The long-term evolutionary potential of four yeast species and their hybrids in extreme temperature conditions
Authors: Pinto Javier , Stelkens Rike 
Published: September 2024

AbstractAccelerating climate change and extreme temperature events urge us to better understand the potential of populations to tolerate and adapt to thermal challenges. Interspecific hybridization can facilitate adaptation to novel or extreme environments. However, predicting the long-term fitness effects of hybridization remains a major challenge in evolutionary and conservation biology. Experimental evolution with microbes provides a powerful tool for tracking adaptive processes across hundreds of generations in real time. Here, we investigated thermal adaptation dynamics of four species of budding yeast (Saccharomyces) and their interspecific F2 hybrids, for 200 generations under extremely cold (5°C) and warm (31°C) conditions. We found significant variation in the evolutionary potential of species and hybrids. Cold-tolerant species showed larger fitness increases in warm temperature, whereas warm-tolerant species showed larger fitness gains in cold temperature. By far the largest fitness improvements occurred in hybrids, with some populations nearly quadrupling in fitness in the cold environment over the course of experimental evolution. Some hybrids exceeded both their parents in thermal adaptive potential. Reciprocal transplanting of evolved populations from the endpoint of evolution into opposite temperatures revealed that hybrids generally have greater resilience than their parents when challenged with sudden temperature shifts. Our results highlight that hybridization alters the fitness outcomes of long-term adaptation to extreme environments and may render populations more resilient to sudden environmental change, presenting both opportunities and challenges for conservation and sustainable agriculture.Lay summaryUnderstanding how populations adapt to extreme temperatures is crucial in times of accelerating climate change. Hybridization and genetic exchange between species can help populations adapt to new or extreme environments, but can also have negative effects on fitness. Predicting the long-term effects of hybridization remains challenging for evolutionary biologists. We usually do not know how hybrid offspring respond to future environmental change. Experimental evolution with microbes is a powerful tool to provide insight here, because we can observe fitness changes in real-time, across many generations. We tracked the fitness of six species of budding yeastSaccharomycesand their hybrids, over 200 generations in extreme cold (5°C) and warm (31°C) conditions. We found that species and hybrids have significantly different abilities to adapt. The largest fitness improvements were observed in hybrid populations, particularly in the cold, where some nearly quadrupled in fitness and exceeded both their parents. When exposing evolved populations to a sudden shift into opposite temperatures, hybrids were more resilient than their parent species. Even after 200 generations of evolution under opposite temperature conditions, hybrids still showed a similar performance to their ancestors. Our results suggest that hybridization can enhance the ability of populations to adapt to extreme environments, offering potential benefits for conservation and agriculture.