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Abstract The phenotype of an organism is shaped by gene expression within developing tissues. This shaping relates the evolution of gene expression to phenotypic evolution, through divergence in gene expression and consequent phenotype. Rates of phenotypic evolution receive extensive attention. However, the degree to which divergence in the phenotype of gene expression is subject to heterogeneous rates of evolution across developmental stages has not previously been assessed. Here, we analyzed the evolution of the expression of single-copy orthologs within 9 species of Sordariomycetes Fungi, across 9 developmental stages within asexual spore germination and sexual reproduction. Rates of gene expression evolution exhibited high variation both within and among developmental stages. Furthermore, rates of gene expression evolution were correlated with nonsynonymous to synonymous substitution rates (dN/dS), suggesting that gene sequence evolution and expression evolution are indirectly or directly driven by common evolutionary forces. Functional pathway analyses demonstrate that rates of gene expression evolution are higher in labile pathways such as carbon metabolism, and lower in conserved pathways such as those involved in cell cycle and molecular signaling. Lastly, the expression of genes in the meiosis pathway evolved at a slower rate only across the stages where meiosis took place, suggesting that stage-specific low rates of expression evolution implicate high relevance of the genes to developmental operations occurring between those stages.
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Disentangling the developmental origins of a novel phenotype: enhancement versus reversal of environmentally induced gene expression
Increasing evidence suggests that many novel traits might have originated via plasticity-led evolution (PLE). Yet, little is known of the developmental processes that underpin PLE, especially in its early stages. One such process is ‘phenotypic accommodation’, which occurs when, in response to a change in the environment, an organism experiences adjustments across variable parts of its phenotype that improve its fitness. Here, we asked if environmentally induced changes in gene expression are enhanced or reversed during phenotypic accommodation of a novel, complex phenotype in spadefoot toad tadpoles ( Spea multiplicata ). More genes than expected were affected by both the environment and phenotypic accommodation in the liver and brain. However, although phenotypic accommodation primarily reversed environmentally induced changes in gene expression in liver tissue, it enhanced these changes in brain tissue. Thus, depending on the tissue, phenotypic accommodation may either minimize functional disruption via reversal of gene expression patterns or promote novelty via enhancement of existing expression patterns. Our study thereby provides insights into the developmental origins of a novel phenotype and the incipient stages of PLE.
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- Award ID(s):
- 1753865
- PAR ID:
- 10423675
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 289
- Issue:
- 1985
- ISSN:
- 0962-8452
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rspb.2022.1764
