Selection against early flowering in geothermally heated soils is associated with pollen but not prey availability in a carnivorous plant.

PREMISE: In high-latitude environments, plastic responses of phenology to increasing spring temperatures allow plants to extend growing seasons while avoiding late frosts. However, evolved plasticity might become maladaptive if climatic conditions change and spring temperatures no longer provide reliable cues for conditions important for fitness. Maladaptative phenological responses might be related to both abiotic factors and mismatches with interacting species. When mismatches arise, we expect selection to favor changes in phenology. METHODS: We combined observations along a soil temperature gradient in a geothermally heated area with pollen and prey supplementation experiments and examined how phenotypic selection on flowering time in the carnivorous plant Pinguicula vulgaris depends on soil temperature, and pollen and prey availability. RESULTS: Flowering advanced and fitness decreased with increasing soil temperature. However, in pollen-supplemented plants, fitness instead increased with soil temperature. In heated soils, there was selection favoring later flowering, while earlier flowering was favored in unheated soils. This pattern remained also after artificially increasing pollen and prey availability. CONCLUSIONS: Plant-pollinator mismatches can be an important reason why evolved plastic responses of flowering time to increasing spring temperatures become maladaptive under novel environmental conditions, and why there is selection to delay flowering. In our study, selection for later flowering remained after artificially increasing pollen availability, suggesting that abiotic factors also contribute to the observed selection. Identifying the factors that make evolved phenological responses maladaptive under novel conditions is fundamental for understanding and predicting evolutionary responses to climate warming.

Maladaptive plastic responses of flowering time to geothermal heating.

Phenotypic plasticity might increase fitness if the conditions under which it evolved remain unaltered, but becomes maladaptive if the environment no longer provides reliable cues for subsequent conditions. In seasonal environments, timing of reproduction can respond plastically to spring temperature, maximizing the benefits of a long season while minimizing the exposure to unfavorable cold temperatures. However, if the relationship between early spring temperatures and later conditions changes, the optimal response might change. In geothermally heated ecosystems, the plastic response of flowering time to springtime soil temperature that has evolved in unheated areas is likely to be non-optimal, because soil temperatures are higher and decoupled from air temperatures in heated areas. We therefore expect natural selection to favor a lower plasticity and a delayed flowering in these areas. Using observational data along a natural geothermal warming gradient, we tested the hypothesis that selection on flowering time depends on soil temperature and favors later flowering on warmer soils in the perennial Cerastium fontanum. In both study years, plants growing in warmer soils began flowering earlier than plants growing in colder soils, suggesting that first flowering date (FFD) responds plastically to soil temperature. In one of the two study years, selection favored earlier flowering in colder soils but later flowering in warmer soils, suggesting that the current level of plastic advance of FFD on warmer soils may be maladaptive in some years. Our results illustrate the advantages of using natural experiments, such as geothermal ecosystems, to examine selection in environments that recently have undergone major changes. Such knowledge is essential to understand and predict both ecological and evolutionary responses to climate warming.