Biology subjects

VanKuren, N.

Publications and source records attributed to VanKuren, N..

2 recordsLinked to original sources

bioRxiv2022

Conserved signaling pathways antagonize and synergize with co-opted doublesex to control development of novel mimetic butterfly wing patterns

Novel phenotypes are increasingly recognized to have evolved by co-option of conserved genes into new developmental contexts, yet the impact of co-option on existing developmental programs remains obscure. Here we provide insight into this process by characterizing the consequences of doublesex co-option on wing color pattern development in Papilio swallowtail butterflies. doublesex is the master regulator of insect sex differentiation but has been co-opted to control the switch between discrete mimetic and non-mimetic, male-like color patterns in Papilio polytes and its close relatives. Here we show that development of the mimetic color pattern in P. polytes is caused by a pulse of dsx expression early in female wing development that results in a corresponding pulse of differential expression that both alters color pattern development and quickly becomes decoupled from dsx expression itself. Differentially expressed genes were enriched in canonical Wnt and Hedgehog signaling pathway genes, but case studies of key genes using RNAi and antibody stains suggested opposing, novel roles for the two pathways in mimetic color pattern development. The pulse of Dsx expression caused Engrailed, the key transcription factor effector of Hh signaling, to gain anterior expression in early pupal wing development. However, Dsx and En became decoupled by mid-pupal development when En pre-figured melanic and red patterns and Dsx pre-figured white patterns. In contrast, Wnt signaling antagonizes Dsx in restricted regions of the wing to refine the mimetic color pattern. Our results therefore provide strong experimental evidence that dsx co-option significantly altered spatiotemporal activities of conserved wing patterning pathways to promote and refine the development of a novel adaptive color pattern. Altogether, our findings provide strong evidence for how co-opted genes can both cause and elicit changes to established gene regulatory networks during the evolution and development of novel phenotypes.

evolutionary biology↗

bioRxiv2021

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

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.

developmental biology↗