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

Abstract

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

“…In our study, observed temperature‐dependent selection on flowering time might also have been mediated by interactions with pollinators and herbivores. Although we did not investigate the role of pollinators in this study, a study with Pinguicula vulgaris in the same area showed that fitness decreased with increasing soil temperature in untreated plants but increased with temperature in plants supplemented with pollen (Valdés et al, 2022). This suggests that early‐flowering plants in warm soils might receive fewer pollinator visits, for example, because pollinators experience a different degree of warming, or because the sensitivity to temperature differs between plants and pollinators (Kharouba & Vellend, 2015).…”

What determines the evolutionary trajectories of wild plant species? Approaches to the study of quantitative fitness‐related traits

“…It also permits the detection and measurement of the three distinct modes of selection on individual traits: linear, stabilizing (or optimizing), and disruptive selection. In this issue, many of the investigators used selection analysis to examine or to infer the process of selection on traits such as germination time (Muir et al, 2022), flowering phenology (Johnson et al, 2022, MacTavish and Anderson, 2022, Valdés et al, 2022), flower size and height (Chen and Pannell, 2022), plant size at flowering (MacTavish and Anderson, 2022), specific leaf area and plant height (Waterton et al, 2022), and physiological performance (Mazer et al, 2022; see also Johnson et al, 2022).…”

“…Valdés et al (2022) investigated whether mean flowering time, mean fitness, and the pattern of selection on flowering time in the carnivorous common butterwort, Pinguicula vulgaris (Lentibulariaceae), are influenced by geothermally heated local soil temperature, experimentally manipulated pollination intensity, and prey availability. In addition, they assessed whether the plastic response of flowering time to environmental conditions was maladaptive based on the environment‐specific patterns of selection on this trait.…”

“…Their comparison of the post-selection populations corroborated the prediction that drought induced the evolution of earlier flowering and lower water-use efficiency relative to watered conditions, consistent with the interpretation that in this species, drought imposes effective selection for traits that promote escape from drought. Valdés et al (2022) investigated whether mean flowering time, mean fitness, and the pattern of selection on flowering time in the carnivorous common butterwort, Pinguicula vulgaris (Lentibulariaceae), are influenced by geothermally heated local soil temperature, experimentally manipulated pollination intensity, and prey availability. In addition, they assessed whether the plastic response of flowering time to environmental conditions was maladaptive based on the environment-specific patterns of selection on this trait.…”