Deep cis-regulatory homology of the butterfly wing pattern ground plan

Mazo‐Vargas, Anyi; Langmüller, Anna Maria; Wilder, Alexis; Burg, Karin R. L. van der; Lewis, James J.; Messer, Philipp W.; Zhang, Linlin; Martin, Arnaud; Reed, Robert D.

doi:10.1126/science.abi9407

Cited by 28 publications

(34 citation statements)

References 44 publications

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“…Likewise, several pCREs reside with the bab locus, suggesting the temporal, sex-specific, and quantitative levels of Bab1 and Bab2 expression are under control of more CREs than currently appreciated. These examples raise the possibility that several key trans -regulators of this GRN have their expression controlled by a landscape of CREs similar to what has been observed in the regulation of tetrapod Hox genes [ 33 , 34 ], the butterfly WntA gene [ 35 ], and svb of fruit flies [ 36 , 37 ]. In addition to these known regulatory genes of the pigmentation GRN having multiple pCREs, the roster of pCREs ( S4 Table ) is flush with occurrences of multiple pCREs per gene, including 18 for the mamo locus.…”

Section: Discussionmentioning

confidence: 82%

A novel role for trithorax in the gene regulatory network for a rapidly evolving fruit fly pigmentation trait

et al. 2023

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Animal traits develop through the expression and action of numerous regulatory and realizator genes that comprise a gene regulatory network (GRN). For each GRN, its underlying patterns of gene expression are controlled by cis-regulatory elements (CREs) that bind activating and repressing transcription factors. These interactions drive cell-type and developmental stage-specific transcriptional activation or repression. Most GRNs remain incompletely mapped, and a major barrier to this daunting task is CRE identification. Here, we used an in silico method to identify predicted CREs (pCREs) that comprise the GRN which governs sex-specific pigmentation of Drosophila melanogaster. Through in vivo assays, we demonstrate that many pCREs activate expression in the correct cell-type and developmental stage. We employed genome editing to demonstrate that two CREs control the pupal abdomen expression of trithorax, whose function is required for the dimorphic phenotype. Surprisingly, trithorax had no detectable effect on this GRN’s key trans-regulators, but shapes the sex-specific expression of two realizator genes. Comparison of sequences orthologous to these CREs supports an evolutionary scenario where these trithorax CREs predated the origin of the dimorphic trait. Collectively, this study demonstrates how in silico approaches can shed novel insights on the GRN basis for a trait’s development and evolution.

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Section: Discussionmentioning

confidence: 82%

A novel role for trithorax in the gene regulatory network for a rapidly evolving fruit fly pigmentation trait

et al. 2023

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“…These phenotypic differences may be a direct result of the fixation of independent developmental alterations (e.g., CRE changes) in the two butterfly lineages. Thus, since their split, H. erato and H. melpomene appear to have independently accumulated distinct genetic variations that modified an initially shared developmental system ( 20 ).…”

Section: Discussionmentioning

confidence: 99%

“…Of the ATAC-seq peaks that were more accessible in the hindwing, many were concentrated within 100 kb of the Ubx gene [5.56% (82) and 2.04% (20) in H. erato and H. melpomene, respectively], which is known to be a key gene for insect hindwing specification (23, 24) (Fig. 2B and fig.…”

Section: Dissimilarities In Chromatin Profiles Of Developing Fore-and...mentioning

confidence: 99%

“…Moreover, a third study on WntA suggested that divergent regulatory changes could explain the different melanic wing patterns induced by a CRISPR-Cas9 WntA gene deletion, or knockout (KO), across three pairs of Heliconius mimics (18,19). Overall, these studies are suggesting a divergent regulation of mimetic wing patterning that has evolved from an ancestral developmental plan (20).…”

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confidence: 99%

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High level of novelty under the hood of convergent evolution

Belleghem

Ruggieri

Concha

et al. 2023

Science

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Little is known about the extent to which species use homologous regulatory architectures to achieve phenotypic convergence. By characterizing chromatin accessibility and gene expression in developing wing tissues, we compared the regulatory architecture of convergence between a pair of mimetic butterfly species. Although a handful of color pattern genes are known to be involved in their convergence, our data suggest that different mutational paths underlie the integration of these genes into wing pattern development. This is supported by a large fraction of accessible chromatin being exclusive to each species, including the de novo lineage-specific evolution of a modular optix enhancer. These findings may be explained by a high level of developmental drift and evolutionary contingency that occurs during the independent evolution of mimicry.

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“…In cichlids, for example, a CRE at the gene encoding agouti-related peptide 2 controls variation in strip patterning in two closely related species (Kratochwil et al ., 2018). Conserved CREs were shown to have wide ranging effects on wing patterning in multiple Nymphalidae butterflies (Mazo-Vargas et al ., 2022).…”

Section: Discussionmentioning

confidence: 99%

Colour polymorphism associated with a gene duplication in male wood tiger moths

Brien

Orteu

Yen

et al. 2022

Preprint

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Colour is often used as an aposematic warning signal, with predator learning expected to lead to a single colour pattern within a population. However, there are many puzzling cases where aposematic signals are also polymorphic. The wood tiger moth, Arctia plantaginis, uses bright hindwing colours as a signal of unpalatability, and males have discrete colour morphs which vary in frequency geographically. In Finland, both white and yellow morphs can be found, and these colour morphs also differ in behavioural and life-history traits. Complex polymorphisms such as these are often explained by supergenes. Here, we show that male colour is linked to an extra copy of a yellow family gene that is only present in the white morphs. This white-specific duplication, which we name valkea, is highly upregulated during wing development, and could act to reduce recombination, thus potentially representing a supergene. We also characterise the pigments responsible for yellow, white and black colouration, showing that yellow is partly produced by pheomelanins, while black is dopamine-derived eumelanin. The yellow family genes have been linked to melanin synthesis and behavioural traits in other insect species. Our results add to only a few examples of seemingly paradoxical and complex polymorphisms which are associated with single genes.

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Deep cis-regulatory homology of the butterfly wing pattern ground plan

Cited by 28 publications

References 44 publications

A novel role for trithorax in the gene regulatory network for a rapidly evolving fruit fly pigmentation trait

A novel role for trithorax in the gene regulatory network for a rapidly evolving fruit fly pigmentation trait

High level of novelty under the hood of convergent evolution

Colour polymorphism associated with a gene duplication in male wood tiger moths

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