The developmental gene disco regulates diel-niche evolution in adult moths

Sondhi, Y.; Messcher, R. L.; Bellantuano, A. J.; Storer, C. G.; Cinel, S. D.; Godfrey, R. K.; Glass, D.; St. Laurent, R. A.; Hamilton, C. A.; Earl, C.; Brislawn, C. J.; Kitching, I. J.; Bybee, S. M.; Theobald, J. C.; Kawahara, A. Y.

doi:10.1101/2023.05.28.542320

bioRxiv · 10.1101/2023.05.28.542320

The developmental gene disco regulates diel-niche evolution in adult moths

Sondhi, Y.·Messcher, R. L.·Bellantuano, A. J.·Storer, C. G.·Cinel, S. D.·Godfrey, R. K.·Glass, D.·St. Laurent, R. A.·Hamilton, C. A.·Earl, C.·Brislawn, C. J.·Kitching, I. J.·Bybee, S. M.·Theobald, J. C.·Kawahara, A. Y.

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Abstract

AbstractAnimals shift activity periods to reduce predation, minimize competition, or exploit new resources, and this can drive sensory system evolution. But adaptive mechanisms underlying niche- shifts are poorly understood, and model organisms are often too distantly related to reveal the genetic drivers. To address this, we examined expression patterns between two closely related silk moths that have undergone temporal niche divergence. We found 200-700 differentially expressed genes, including day upregulation in eye development and visual processing genes, and night upregulation of antennal and olfactory brain development genes. Further, clusters of circadian, sensory, and brain development genes co-expressed with diel-activity. In both species, eight genes showed expression significantly correlated to diel activity, and are involved in vision, olfaction, brain development, neural plasticity, energy utilization, and cellular maintenance. We repeatedly recovered disco, a zinc- finger transcription factor involved in antennal development, circadian activity, and optic lobe brain development in flies. While disco mutants have circadian arrhythmia, most studies attribute this to improper clock neuron development, not adult circadian maintenance. Comparing predicted 3D protein structure across moth and fly genetic models revealed disco likely retained developmental function with a conserved zinc finger domain, but gained functional zinc finger domains absent in D. melanogaster. These regions have several mutations between nocturnal and diurnal species that co- occur with higher levels of predicted phosphorylation sites. With robust circadian expression, functional nocturnal and diurnal mutations, and structural and sequence conservation, we hypothesize that disco may be a master regulator contributing to diel-activity diversification in adult moths. SignificanceInsect diel-activity patterns are diverse, yet the underlying evolutionary processes are poorly understood. Light environment powerfully entrains circadian rhythms and drives diel-niche and sensory evolution. To investigate its impact, we compared gene expression in closely related day- and night-active wild silk moths, with otherwise similar ecologies. Expression patterns that varied with diel activity included genes linked to eye development, neural plasticity and cellular maintenance. Notably, disco, which encodes a zinc-finger transcription factor involved in pupal Drosophila optic lobe and antennal development, shows robust adult circadian mRNA cycling in moth heads, is highly conserved in moths, and has additional zinc-finger domains with specific nocturnal and diurnal mutations. We hypothesize that disco may contribute to diversification of adult diel-activity patterns in moths.

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Sondhi, Y., Messcher, R. L., Bellantuano, A. J., Storer, C. G., Cinel, S. D., Godfrey, R. K., Glass, D., St. Laurent, R. A., Hamilton, C. A., Earl, C., Brislawn, C. J., Kitching, I. J., Bybee, S. M., Theobald, J. C., Kawahara, A. Y.. 2023-05-28. The developmental gene disco regulates diel-niche evolution in adult moths. https://doi.org/10.1101/2023.05.28.542320

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