Biology subjects

McDonald, J. M. C.

Publications and source records attributed to McDonald, J. M. C..

4 recordsLinked to original sources

bioRxiv2026

nubbin, ventral veinless, and pdm3 play diverse roles in butterfly wing pattern development

Butterfly wings present a tremendous gallery of colorful patterns, offering a unique opportunity to study how developmental pattern formation processes evolve. We still do not understand the genetic basis of several key aspects of wing pattern development, however. Three paralogous POU domain transcription factors nubbin, ventral veinless (vvl), and pdm3 are all known wing development genes in Drosophila melanogaster. Here we combine gene expression and knockout approaches to show that each of these genes plays multiple novel wing patterning roles in the common buckeye butterfly, Junonia coenia. We found that nubbin controls eyespot pattern determination via a non-cell autonomous repressor-like effect originating at the wing veins, such that nubbin knockouts have larger eyespots. nubbin also regulates pigment identity and scale morphology across the wings. We also found that vvl regulates pigment identity of the discal bands and ventral hindwing. Last, we found that pdm3 is required for determining the outer rings of eyespot patterns, where it is co-expressed with spalt and the lncRNA ivory. pdm3 is also necessary for determining wing margin stripes, where it is again co-expressed with spalt, leading us to propose that the eyespot and wing margin gene regulatory networks could be homologous. Finally, pdm3 affects pigmentation of the ventral hindwing, phenocopying the seasonally-plastic color switch in J. coenia. Together, our work shows that POU domain transcription factors play diverse roles in butterfly wing pattern development and highlights nubbin as one of the first genes implicated in the repressive function of wing veins in color pattern determination. Highlights- Gene expression and knockouts reveal three POU factors regulate butterfly wing color pattern - nubbin regulates eyespot development, likely via a repressor from the wing veins - nubbin controls scale color and morphology across the wing - pdm3 coordinates eyespot development and is co-expressed with spalt and ivory - Expression of genes in the eyespot and wing margin suggests network homology

developmental biology↗

bioRxiv2024

The ivory lncRNA regulates seasonal color patterns in buckeye butterflies

Long non-coding RNAs (lncRNAs) are transcribed elements increasingly recognized for their roles in regulating gene expression. Thus far, however, we have little understanding of how lncRNAs contribute to evolution and adaptation. Here we show that a conserved lncRNA, ivory, is an important color patterning gene in the buckeye butterfly Junonia coenia. ivory overlaps with cortex, a locus linked to multiple cases of crypsis and mimicry in Lepidoptera. Along with a companion paper by Livraghi et. al., we argue that ivory, not cortex, is the color pattern gene of interest at this locus. In J. coenia a cluster of cis-regulatory elements (CREs) in the first intron of ivory are genetically associated with natural variation in seasonal color pattern plasticity, and targeted deletions of these CREs phenocopy seasonal phenotypes. Deletions of different ivory CREs produce other distinct phenotypes as well, including loss of melanic eyespot rings, and positive and negative changes in overall wing pigmentation. We show that the color pattern transcription factors Spineless, Bric-a-brac, and Ftz-f1 bind to the ivory promoter during wing pattern development, suggesting that they directly regulate ivory. This case study demonstrates how cis-regulation of a single non-coding RNA can exert diverse and nuanced effects on the evolution and development of color patterns, including modulating seasonally plastic color patterns. SignificanceThe genomic locus hosting the cortex gene has been linked to numerous cases of color pattern adaptation in moths and butterflies, including crypsis, mimicry, and seasonal polyphenism. Here we show in buckeye butterflies that the actual color pattern gene at the cortex locus is an evolutionarily conserved long non-coding RNA (lncRNA), dubbed ivory, that overlaps with cortex. Compared with other wing pattern genes, ivory stands out because of the highly nuanced, quantitative changes in pigmentation that can be achieved by manipulating adjacent cis-regulatory sequences. This study highlights how lncRNAs can be important factors underlying morphological evolution, and emphasizes the importance of considering non-coding transcripts in comparative genomics.

genetics↗

bioRxiv2023

Butterfly wing iridescence is regulated by araucan, a direct target of optix and spalt

Butterfly wings exhibit a remarkable diversity of structural iridescent colors, yet the genetic regulation of iridescence remains poorly understood. Here, we show that the Iroquois-complex transcription factor gene araucan plays a role in modulating wing scale iridescence in the common buckeye butterfly, Junonia coenia. Using CRISPR-Cas9 knockouts, we demonstrate that loss of araucan function causes dorsal wing scales to shift from golden-brown to blue iridescence, and eyespot center scales to shift from saturated purple-violet to dull grey-brown. These phenotypes are associated with changes in thickness of the lower lamina in scale cells, a structural feature known to influence thin-film interference, along with reduction of pigmentation in ground scales. Together, these results identify araucan as a single transcription factor that determines coloration by simultaneously regulating both photonic architecture and light-absorbing pigmentation, and show that these effects can be regulated in pattern-specific manner. Our findings provide a framework for linking gene regulation to the spatially coordinated evolution of structural and pigmentary components of color.

genetics↗

bioRxiv2020

Sex-specific plasticity and the nutritional geometry of insulin-signaling gene expression in Drosophila melanogaster

1.BackgroundSexual-size dimorphism (SSD) is replete among animals, but while the selective pressures that drive the evolution of SSD have been well studied, the developmental mechanisms upon which these pressures act are poorly understood. Ours and others research has shown that SSD in Drosophila reflects elevated levels of nutritional plasticity in females versus males, such that SSD increases with dietary intake and body size, a phenomenon called sex-specific plasticity (SSP). Additional data indicate that while body size in both sexes responds to variation in protein level, only female body size is sensitive to variation in carbohydrate level. Here we explore whether these difference in sensitivity at the morphological level are reflected by differences in how the insulin/IGF-signaling (IIS) and TOR-signaling pathways respond to changes in carbohydrates and proteins in females versus males, using a nutritional geometry approach. ResultsThe IIS-regulated transcripts of 4E-BP and InR most strongly correlated with body size in females and males respectively, but neither responded to carbohydrate level and so could not explain the sex-specific response to body size to dietary carbohydrate. Transcripts regulated by TOR-signaling did, however, respond to dietary carbohydrate in a sex-specific manner. In females, expression of dILP5 positively correlated with body size, while expression of dILP2,3 and 8, was elevated on diets with a low concentration of both carbohydrate and protein. In contrast, we detected lower levels of dILP2 and 5 protein in the brains of females fed on low concentration diets. We could not detect any effect of diet on dILP expression in males. ConclusionAlthough females and males show sex-specific transcriptional responses to changes in protein and carbohydrate, the patterns of expression do not support a simple model of the regulation of body-size SSP by either insulin-or TOR-signaling. The data also indicate a complex relationship between carbohydrate and protein level, dILP expression and dILP peptide levels in the brain. In general, diet quality and sex both affect the transcriptional response to changes in diet quantity, and so should be considered in future studies that explore the effect of nutrition on body size.

developmental biology↗