Nathan G. Walworth, Emily J. Zakem,  John P. Dunne,  Sinéad Collins, and Naomi M. Levine

PNAS March 17, 2020 117 (11) 5943-5948

Significance

Robust predictions of future changes in global biogeochemical cycling require an understanding of how microorganisms adapt to stressful and changing environments. In the ocean, rates of adaptation will be a function of both evolutionary timescales and physical dynamics. However, little is known about this interaction. We examined evolutionary dynamics of marine microbes by combining a model of microbial adaptation with varying selection pressures with a high-resolution ocean circulation model. A trade-off emerged between two evolutionary strategies: (i) ability to adapt plastically to short-term environmental fluctuations with delayed genetic adaptation and (ii) more rapid genetic adaptation with limited response to short-term environmental fluctuations. This trade-off determines evolutionary timescales and provides a foundation for understanding distributions of microbial traits and biogeochemistry.

Abstract

Marine microbes form the base of ocean food webs and drive ocean biogeochemical cycling. Yet little is known about the ability of microbial populations to adapt as they are advected through changing conditions. Here, we investigated the interplay between physical and biological timescales using a model of adaptation and an eddy-resolving ocean circulation climate model. Two criteria were identified that relate the timing and nature of adaptation to the ratio of physical to biological timescales. Genetic adaptation was impeded in highly variable regimes by nongenetic modifications but was promoted in more stable environments. An evolutionary trade-off emerged where greater short-term nongenetic transgenerational effects (low-γ strategy) enabled rapid responses to environmental fluctuations but delayed genetic adaptation, while fewer short-term transgenerational effects (high-γ strategy) allowed faster genetic adaptation but inhibited short-term responses. Our results demonstrate that the selective pressures for organisms within a single water mass vary based on differences in generation timescales resulting in different evolutionary strategies being favored. Organisms that experience more variable environments should favor a low-γ strategy. Furthermore, faster cell division rates should be a key factor in genetic adaptation in a changing ocean. Understanding and quantifying the relationship between evolutionary and physical timescales is critical for robust predictions of future microbial dynamics.

See https://www.pnas.org/content/117/11/5943

Fig. 1:

Illustrative example of model dynamics for a high-γ (A) and low-γ (B) simulation. Fitness changes (black line) are primarily driven by HT modifications (purple line) in the high-γ simulation and by both HT and LT (blue line) modifications in the low-γ simulation. The time-to-sweep (τ_sweep) is longer for the low-γ simulation (B) than the high-γ simulation (A). White shading denotes the “new” environment while gray shading denotes the “ancestral” environment.