Nutrition-responsive gene expression and the developmental evolution of insect polyphenism

Abstract

Nutrition-responsive development is a ubiquitous and highly diversified example of phenotypic plasticity, yet its underlying molecular and developmental mechanisms and modes of evolutionary diversification remain poorly understood. We measured genome-wide transcription in three closely related species of horned beetles exhibiting strikingly diverse degrees of nutrition responsiveness in the development of male weaponry. We show that (1) counts of differentially expressed genes between low- and high-nutritional backgrounds mirror species-specific degrees of morphological nutrition responsiveness; (2) evolutionary exaggeration of morphological responsiveness is underlain by both amplification of ancestral nutrition-responsive gene expression and recruitment of formerly low nutritionally responsive genes; and (3) secondary loss of morphological responsiveness to nutrition coincides with a dramatic reduction in gene expression plasticity. Our results further implicate genetic accommodation of ancestrally high variability of gene expression plasticity in both exaggeration and loss of nutritional plasticity, yet reject a major role of taxon-restricted genes in the developmental regulation and evolution of nutritional plasticity.

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Fig. 1: Diversity of morphological plasticity among three onthophagine species.
Fig. 2: Nutrition-responsive differential gene expression as a function of nutrition across three onthophagine species.
Fig. 3: Distribution of differentially expressed genes following different patterns of response to nutrition.
Fig. 4: Comparative analyses of dsx function in the regulation of horn growth.
Fig. 5: Gene expression variation (MAD) across plasticity categories.

Data availability

All data are available through NCBI’s Short Read Archive (BioProject accession: PRJNA608082).

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Acknowledgements

We thank the Center for Genomics and Bioinformatics at Indiana University, which conducted sequencing and library construction, the Zdobnov laboratory for their guidance using OrthoDB and the National Center for Genome Analysis. We sincerely thank C. Ledón-Rettig, T. Ledón-Rettig, S. Close and W. Arnold for collecting beetles in the wild. This research was made possible through support by National Science Foundation grant nos. IOS 1256689 and 1901680 to A.P.M., as well as grant no. 61369 from the John Templeton Foundation. The opinions, interpretations, conclusions and recommendations are those of the authors and are not necessarily endorsed by the National Science Foundation or John Templeton Foundation.

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S.C., E.E.Z. and A.P.M. designed the experiments. S.C. conducted the experiments (phenotyping, tissue dissection and RNA extraction). S.C., E.E.Z. and A.P.M. analysed and interpreted the data. S.C., E.E.Z. and A.P.M. wrote the manuscript.

Corresponding authors

Correspondence to Sofia Casasa or Eduardo E. Zattara.

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Extended data

Extended Data Fig. 1 Individuals used for dissections.

Relative pupal body size- horn size allometry for the three species used in this study (D. gazella: blue; O. taurus: red; O. sagittarius: yellow). Additionally, the novel, anterior head horn size of O. sagittarius is shown in white. Small and large individuals of each species that were used for dissections are shown in triangles. Relative body size was used to control for absolute body size differences across species and was calculated as the residual from the mean over the species’ body size range.

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Supplementary Tables 1–12, results and discussion, and methods.

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Casasa, S., Zattara, E.E. & Moczek, A.P. Nutrition-responsive gene expression and the developmental evolution of insect polyphenism. Nat Ecol Evol 4, 970–978 (2020). https://doi.org/10.1038/s41559-020-1202-x

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