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Gilbert, L. E.

Publications and source records attributed to Gilbert, L. E..

6 recordsLinked to original sources

The gene ivory:mir-193 controls scale type differentiation in Heliconius butterflies

The ivory:mir-193 locus is a genetic hotspot underlying melanic wing pattern variation across Lepidoptera, acting as a master regulator of melanic scale fate. This includes the genus Heliconius, where aposematic mimicry is driven by three scale cell types: light Type I, dark-melanic Type II, and red Type III scales. We tested functions of ivory:mir-193 in Heliconius using CRISPR-induced somatic mosaic knockouts of ivory and mir-193 across multiple pattern morphs. Knockouts converted Type II scales to Type I scales. Effects on Type III scales varied among and within individuals, indicating that ivory:mir-193 is permissive for Type III development. Using single-nucleus RNA-seq, we profiled the transcriptional landscape of H. melpomene-{Delta}78k mutants lacking mir-193. Loss of mir-193 produced readthrough transcription, consistent with a model where miR-193 acts as a co-transcriptional terminator. These data show that ivory drives wing pattern variation, while mir-193 mediates downstream diversity in scale fate across Lepidoptera.

evolutionary biology↗

Ancient inversion polymorphisms are locally adaptive in a widespread butterfly species

Wide-ranging species are subject to varying biotic and abiotic selection pressures across their distribution. While local adaptation does not manifest in obvious morphological changes, population genomic studies can reveal cryptic diversity and provide insights into local adaptive processes. In this study, we investigated the biogeographic history and genomic diversity across the range of the zebra longwing butterfly Heliconius charithonia, a species with a widespread distribution in the Neotropics, but which is phenotypically homogenous across its range. We examined whole genome sequence data from 55 individuals from the eight described subspecies. We infer that there were at least two distinct colonization events of the Caribbean islands from the mainland. The second colonization wave occurred relatively recently, accounting for the genetic homogeneity observed across the species range. Despite low divergence across most of the genome, two large non-recombining genomic regions showed deeply divergent haplotypes that correspond to chromosomal inversions. Phylogenetic analyses indicate ancient origins of these inversion polymorphisms, and there is no evidence that they were introgressed from another extant lineage of Heliconius. These ancient polymorphisms are likely maintained by heterogeneous selection across the landscape, with the inversion on chromosome 19 likely playing a role in local adaptation to cold and desiccation. Our findings underscore the importance of genomic analysis in uncovering hidden diversity and adaptation in phenotypically homogenous species and highlight the significant role of chromosomal inversions in driving local adaptation.

evolutionary biology↗

Cis-regulatory modes of Ultrabithorax inactivation in butterfly forewings

Hox gene clusters encode transcription factors that drive regional specialization during animal development: e.g. the Hox factor Ubx is expressed in the insect metathoracic (T3) wing appendages and differentiates them from T2 mesothoracic identities. Hox transcriptional regulation requires silencing activities that prevent spurious activation and regulatory crosstalks in the wrong tissues, but this has seldom been studied in insects other than Drosophila, which shows a derived Hox dislocation into two genomic clusters that disjoined Antennapedia (Antp) and Ultrabithorax (Ubx). Here we investigated how Ubx is restricted to the hindwing in butterflies, amidst a contiguous Hox cluster. By analysing Hi-C and ATAC-seq data in the butterfly Junonia coenia, we show that a Topologically Associated Domain (TAD) maintains a hindwing-enriched profile of chromatin opening around Ubx. This TAD is bordered by a Boundary Element (BE) that separates it from a region of joined wing activity around the Antp locus. CRISPR mutational perturbation of this BE releases ectopic Ubx expression in forewings, inducing homeotic clones with hindwing identities. Further mutational interrogation of two non-coding RNA encoding regions and one putative cis-regulatory module within the Ubx TAD cause rare homeotic transformations in both directions, indicating the presence of both activating and repressing chromatin features. We also describe a series of spontaneous forewing homeotic phenotypes obtained in Heliconius butterflies, and discuss their possible mutational basis. By leveraging the extensive wing specialization found in butterflies, our initial exploration of Ubx regulation demonstrates the existence of silencing and insulating sequences that prevent its spurious expression in forewings.

