Adaptive phenotypic evolution of Skeletonema costatum to ocean acidification and warming with trade-offs from a multi-year outdoor experiment.

Human-induced climate change is increasing variability in marine environments, significantly affecting marine organisms and ecosystems. While marine diatoms can adapt to ocean acidification and warming in stable laboratory settings, their responses to long-term environmental changes under natural variability remain unclear. To investigate this, we cultivated Skeletonema costatum in outdoor semi-continuous cultures for over 3 years, exposing them to fluctuating natural light and temperature that tracked the in situ sea surface temperatures. We simulated current and future ocean conditions through four treatments: ambient CO2 and temperature (LTLC), elevated CO2 (LTHC), elevated temperature (+4°C, HTLC) and combined increases (HTHC). After 1396 days, we assessed populations in two assay environments (20°C, 400 ppm CO2 and 24°C, 1000 ppm CO2) for adaptations in growth rate, pigment composition and photosynthesis. The HTLC-selected group showed the highest growth rates in the HTHC assay environment, while the LTLC-selected group grew fastest in the LTLC assay environment, indicating adaptive evolution. Furthermore, populations selected under elevated conditions exhibited lower fitness in LTLC environments, highlighting a trade-off and underscoring the complexity of evolutionary adaptation in marine diatoms. Understanding these mechanisms is crucial for predicting phytoplankton dynamics and their role in marine ecosystems, especially in response to climate change.