Butterfly eyespots reuse gene regulatory network that patterns antennae,
legs and wings

Date:
February 16, 2022
Source:
National University of Singapore
Summary:
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
conducted a research study to better understand the evolutionary
origins of these eyespots, and they discovered that eyespots appear
to have derived from the recruitment of a complex network of genes
that was already operating in the body of the butterflies to build
antennae, legs, and even wings.



FULL STORY ========================================================================== Eyespots, the circular markings of contrasting colours 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 Anto'nia Monteiro from the National University of Singapore
(NUS) conducted a research study to better understand the evolutionary
origins of these eyespots, and they discovered that eyespots appear to
have derived from the recruitment of a complex network of genes that
was already operating in the body of the butterflies to build antennae,
legs, and even wings.


========================================================================== "This new study addresses how novel complex traits might originate. These complex traits require the input of many interacting genes for their development, and are often illustrated by the vertebrate eye, or
the bacteria flagellum. In our study, we looked at the how butterfly
eyespots -- an example of a complex trait -- came about and concluded
that a network recruitment approach is adopted by butterflies for the
creation of eyespots. We have also identified the specific network of
genes that was likely recruited," said Prof Monteiro, who is from the
NUS Department of Biological Sciences.

The findings were first published in the journal Proceedings of the
National Academy of Sciences on 16 February 2022.

The mystery of how organisms are built Understanding gene network
recruitment can be approached by imagining a complex computer program
with thousands of lines of code, with each line representing a simple instruction or function. Within the code are blocks of text, positioned
a bit further inward from the margin, representing subroutines. These subroutines, or sets of instructions that perform specific tasks, are
written once in the code, but are referred to repeatedly by the program
as it runs. For this to occur, each subroutine has to be given a unique
name, and referred to in the subsequent code. A complex bit of code often contains many subroutines, where each unique subroutine is written only
once in full.

The same subroutine logic appears to hold true for how the process of development is encoded in an organism's DNA. In this case, the subroutine
is called a gene regulatory network. A gene regulatory network is a
chain of instructions that involve the transcription, or silencing,
of several genes in a temporal 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 discovered
that the development of eyespots on the wings of butterflies relies on
the deployment of a pre-existing gene regulatory network that was already
being used to build the antennae, legs and wings of those butterflies.



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

Discovering the role of gene network recruitment in novel traits To
figure this out, NUS postdoctoral fellow Dr Heidi Connahs and doctoral
student Mr Suriya Murugesan deleted unique DNA regulatory sequences in
the genome, but not the genes themselves, and showed that multiple traits
were affected by these mutations. This argues for a single gene regulatory network, or subroutine, underlying the development of all the traits. The
two pieces of DNA that were targeted were regulatory switches next to the
genes Distal-less and spalt. The development of eyespots, antennae, legs,
and wings were all disrupted when these regions of around 390-700 base
pairs were disrupted. "It was amazing to observe how these significant
complex traits were affected by the same changes in DNA," said Dr Connahs.

Mr Murugesan also sequenced the pieces of tissue that develop eyespots
on the wings and compared the complete set of expressed genes with those expressed in other traits. "Eyespots shared the closest gene expression
profile with antennae, but not with legs or other wing tissue, such as
the wing margin," said Mr Murugesan. NUS postdoctoral fellow, Dr Yuji
Matusoka, then examined three genes expressed in both eyespots 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 eyespot region without the expression
of the first gene, I realised that the expression of the other two genes
was also missing," said Dr Matusoka.

"These experiments relied on discovering mutations that hit exactly the
eyespot central cells after embryonic injections which required a lot
of patience," said Prof Monteiro.

Overall, the study highlighted that the evolution of novel complex traits,
such as butterfly eyespots, proceeds via mutations in the genetic code
that recall a pre-existent 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 are still left to be discovered, but they are predicted
to be ordinary mutations that, by chance, lead to the recall of large pre-existent genomic sub-routines involving hundreds of genes.

The next step in this research is to further test whether the
corresponding regulatory sequences from these two genes from butterfly
species without eyespots are able to activate gene expression in the
eyespot region in species with eyespots. "This would be the icing
on the cake," said Prof Monteiro, "because it further confirms
that a genetic sequence from an old subroutine will get recalled
to that novel place in the body in species with the recall mutation." ========================================================================== Story Source: Materials provided by
National_University_of_Singapore. Note: Content may be edited for style
and length.


========================================================================== Related Multimedia:
* Distinctive_eyespots_on_butterfly_wings ========================================================================== Journal Reference:
1. Suriya Narayanan Murugesan, Heidi Connahs, Yuji Matsuoka, Mainak Das
Gupta, Galen J. L. Tiong, Manizah Huq, V. Gowri, Sarah Monroe,
Kevin D.

Deem, Thomas Werner, Yoshinori Tomoyasu, Anto'nia
Monteiro. Butterfly eyespots evolved via cooption of an ancestral
gene-regulatory network that also patterns antennae, legs, and
wings. Proceedings of the National Academy of Sciences, 2022; 119
(8): e2108661119 DOI: 10.1073/ pnas.2108661119 ==========================================================================

Link to news story: https://www.sciencedaily.com/releases/2022/02/220216095830.htm

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