genomics↗

Sex-linked gene traffic underlies the acquisition of sexually dimorphic UV color vision in Heliconius butterflies

Butterflies have photoreceptor cells that are sensitive to the ultraviolet part of the spectrum due to ultraviolet-sensitive rhodopsin (UVRh), a gene that has been duplicated in the Heliconius genus. In individuals expressing UVRh1 and UVRh2, electrophysiological and behavioral studies demonstrate that these opsin proteins enable discrimination of UV wavelengths. This behavioral trait varies between species, being absent in H. melpomene and limited to females in H. erato. To identify the evolutionary origins of this trait, we first examined UV color vision in H. charithonia, a species related to H. erato in the sara/sapho group. We found that this species also has sexually dimorphic UV color vision. To identify the genetic basis of this trait, we built a reference-grade genome assembly of H. charithonia. We discovered that one duplicate, UVRh1, is present on the W chromosome, making it obligately female-specific. We employed gDNA PCR assays of UVRh1 across the Heliconius genus. In species with sexually dimorphic UVRh1 mRNA expression, UVRh1 gDNA is absent in males, whereas in species with sexually monomorphic UVRh1 mRNA expression, UVRh1 gDNA is found in both sexes. The presence or absence of male UVRh1 expression across the Heliconius phylogeny supports a model where sexual dimorphism was acquired early via movement of a gene duplication to the W-chromosome. We used CRISPR-Cas9 to engineer a deletion in the UVRh1 locus in female H. charithonia and use immunohistochemistry to show that UVRh1 protein expression is absent in mutant tissue, similar to that of males. Our results show that a rare behavioral phenotype, sex-specific UV color vision, was acquired via sex chromosome gene traffic of a duplicated UV rhodopsin.

evolutionary biology↗

A macromutation eliminates colour patterning in captive butterflies

Captive populations often harbor variation that is not present in the wild due to artificial selection. Recent efforts to map this variation have provided insights into the genetic and molecular basis of variation. Heliconius butterflies display a large array of pattern variants in the wild and the genetic basis of these patterns has been well-described. Here we sought to identify the genetic basis of 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 78kb deletion at the cortex wing patterning locus as the ivory mutation. 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 5UTR 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, 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.

genetics↗

Egg cannibalism by passion vine specialist Disonycha Chevrolat beetles (Coleoptera: Chrysomelidae: Galerucinae: Alticini)

Cannibalistic behavior is now recognized to be an important component of nutritional ecology in both carnivorous and herbivorous species, including many beetle families (Englert and Thomas 1970; Beaver 1974; Dickinson 1992; Bartlett 1987; Alabi et al. 2008). This habit was historically viewed by an incidental outcome of unnaturally crowded laboratory situations with little ecological importance (Fox 1975), but it is increasingly acknowledged that cannibalism represents a potentially advantageous behavior (Richardson et al. 2010). Here we report on multiple cases of egg cannibalism, or conspecific oophagy, by adults of two species of passion vine (Passiflora Linnaeus: Passifloraceae) specialist flea beetles in the genus Disonycha Chevrolat (Coleoptera: Chrysomelidae: Galerucinae: Alticini). This is the first report of egg cannibalism from the Galerucinae, and to our knowledge, only the fourth report of egg cannibalism by adults in the Chrysomelidae; the other three reports are of adult Chrysomelinae species eating conspecific eggs (Dickinson 1992; McCauley 1992; Schrod et al. 1996). We conclude this note with several questions raised by our observations, followed by a discussion that may contribute to explanations of this behavior.

animal behavior and cognition↗