Hidden diversity: Cryptic phenotypic heterogeneity as a key adaption to fluctuating environments

Ziel

Unpredictable environmental fluctuations are ubiquitous. They shape the evolution and biology of virtually all organisms. Yet, a causal, empirical understanding of how organisms adapt to such unpredictability remains elusive. This project proposes that cryptic phenotypic heterogeneity constitutes a fundamental evolutionary adaptation to unpredictable change. Cryptic phenotypic heterogeneity occurs when a single genotype generates a very small fraction of offspring with a phenotype distinct from the remaining offspring. The production of this small offspring fraction is genetically controlled; it lies well below the 0.1% threshold commonly applied to detect rare alleles, yet it remains far above the baseline mutation rate. I hypothesize that cryptic phenotypic heterogeneity confers a dual selective benefit: it minimizes evolutionary costs in stable environments while ensuring the presence of advantageous variants when conditions change unexpectedly. The central objective of this project is to test this adaptive benefit. I will utilize the interaction between a bacterial pathogen and antimicrobial compounds as a powerful, experimentally tractable model, for which cryptic heterogeneity in antimicrobial resistance has already been documented, providing an ideal entry point for an in-depth evolutionary analysis. This project integrates two experimental subprojects to dissect the process of adaptation to fluctuating conditions – based on evolution experiments, genomics, and functional genetics – and a third theory-driven subproject to generalize the new experimental insights through multivariate statistics and mathematical modelling. By combining experiments with theory, this project will establish a new general framework for understanding adaptation to environmental unpredictability. Beyond its fundamental impact, it will additionally illuminate how pathogens adapt to varying antimicrobial pressures, thereby informing the development of novel therapeutic strategies.

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