More Like this

1. The roles of hybridization and habitat fragmentation in the evolution of Brazil’s enigmatic longwing butterflies, Heliconius nattereri and H. hermathena

   https://doi.org/10.1186/s12915-020-00797-1  

   Massardo, Darli; VanKuren, Nicholas W.; Nallu, Sumitha; Ramos, Renato R.; Ribeiro, Pedro G.; Silva-Brandão, Karina L.; Brandão, Marcelo M.; Lion, Marília B.; Freitas, André V.; Cardoso, Márcio Z.; et al (December 2020, BMC Biology)

   null (Ed.)

   Abstract Background Heliconius butterflies are widely distributed across the Neotropics and have evolved a stunning array of wing color patterns that mediate Müllerian mimicry and mating behavior. Their rapid radiation has been strongly influenced by hybridization, which has created new species and allowed sharing of color patterning alleles between mimetic species pairs. While these processes have frequently been observed in widespread species with contiguous distributions, many Heliconius species inhabit patchy or rare habitats that may strongly influence the origin and spread of species and color patterns. Here, we assess the effects of historical population fragmentation and unique biology on the origins, genetic health, and color pattern evolution of two rare and sparsely distributed Brazilian butterflies, Heliconius hermathena and Heliconius nattereri . Results We assembled genomes and re-sequenced whole genomes of eight H. nattereri and 71 H. hermathena individuals. These species harbor little genetic diversity, skewed site frequency spectra, and high deleterious mutation loads consistent with recent population bottlenecks. Heliconius hermathena consists of discrete, strongly isolated populations that likely arose from a single population that dispersed after the last glacial maximum. Despite having a unique color pattern combination that suggested a hybrid origin, we found no genome-wide evidence that H. hermathena is a hybrid species. However, H. hermathena mimicry evolved via introgression, from co-mimetic Heliconius erato , of a small genomic region upstream of the color patterning gene cortex . Conclusions Heliconius hermathena and H. nattereri population fragmentation, potentially driven by historical climate change and recent deforestation, has significantly reduced the genetic health of these rare species. Our results contribute to a growing body of evidence that introgression of color patterning alleles between co-mimetic species appears to be a general feature of Heliconius evolution. 

   more » « less
2. True UV color vision in a female butterfly with two UV opsins

   https://doi.org/10.1242/jeb.242802  

   Finkbeiner, Susan D.; Briscoe, Adriana D. (September 2021, Journal of Experimental Biology)

   ABSTRACT In true color vision, animals discriminate between light wavelengths, regardless of intensity, using at least two photoreceptors with different spectral sensitivity peaks. Heliconius butterflies have duplicate UV opsin genes, which encode ultraviolet and violet photoreceptors, respectively. In Heliconius erato, only females express the ultraviolet photoreceptor, suggesting females (but not males) can discriminate between UV wavelengths. We tested the ability of H. erato, and two species lacking the violet receptor, Heliconius melpomene and Eueides isabella, to discriminate between 380 and 390 nm, and between 400 and 436 nm, after being trained to associate each stimulus with a sugar reward. We found that only H. erato females have color vision in the UV range. Across species, both sexes show color vision in the blue range. Models of H. erato color vision suggest that females have an advantage over males in discriminating the inner UV-yellow corollas of Psiguria flowers from their outer orange petals. Moreover, previous models ( McCulloch et al., 2017) suggested that H. erato males have an advantage over females in discriminating Heliconius 3-hydroxykynurenine (3-OHK) yellow wing coloration from non-3-OHK yellow wing coloration found in other heliconiines. These results provide some of the first behavioral evidence for female H. erato UV color discrimination in the context of foraging, lending support to the hypothesis ( Briscoe et al., 2010) that the duplicated UV opsin genes function together in UV color vision. Taken together, the sexually dimorphic visual system of H. erato appears to have been shaped by both sexual selection and sex-specific natural selection. 

   more » « less
3. Multiple Mechanisms of Photoreceptor Spectral Tuning in Heliconius Butterflies

   https://doi.org/10.1093/molbev/msac067  

   McCulloch, Kyle J.; Macias-Muñoz, Aide; Mortazavi, Ali; Briscoe, Adriana D. (April 2022, Molecular Biology and Evolution)

   Chang, Belinda (Ed.)

