Cortex cis-regulatory switches establish scale colour identity and pattern diversity in Heliconius

Livraghi, Luca; Hanly, Joseph J.; Bellghem, Steven M Van; Montejo‐Kovacevich, Gabriela; Heijden, Eva Sm van der; Loh, Ling Sheng; Ren, Anna; Warren, Ian A.; Lewis, James J.; Concha, Carolina; Hebberecht, Laura; Wright, Charlotte; Walker, Jonah M.; Foley, Jessica; Goldberg, Zachary H; Arenas-Castro, Henry; Salazar, Camilo; Perry, Michael W.; Papa, Riccardo; Martin, Arnaud; McMillan, W. Owen; Jiggins, Chris D.

doi:10.7554/elife.68549

Cited by 52 publications

(72 citation statements)

References 87 publications

(162 reference statements)

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“…transcription factors optix (Reed et al, 2011) and aristaless (Westerman et al, 2018), signalling ligand WntA (Martin et al, 2012;Mazo-Vargas et al, 2017) and cycle-cell regulator cortex (Nadeau et al, 2016;Saenko et al, 2019). Thus, the establishment of the colour patterns takes place through a specific kinetic of these genes during metamorphosis and wing formation (Connahs et al, 2016;Hines et al, 2012;Livraghi et al, 2021).…”

Section: Indeed Offspring Of Crosses Between Individuals Of Different...mentioning

confidence: 99%

“…To this end, we sequenced RNA from multiple tissues and developmental stages to generate a reference transcriptome for M. marsaeus -the first to date for an ithomiine species -as a tool to investigate gene expression in the two subspecies phasiana and rileyi. We focussed on two stages of pupal wing discs, where colour patterns form in butterflies (Connahs et al, 2016;Hines et al, 2012;Livraghi et al, 2021), and in adult female antennae, where chemical signals are detected, to screen for differentially expressed genes between subspecies and throughout development. We also undertook a candidate gene approach and looked more specifically at the expression of genes known to be involved in colour pattern variation and in chemosensory activity in other Lepidoptera.…”

Section: Significancementioning

confidence: 99%

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Comparative transcriptome analysis at the onset of speciation in a mimetic butterfly—The Ithomiini Melinaea marsaeus

Piron‐Prunier

Persyn

Legeai

et al. 2021

J of Evolutionary Biology

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Ecological speciation entails divergent selection on specific traits, and ultimately on the developmental pathways responsible for these traits. Selection can act on gene sequences, but also on regulatory regions responsible for gene expression. Mimetic butterflies are a relevant system for speciation studies because wing color pattern (WCP) often diverges between closely related taxa, and is thought to drive speciation through assortative mating and increased predation on hybrids. Here we generate the first transcriptomic resources for a mimetic butterfly of the tribe Ithomiini, Melinaea marsaeus, to examine patterns of differential expression between two subspecies and between tissues that express traits that likely drive reproductive isolation; WCP and chemosensory genes. We sequenced whole transcriptomes of three life stages to cover a large catalogue of transcripts and we investigated differential expression between subspecies in pupal wing discs and antennae. Eighteen known WCP genes were expressed in wing discs and 115 chemosensory genes were expressed in antennae, with a remarkable diversity of chemosensory protein genes. Many transcripts were differentially expressed between subspecies, including two WCP genes and one odorant receptor. Our results suggest that in M. marsaeus the same genes as in other mimetic butterflies are involved in traits causing reproductive isolation, and point at possible candidates for the differences in those traits between subspecies. Differential expression analyses of other developmental stages and body organs and functional studies are needed to confirm and expand these results. Our work provides key resources for comparative genomics in mimetic butterflies, and more generally in Lepidoptera.

