adult lifespan and increased fertility, yet there is a lack of empirical data demonstrating how pollen consumption influences key fitness traits, including chemical defences and adult body weight, as well as fertility over the long lifespan. Here, we investigate the effect of pollen-feeding on fertility, weight and chemical defences, as well as offspring defences, controlling for butterfly age and sex. Recently emergedHeliconius eratobutterflies of similar size were fed for 14 or 45 days on one of three diets: sugar solution only, or sugar solution replenished with either supplement or pollen. At the end of the experiment, oviposition assays were performed to evaluate fertility, and afterwards all butterflies and eggs were weighed and used for target metabolomics to quantify cyanogenic glucosides (CG). We found that there is an age-specific and sex-specific effect of pollen-feeding on butterfly weight, with both the sugar-only and amino-acid supplement diets reducing the weight of old females (45d), but not young females (14d) or males of any age. Females fed only sugar significantly reduce their egg-laying through adulthood, whereas females that have access to pollen maintain their fertility. Diet had a significant effect on the maintenance of the chemical defence of females, but not males. Curiously, even though females that have access to pollen are heavier, more toxic and lay more eggs, this does not translate into improvements in offspring defences, as eggs from butterflies of all ages and diet treatment had similar CG content. Our results emphasise the importance of controlling for age-specific and sex-specific effects in studies of life-history evolution and demonstrate that dietary novelty can relax energetic constraints.

Heliconiusbutterflies, a speciose genus of Müllerian mimics, represent a classic example of an adaptive radiation that includes a range of derived dietary, life history, physiological and neural traits. However, key lineages within the genus, and across the broader Heliconiini tribe, lack genomic resources, limiting our understanding of how adaptive and neutral processes shaped genome evolution during their radiation. We have generated highly contiguous genome assemblies for nine new Heliconiini, 29 additional reference-assembled genomes, and improve 10 existing assemblies. Altogether, we provide a major new dataset of annotated genomes for a total of 63 species, including 58 species within the Heliconiini tribe. We use this extensive dataset to generate a robust and dated heliconiine phylogeny, describe major patterns of introgression, explore the evolution of genome architecture, and the genomic basis of key innovations in this enigmatic group, including an assessment of the evolution of putative regulatory regions at theHeliconiusstem. Our work illustrates how the increased resolution provided by such dense genomic sampling improves our power to generate and test gene-phenotype hypotheses, and precisely characterize how genomes evolve.