Hitting a moving target: Microbial evolutionary strategies in a warming ocean

Naomi Marcil Levine, University of Southern California, Los Angeles, United States, Nathan gerard Walworth, Vesta, PBC, Los Angeles, United States, Emily Zakem, University of Southern California, Los Angeles, CA, United States, John P Dunne, NOAA Geophys Fluid Dynamic, Princeton, United States and Sinead Collins, University of Edinburgh, Edinburgh, United Kingdom
Marine microbes form the base of ocean food webs and drive ocean biogeochemical cycling. Yet little is known about how microbial populations will evolve due to global change-driven shifts in ocean dynamics. Understanding adaptive timescales is critical where long-term trends (e.g. warming) are coupled to shorter-term advection dynamics that move organisms rapidly between ecoregions. 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 (alpha and beta) were identified that relate physical and biological timescales and determine the timing and nature of adaptation. Genetic adaptation was impeded in highly variable regimes (alpha<1) but promoted in more stable environments (alpha>1). An evolutionary trade-off emerged where greater short-term transgenerational effects (low-beta-strategy) enabled rapid responses to environmental fluctuations but delayed genetic adaptation, while fewer short-term transgenerational effects (high-beta-strategy) allowed faster genetic adaptation but inhibited short-term responses. Our results suggest that organisms with faster growth rates are better positioned to adapt to rapidly changing ocean conditions and that more variable environments will favor a bet-hedging, low-beta-strategy. Understanding the relationship between evolutionary and physical timescales is critical for robust predictions of future microbial dynamics.