   Abstract The evolution of color vision is often studied through the lens of receptor gain relative to an ancestor with fewer spectral classes of photoreceptor. For instance, in Heliconius butterflies, a genus-specific UVRh opsin duplication led to the evolution of UV color discrimination in Heliconius erato females, a rare trait among butterflies. However, color vision evolution is not well understood in the context of loss. In Heliconius melpomene and Heliconius ismenius lineages, the UV2 receptor subtype has been lost, which limits female color vision in shorter wavelengths. Here, we compare the visual systems of butterflies that have either retained or lost the UV2 photoreceptor using intracellular recordings, ATAC-seq, and antibody staining. We identify several ways these butterflies modulate their color vision. In H. melpomene, chromatin reorganization has downregulated an otherwise intact UVRh2 gene, whereas in H. ismenius, pseudogenization has led to the truncation of UVRh2. In species that lack the UV2 receptor, the peak sensitivity of the remaining UV1 photoreceptor cell is shifted to longer wavelengths. Across Heliconius, we identify the widespread use of filtering pigments and co-expression of two opsins in the same photoreceptor cells. Multiple mechanisms of spectral tuning, including the molecular evolution of blue opsins, have led to the divergence of receptor sensitivities between species. The diversity of photoreceptor and ommatidial subtypes between species suggests that Heliconius visual systems are under varying selection pressures for color discrimination. Modulating the wavelengths of peak sensitivities of both the blue- and remaining UV-sensitive photoreceptor cells suggests that Heliconius species may have compensated for UV receptor loss. 

   more » « less
4. The evolution and genetics of sexually dimorphic ‘dual’ mimicry in the butterfly Elymnias hypermnestra

   https://doi.org/10.1098/rspb.2020.2192  

   Ruttenberg, Dee M.; VanKuren, Nicholas W.; Nallu, Sumitha; Yen, Shen-Horn; Peggie, Djunijanti; Lohman, David J.; Kronforst, Marcus R. (January 2021, Proceedings of the Royal Society B: Biological Sciences)

   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 single nucleotide polymorphisms (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 WntA 's role in colour patterning across Nymphalidae, E. hypermnestra females demonstrate the repeatability of the evolution of sexual dimorphism. 

   more » « less
5. A large deletion at the cortex locus eliminates butterfly wing patterning

   https://doi.org/10.1093/g3journal/jkac021  

   Hanly, Joseph J.; Livraghi, Luca; Heryanto, Christa; McMillan, W. Owen; Jiggins, Chris D.; Gilbert, Lawrence E.; Martin, Arnaud; Oliver, ed., B. (January 2022, G3 Genes|Genomes|Genetics)

   Abstract As the genetic basis of natural and domesticated variation has been described in recent years, a number of hotspot genes have been repeatedly identified as the targets of selection, Heliconius butterflies display a spectacular diversity of pattern variants in the wild and the genetic basis of these patterns has been well-described. Here, we sought to identify the mechanism behind an unusual pattern variant that is instead found in captivity, the ivory mutant, in which all scales on both the wings and body become white or yellow. Using a combination of autozygosity mapping and coverage analysis from 37 captive individuals, we identify a 78-kb deletion at the cortex wing patterning locus, a gene which has been associated with wing pattern evolution in H. melpomene and 10 divergent lepidopteran species. This deletion is undetected among 458 wild Heliconius genomes samples, and its dosage explains both homozygous and heterozygous ivory phenotypes found in captivity. The deletion spans a large 5′ region of the cortex gene that includes a facultative 5′UTR exon detected in larval wing disk transcriptomes. CRISPR mutagenesis of this exon replicates the wing phenotypes from coding knock-outs of cortex, consistent with a functional role of ivory-deleted elements in establishing scale color fate. Population demographics reveal that the stock giving rise to the ivory mutant has a mixed origin from across the wild range of H. melpomene, and supports a scenario where the ivory mutation occurred after the introduction of cortex haplotypes from Ecuador. Homozygotes for the ivory deletion are inviable while heterozygotes are the targets of artificial selection, joining 40 other examples of allelic variants that provide heterozygous advantage in animal populations under artificial selection by fanciers and breeders. Finally, our results highlight the promise of autozygosity and association mapping for identifying the genetic basis of aberrant mutations in captive insect populations. 

   more » « less