Alternative splicing in seasonal plasticity and the potential for adaptation to environmental change

Rachel A Steward,Maaike A De Jong,Christopher W Wheat,Vicencio Oostra

doi:10.1038/s41467-022-28306-8

Rachel A Steward, Maaike A De Jong + Show 2 more

Open Access

https://doi.org/10.1038/s41467-022-28306-8

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Abstract

Seasonal plasticity is accomplished via tightly regulated developmental cascades that translate environmental cues into trait changes. Little is known about how alternative splicing and other posttranscriptional molecular mechanisms contribute to plasticity or how these mechanisms impact how plasticity evolves. Here, we use transcriptomic and genomic data from the butterfly Bicyclus anynana, a model system for seasonal plasticity, to compare the extent of differential expression and splicing and test how these axes of transcriptional plasticity differ in their potential for evolutionary change. Between seasonal morphs, we find that differential splicing affects a smaller but functionally unique set of genes compared to differential expression. Further, we find strong support for the novel hypothesis that spliced genes are more susceptible than differentially expressed genes to erosion of genetic variation due to selection on seasonal plasticity. Our results suggest that splicing plasticity is especially likely to experience genetic constraints that could affect the potential of wild populations to respond to rapidly changing environments.

Highlights

Seasonal plasticity is accomplished via tightly regulated developmental cascades that translate environmental cues into trait changes
Our results add to the mounting evidence that differential splicing affects a smaller but nonredundant subset of genes compared to differential expression
Differential splicing is introducing protein variation for genes that remains uncaptured in analyses of average whole gene expression, and represents an important route to identifying and studying genes involved in phenotypic plasticity

Summary

Introduction

Seasonal plasticity is accomplished via tightly regulated developmental cascades that translate environmental cues into trait changes. To understand the evolutionary importance of differential splicing, especially in the context of environmental change, it is important to quantify whether any such erosion of natural genetic variation occurs in genes where splicing is important for plasticity To address these gaps, we assess the role and adaptive potential of splicing in plasticity, using the African butterfly Bicyclus anynana, a model for seasonal polyphenism[41]. Its wet and dry season morphs are end points of alternative developmental pathways induced by seasonal temperature variation[42,43], and comprise distinct wing patterns, behaviours and life history strategies (e.g., pace of life, reproductive investment)[44–46] In these butterflies, we previously found that genetic variation for plasticity is depleted, both at phenotypic and whole gene expression level, suggesting a limited potential for short-term evolution of plasticity[30]. Our study clarifies the role of splicing for adaptive plasticity, tests its importance compared to gene expression, and reveals its potential to evolve in the wild

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