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Section: Indeed Offspring Of Crosses Between Individuals Of Different...mentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

Comparative transcriptome analysis at the onset of speciation in a mimetic butterfly—The Ithomiini Melinaea marsaeus

Piron‐Prunier

Persyn

Legeai

et al. 2021

J of Evolutionary Biology

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“…In recent years, reverse genetics research has revealed a surprising connection between the molecular machinery underlying the development of pigmented wing patterns and the ultrastructure of butterfly scales in various species (Zhang, Mazo-Vargas and Reed, 2017; Concha et al ., 2019; Fenner et al ., 2020; Livraghi et al ., 2021). However, our QTL are not associated with any known colour pattern gene of large or small effect in Heliconius ( aristaless, WntA, vvl, cortex and optix - located on chromosomes 1, 10, 13, 15 and 18 respectively) (Nadeau, 2016).…”

Section: Discussionmentioning

confidence: 99%

The genetic basis of structural colour variation in mimeticHeliconiusbutterflies

et al. 2021

Preprint

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Structural colours, produced by the reflection of light from ultrastructures, have evolved multiple times in butterflies. Unlike pigmentary colours and patterns, little is known about the genetic basis of these colours. Reflective structures on wing-scale ridges are responsible for iridescent structural colour in many butterflies, including the Müllerian mimics Heliconius erato and Heliconius melpomene. Here we quantify aspects of scale ultrastructure variation and colour in crosses between iridescent and non-iridescent subspecies of both of these species and perform quantitative trait locus (QTL) mapping. We show that iridescent structural colour has a complex genetic basis in both species, with offspring from crosses having wide variation in blue colour (both hue and brightness) and scale structure measurements. We detect two different genomic regions in each species that explain modest amounts of this variation, with a sex-linked QTL in H. erato but not H. melpomene. We also find differences between species in the relationships between structure and colour. Our results suggest that these species have followed different evolutionary trajectories in their convergent evolution of similar structural colour. This study provides a starting point for determining the genetic basis of structural colouration more broadly.

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“…Most changes have been mapped to just four major effect pigment patterning genes: optix, cortex, aristaless1, and WntA (Figure 3B) [40,[46][47][48][49][50][51]. Responsible for establishing wing scale cell identity and competence to respond to TFs more directly involved in pigmentation [reviewed by 51]), cortex and WntA act at a higher tier in the GRN (Figure 3B, top): cortex is necessary to specify "Type II/III" scales [52]; and optix is responsible for further differentiation into Type III scales and promotion of red ommochrome production, while repressing the melanin pathway [53] (Figure 3B, middle right). In the absence of cortex, cells take on the "Type I" fate in which aristaless1 dictates white or yellow pigmentation via repression of yellow ommochrome production [54] (Figure 3B, middle left).…”

Section: Evolution Of the Heliconius Pigmentation Grnmentioning

confidence: 99%

Common Themes and Future Challenges in Understanding Gene Regulatory Network Evolution

Schember

Halfon

2022

Cells

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A major driving force behind the evolution of species-specific traits and novel structures is alterations in gene regulatory networks (GRNs). Comprehending evolution therefore requires an understanding of the nature of changes in GRN structure and the responsible mechanisms. Here, we review two insect pigmentation GRNs in order to examine common themes in GRN evolution and to reveal some of the challenges associated with investigating changes in GRNs across different evolutionary distances at the molecular level. The pigmentation GRN in Drosophila melanogaster and other drosophilids is a well-defined network for which studies from closely related species illuminate the different ways co-option of regulators can occur. The pigmentation GRN for butterflies of the Heliconius species group is less fully detailed but it is emerging as a useful model for exploring important questions about redundancy and modularity in cis-regulatory systems. Both GRNs serve to highlight the ways in which redeployment of trans-acting factors can lead to GRN rewiring and network co-option. To gain insight into GRN evolution, we discuss the importance of defining GRN architecture at multiple levels both within and between species and of utilizing a range of complementary approaches.

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Cortex cis-regulatory switches establish scale colour identity and pattern diversity in Heliconius

Cited by 52 publications

References 87 publications

Comparative transcriptome analysis at the onset of speciation in a mimetic butterfly—The Ithomiini Melinaea marsaeus

Comparative transcriptome analysis at the onset of speciation in a mimetic butterfly—The Ithomiini Melinaea marsaeus

The genetic basis of structural colour variation in mimeticHeliconiusbutterflies

Common Themes and Future Challenges in Understanding Gene Regulatory Network Evolution

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