Natural selection contributes to geographic patterns of thermal plasticity in Plantago lanceolata

Abstract

A long‐standing debate in evolutionary biology concerns the relative importance of different evolutionary forces in explaining phenotypic diversification at large geographic scales. For example, natural selection is typically assumed to underlie divergence along environmental gradients. However, neutral evolutionary processes can produce similar patterns. We collected molecular genetic data from 14 European populations of Plantago lanceolata to test the contributions of natural selection versus neutral evolution to population divergence in temperature‐sensitive phenotypic plasticity of floral reflectance. In P . lanceolata, reflectance plasticity is positively correlated with latitude/altitude. We used population pairwise comparisons between neutral genetic differentiation ( F ST and Jost's D ) and phenotypic differentiation ( P ST ) to assess the contributions of geographic distance and environmental parameters of the reproductive season in driving population divergence. Data are consistent with selection having shaped large‐scale geographic patterns in thermal plasticity. The aggregate pattern of P ST versus F ST was consistent with divergent selection. F ST explained thermal plasticity differences only when geographic distance was not included in the model. Differences in the extent of cool reproductive season temperatures, and not overall temperature variation, explained plasticity differences independent of distance. Results are consistent with the hypothesis that thermal plasticity is adaptive where growing seasons are shorter and cooler, that is, at high latitude/altitude.

Two reproductive traits show contrasting genetic architectures in Plantago lanceolata

“…As ambient temperature changes throughout the lengthy flowering season, a thermally plastic individual modifies the colour/reflectance of its newly developed flowers. Results of multiple experiments are consistent with the hypothesis that this thermal plasticity is locally adaptive (Lacey, Lovin, & Richter, 2012;Lacey et al, 2010;Marshall, Batten, Remington, & Lacey, 2019). Plastic individuals produce darker, less reflective flowers in cool temperatures and lighter, more reflective flowers in warm temperatures-e.g., typically, dark flowers in spring and autumn and light flowers in F I G U R E 1 Reaction norms for Plantago lanceolata genotypes from Veno, Denmark, (black) and Hameau de St. Felix, France (red), grown under cool (15°C day/10°C night) and warm (27°C day/20°C night) temperature.…”

“…Plastic individuals produce darker, less reflective flowers in cool temperatures and lighter, more reflective flowers in warm temperatures-e.g., typically, dark flowers in spring and autumn and light flowers in F I G U R E 1 Reaction norms for Plantago lanceolata genotypes from Veno, Denmark, (black) and Hameau de St. Felix, France (red), grown under cool (15°C day/10°C night) and warm (27°C day/20°C night) temperature. Temperature-sensitive plasticity is positively correlated with latitude and altitude in the species' native European range ( Figure 1 and Lacey et al, 2010), and this geographical pattern is better explained by local adaptation than by neutral evolutionary factors (Marshall et al, 2019). Results of multiple experiments are consistent with the hypothesis that this thermal plasticity is locally adaptive (Lacey, Lovin, & Richter, 2012;Lacey et al, 2010;Marshall, Batten, Remington, & Lacey, 2019).…”

“…Many species, particularly ectotherms (i.e., most species on Earth), exhibit thermal plasticity (tempera-summer (Lacey & Herr, 2005). Results of multiple experiments are consistent with the hypothesis that this thermal plasticity is locally adaptive (Lacey, Lovin, & Richter, 2012;Lacey et al, 2010;Marshall, Batten, Remington, & Lacey, 2019). However, not all individuals are thermally plastic.…”

“…Darker, less reflective flowers absorb more incoming solar radiation than lighter, more reflective flowers, thereby helping to warm reproductive tissues, which can improve seed production and offspring fitness (Lacey, 1996;Lacey & Herr, 2000, 2005. Additionally, population pairwise comparisons of neutral genetic differentiation, phenotypic differentiation and environmental differences, along with gene flow data, together indicate that natural selection best explains the evolutionary divergence in plasticity along latitudinal and altitudinal gradients (Marshall et al, 2019).…”

“…Nonplastic individuals produce lightly coloured/ highly reflective flowers, regardless of ambient temperature (Lacey & Herr, 2005). Temperature-sensitive plasticity is positively correlated with latitude and altitude in the species' native European range (Figure 1 and Lacey et al, 2010), and this geographical pattern is better explained by local adaptation than by neutral evolutionary factors (Marshall et al, 2019).…”