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Sexual dimorphism is a major component of morphological variation across the tree of life, but the mechanisms underlying phenotypic differences between sexes of a single species are poorly understood. We examined the population genomics and biogeography of the common palmfly Elymnias hypermnestra, a dual mimic in which female wing colour patterns are either dark brown (melanic) or bright orange, mimicking toxic Euploea and Danaus species, respectively. As males always have a melanic wing colour pattern, this makes E. hypermnestra a fascinating model organism in which populations vary in sexual dimorphism. Population structure analysis revealed that there were three genetically distinct E. hypermnestra populations, which we further validated by creating a phylogenomic species tree and inferring historical barriers to gene flow. This species tree demonstrated that multiple lineages with orange females do not form a monophyletic group, and the same is true of clades with melanic females. We identified two SNPs near the colour patterning gene WntA that were significantly associated with the female colour pattern polymorphism, suggesting that this gene affects sexual dimorphism. Given that WntA's role in colour patterning across Nymphalidae, E. hypermnestra females demonstrate the repeatability of the evolution of sexual dimorphism.

Sexual dimorphism is a major component of morphological variation across the tree of life, but the mechanisms underlying phenotypic differences between sexes of a single species are poorly understood. We examined the population genomics and biogeography of the common palmfly Elymnias hypermnestra, a dual mimic in which female wing colour patterns are either dark brown (melanic) or bright orange, mimicking toxic Euploea and Danaus species, respectively. As males always have a melanic wing colour pattern, this makes E. hypermnestra a fascinating model organism in which populations vary in sexual dimorphism. Population structure analysis revealed that there were three genetically distinct E. hypermnestra populations, which we further validated by creating a phylogenomic species tree and inferring historical barriers to gene flow. This species tree demonstrated that multiple lineages with orange females do not form a monophyletic group, and the same is true of clades with melanic females. We identified two SNPs near the colour patterning gene WntA that were significantly associated with the female colour pattern polymorphism, suggesting that this gene affects sexual dimorphism. Given that WntA's role in colour patterning across Nymphalidae, E. hypermnestra females demonstrate the repeatability of the evolution of sexual dimorphism.

Additional file 1: Table S1. Sample and sequencing information for Brazilian Heliconius hermathena and H. nattereri generated in this study. Table S2.Heliconius hermathena and H. nattereri genome sequencing data. Table S3. Samples used for mitochondrial genome assemblies using NOVOplasty (Dierckxens et al., 2017, Nuc Acids Res). Table S4. Sample information for other Heliconius species used in this study. Table S5. Summary statistics of nucleotide diversity per site (pi) and Tajima’s D calculated in 100 kb genome-wide. Table S6. Numbers of substitutions in Heliconius nattereri and relatives. Table S7. Numbers of substitutions in Heliconius hermathena and relatives. Table S8. Whole genome mean FST and 95% empirical confidence interval between H. hermathena populations. Table S9. Whole genome mean FST and 95% empirical confidence interval between H. erato populations. Table S10. Whole genome mean FST and 95% empirical confidence interval between H. melpomene populations. Table S11. Nucleotide diversity, overall and pairwise FST estimated for H. hermathena mitochondrial genomes. Table S12. Patterson’s D statistics calculated in 10 kb windows across all autosomes. H. erato samples are from French Guiana, the geographically closest population to H. hermathena.

Additional file 1: Table S1. Sample and sequencing information for Brazilian Heliconius hermathena and H. nattereri generated in this study. Table S2.Heliconius hermathena and H. nattereri genome sequencing data. Table S3. Samples used for mitochondrial genome assemblies using NOVOplasty (Dierckxens et al., 2017, Nuc Acids Res). Table S4. Sample information for other Heliconius species used in this study. Table S5. Summary statistics of nucleotide diversity per site (pi) and Tajima’s D calculated in 100 kb genome-wide. Table S6. Numbers of substitutions in Heliconius nattereri and relatives. Table S7. Numbers of substitutions in Heliconius hermathena and relatives. Table S8. Whole genome mean FST and 95% empirical confidence interval between H. hermathena populations. Table S9. Whole genome mean FST and 95% empirical confidence interval between H. erato populations. Table S10. Whole genome mean FST and 95% empirical confidence interval between H. melpomene populations. Table S11. Nucleotide diversity, overall and pairwise FST estimated for H. hermathena mitochondrial genomes. Table S12. Patterson’s D statistics calculated in 10 kb windows across all autosomes. H. erato samples are from French Guiana, the geographically closest population to H. hermathena.

The monarch butterfly (Danaus plexippus) complements its iconic migration with diapause, a hormonally controlled developmental program that contributes to winter survival at overwintering sites. Although timing is a critical adaptive feature of diapause, how environmental cues are integrated with genetically-determined physiological mechanisms to time diapause development, particularly termination, is not well understood. In a design that subjected western North American monarchs to different environmental chamber conditions over time, we modularized constituent components of an environmentally-controlled, internal diapause termination timer. Using comparative transcriptomics, we identified molecular controllers of these specific diapause termination components. Calcium signaling mediated environmental sensitivity of the diapause timer, and we speculate that it is a key integrator of environmental condition (cold temperature) with downstream hormonal control of diapause. Juvenile hormone (JH) signaling changed spontaneously in diapause-inducing conditions, capacitating response to future environmental condition. Although JH is a major target of the internal timer, it is not itself the timer. Epigenetic mechanisms are implicated to be the proximate timing mechanism. Ecdysteroid, JH, and insulin/insulin-like peptide (IIS) signaling are major targets of the diapause program used to control response to permissive environmental conditions. Understanding the environmental and physiological mechanisms of diapause termination sheds light on fundamental properties of biological timing, and also helps inform expectations for how monarch populations may respond to future climate change.

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