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From the formation of embryonic appendages to the color of wings: Conserved and novel roles of aristaless1 in butterfly development

View ORCID ProfileErick X. Bayala, Nicholas VanKuren, Darli Massardo, Marcus Kronforst
doi: https://doi.org/10.1101/2021.12.02.470931
Erick X. Bayala
1Department of Ecology & Evolution, University of Chicago, Chicago, IL 60637
2Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637
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  • ORCID record for Erick X. Bayala
  • For correspondence: ebayala@uchicago.edu
Nicholas VanKuren
1Department of Ecology & Evolution, University of Chicago, Chicago, IL 60637
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Darli Massardo
1Department of Ecology & Evolution, University of Chicago, Chicago, IL 60637
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Marcus Kronforst
1Department of Ecology & Evolution, University of Chicago, Chicago, IL 60637
2Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637
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Abstract

Highly diverse butterfly wing patterns have emerged as a powerful system for understanding the genetic basis of phenotypic variation. While the genetic basis of this pattern variation is being clarified, the precise developmental pathways linking genotype to phenotype are not well understood. The gene aristaless, which plays a role in appendage patterning and extension, has been duplicated in Lepidoptera. One copy, aristaless1, has been shown to control a white/yellow color switch in the butterfly Heliconius cydno, suggesting a novel function associated with color patterning and pigmentation. Here we investigate the developmental basis of al1 in embryos, larvae and pupae using new antibodies, CRISPR/Cas9, RNAi, qPCR assays of downstream targets and pharmacological manipulation of an upstream activator. We find that Al1 is expressed at the distal tips of developing embryonic appendages consistent with its ancestral role. In developing wings, we observe Al1 accumulation within developing scale cells of white H. cydno during early pupation while yellow scale cells exhibit little Al1 at this timepoint. Reduced Al1 expression is also associated with yellow scale development in al1 knockouts and knockdowns. We also find that Al1 expression appears to downregulate the enzyme Cinnabar and other genes that synthesize and transport the yellow pigment, 3–Hydroxykynurenine (3-OHK). Finally, we provide evidence that Al1 activation is under the control of Wnt signaling. We propose a model in which high levels of Al1 during early pupation, which are mediated by Wnt, are important for melanic pigmentation and specifying white portions of the wing while reduced levels of Al1 during early pupation promote upregulation of proteins needed to move and synthesize 3-OHK, promoting yellow pigmentation. In addition, we discuss how the ancestral role of aristaless in appendage extension may be relevant in understanding the cellular mechanism behind color patterning in the context of the heterochrony hypothesis.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted December 03, 2021.
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From the formation of embryonic appendages to the color of wings: Conserved and novel roles of aristaless1 in butterfly development
Erick X. Bayala, Nicholas VanKuren, Darli Massardo, Marcus Kronforst
bioRxiv 2021.12.02.470931; doi: https://doi.org/10.1101/2021.12.02.470931
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From the formation of embryonic appendages to the color of wings: Conserved and novel roles of aristaless1 in butterfly development
Erick X. Bayala, Nicholas VanKuren, Darli Massardo, Marcus Kronforst
bioRxiv 2021.12.02.470931; doi: https://doi.org/10.1101/2021.12.02.470931

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