Eyespots in butterflies reuse the gene network that models antennae, legs and wings

A silky owl butterfly (Taenaris catopsv) with distinctive eye patches on its wings. Credit: Kristof Zyskowski and Yulia Bereshpolova

The findings highlight that complex new traits, such as eye spots, evolve from gene networks that already model pre-existing complex traits in the body.

Eyespots, the circular markings of contrasting colors found on the wings of many butterfly species, are used by these fluttering creatures to intimidate or distract predators. A team of scientists led by Professor Antónia Monteiro from the National University of Singapore (NUS) conducted a research study to better understand the evolutionary origins of these eye spots, and they found that the eye spots appear to originate from the recruitment of a complex network of genes. which already worked in the bodies of butterflies to build antennae, legs and even wings.

“This new study deals with how complex new traits might arise. These complex traits require the contribution of many interacting genes for their development and are often illustrated by the eye of vertebrates or the flagellum of bacteria. In our study, we examined how butterfly eyespots – an example of a complex trait – arose and concluded that a network recruitment approach is taken by butterflies to eyespot creation. We also identified the specific gene network that was likely recruited,” said Professor Monteiro, from the NUS Department of Biological Sciences.

The results were first published in the journal Proceedings of the National Academy of Sciences of the United States on February 16, 2022.

The mystery of the construction of organisms

Understanding gene network recruitment can be approached by imagining a complex computer program with thousands of lines of code, each line representing a simple instruction or function. Within the code are blocks of text, positioned a little further inside the margin, representing subroutines. These subroutines, or sets of instructions that perform specific tasks, are written once in code, but are referenced multiple times by the program during its execution. For this to happen, each subroutine must be given a unique name and referenced in the following code. A complex piece of code often contains many subroutines, where each unique subroutine is written only once in its entirety.

Forest mother of pearl butterfly eye

Close up of an eyespot of the forest mother of pearl butterfly (Protogoniomorpha parhassus). Credit: Emilie Dion, NUS

The same subroutine logic seems to apply to how the process of development is encoded in the structure of an organism. DNA. In this case, the routine is called a gene regulatory network. A gene regulatory network is a chain of instructions that involves the transcription, or silencing, of multiple genes in a time sequence. Organisms are built through the deployment of many such gene regulatory networks, in a precise sequence, during development. The new study by the NUS team has found that the development of eyespots on the wings of butterflies relies on the deployment of a pre-existing genetic regulatory network that was already used to build the antennae, legs and wings of these butterflies. .

The presence of these subroutines had been posited before, primarily because the same genes continued to be discovered as expressed and associated with the development of new traits. However, it was unclear whether the expression of these genes in the new trait represented new lines of genomic code, each calling for the expression of a pre-existing gene, or pre-existing lines of code read one more time. , like a subroutine. in a computer program.

Discover the role of gene network recruitment in novel traits

To understand this, NUS postdoctoral researcher Dr. Heidi Connahs and PhD student Dr. Suriya Murugesan deleted unique DNA regulatory sequences in the genome, but not the genes themselves, and showed that several traits were affected by these mutations. This argues for a single gene regulatory network, or subroutine, underlying the development of all traits. The two pieces of DNA targeted were regulatory switches next to genes Without distal and spatula. The development of eyespots, antennae, legs, and wings was all disrupted when these regions of about 390–700 base pairs were disrupted. “It was amazing to observe how these important complex traits were affected by the same changes in DNA,” Dr. Connahs said.

Murugesan also sequenced the pieces of tissue that develop eye spots on the wings and compared the full set of genes expressed with those expressed in other traits. “Eye spots shared the closest gene expression profile with antennae, but not with legs or other wing tissues, such as the wing margin,” Murugesan said. NUS postdoctoral fellow Dr Yuji Matusoka then looked at three genes expressed in both eye spots and antennae and showed that the regulatory connections between them were identical, with one gene being important in regulating two others. “When I found a patch of cells in the eye-spot region without the expression of the first gene, I realized that the expression of the other two genes was also missing,” Dr. Matusoka said.

“These experiments relied on the discovery of mutations that hit exactly the central cells of the eye spot after embryonic injections that required a lot of patience,” Professor Monteiro said.

Taken together, the study found evidence that the evolution of complex new traits, such as butterfly eyespots, occurs via mutations in the genetic code reminiscent of a pre-existing subroutine in the genome that was already used for other complex traits such as antennae and other limbs. The types of mutations that produce these redeployments of pre-existing gene networks have yet to be discovered, but they are predicted to be ordinary mutations that, by chance, lead to the recall of large pre-existing genomic subroutines involving hundreds of genes. .

The next step in this research is to further test whether the corresponding regulatory sequences of these two genes from eyespotless butterfly species are able to activate gene expression in the eyespot region in species with eyespots. “That would be the icing on the cake,” said Professor Monteiro, “because it further confirms that a genetic sequence from an old subroutine will be recalled to this new location in the body in species with the recall mutation. .”

Reference: “The eyespots of butterflies evolved via the cooptation of an ancestral genetic regulatory network that also shapes the antennae, legs and wings” by Suriya Narayanan Murugesan, Heidi Connahs, Yuji Matsuoka, Mainak Das Gupta, Galen JL Tiong, Manizah Huq, V. Gowri, Sarah Monroe, Kevin D. Deem, Thomas Werner, Yoshinori Tomoyasu and Antónia Monteiro, February 15, 2022, Proceedings of the National Academy of Sciences.
DOI: 10.1073/pnas.2108661119

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