Significance of differential allelic expression in phenotypic plasticity and evolutionary potential of microbial eukaryotes

Abstract

Background: Differential allelic expression (DAE) plays a key role in the regulation of many biological processes, and it may also play a role in adaptive evolution. Recently, environment-dependent DAE has been observed in species of marine phytoplankton, and most remarkably, alleles that showed the highest level of DAE also showed the fastest rate of evolution.

Methods: To better understand the role of DAE in adaptive evolution and phenotypic plasticity, we developed a 2-D cellular automata model “DAEsy-World” that builds on the classical Daisyworld model.

Results: Simulations show that DAE delineates the evolution of alternative alleles of a gene, enabling the two alleles to adapt to different environmental conditions and sub-functionalize. With DAE, the build-up of genetic polymorphisms within genes is driven by positive selection rather than strict neutral evolution, and this can enhance phenotypic plasticity. Moreover, in sexually reproducing organisms, DAE also increased the standing genetic variation, augmenting a species’ adaptive evolutionary potential and ability to respond to fluctuating and/or changing conditions (cf. genetic assimilation). We furthermore show that DAE is likely to evolve in fluctuating environmental conditions.

Conclusions: DAE increases the adaptive evolutionary potential of both sexual and asexually reproducing organisms, and it may affect the pattern of nucleotide substitutions of genes.

Author summary

In diploid organisms, the differential expression of the two alleles of a gene gives individuals more opportunities to adapt to fluctuating environmental conditions, which is particularly beneficial for clonally reproducing species.

Graphical abstract

Keywords

differential allelic expression / daisyworld model / adaptive evolution / phenotypic plasticity

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CODE AVAILABILITY

Simulations of our DAEsy-World model can be run under the following link (https://github.com/ThatPerson/Gaia).

SUPPLEMENTARY MATERIALS

The supplementary materials can be found online with this article at https://doi.org/10.15302/J-QB-021-0258.

AUTHOR CONTRIBUTIONS

BPT implemented the model and carried out the simulation and data analysis; TM participated in study design and data analysis; TW participated in study design and model implementation, and helped draft the manuscript; and CvO conceived, designed and coordinated the study and drafted the manuscript. All authors gave final approval for the publication.

ACKNOWLEDGEMENTS

We would like to thank the NERC for the Research Experience Placement (REP) scheme awarded to the EnvEast doctoral training programme (EnvEast DTP) of the University of East Anglia (UEA). Funding was provided by the NERC for the Research Experience Placement (REP) scheme awarded to the EnvEast doctoral training programme (EnvEast DTP) of the University of East Anglia (UEA). CvO was sponsored by the Earth & Life Systems Alliance (ELSA).

COMPLIANCE WITH ETHICS GUIDELINES

The authors Ben P. Tatman, Thomas Mock, Taoyang Wu and Cock van Oosterhout declare that they have no conflict of interests.ƒAll procedures performed in studies were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

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