Floral Reflectance, Color, and Thermoregulation: What Really Explains Geographic Variation in Thermal Acclimation Ability of Ectotherms?

Abstract

Adaptive phenotypic plasticity in thermally sensitive traits, that is, thermal acclimation, generally increases with increasing latitude and altitude. The presumed explanation is that high-latitude/altitude organisms have evolved greater acclimation ability because of exposure to greater temperature fluctuations. Using a conceptual model of the thermal environment during the reproductive season, we tested this hypothesis against an alternative that plasticity is greater because of increased exposure to specific temperatures that strongly select for thermal acclimation. We examined geographic variation in floral reflectance/color plasticity among 29 European populations of a widespread perennial herb, Plantago lanceolata. Individuals partially thermoregulate reproduction through temperature-sensitive plasticity in floral reflectance/color. Plasticity was positively correlated with latitude and altitude. Path analyses support the hypothesis that the thermal environment mediates these geographic effects. Plasticity declined as seasonal temperature range increased, and it increased as duration of the growing season shortened and as the proportion of time exposed to temperatures favoring thermoregulation increased. Data provide evidence that floral reflectance/color plasticity is adaptive and that it has evolved in response not to the magnitude of temperature variation during the reproductive season but rather to the relative exposure to low temperatures, which favor thermoregulation.

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).…”

“…(Bradshaw, 1965;Case, Lacey, & Hopkins, 1996;Lacey & Herr, 2005Primack & Antonovics, 1981;Schmitt, Niles, & Wulff, 1992;van Tienderen & van der Toorn, 1991a, 1991bVan Hinsberg & Van Tienderen, 1997;Van Tienderen, 1990, 1992Wolff, 1987;Wolff & Van Delden, 1987). However, the degree of plasticity varies from highly plastic (e.g., a difference in percentage of light reflected at 850 nm of ~40% between spikes developed at warm vs. cool temperature) to nonplastic (Lacey & Herr, 2005;Lacey et al, 2010). In response to the natural change in ambient temperature during a reproductive season, plastic individuals produce new flowers of different colour/reflectance, based on the ambient temperature at the time of flower production (Lacey & Herr, 2005;Stiles, Cech, Dee, & Lacey, 2007).…”

“…Most P. lanceolata individuals exhibit temperature-sensitivity in floral colour and, more broadly, reflectance. Nonplastic individuals that constitutively produce dark/ poorly reflective flowers have rarely been found (Lacey et al, 2010). However, the degree of plasticity varies from highly plastic (e.g., a difference in percentage of light reflected at 850 nm of ~40% between spikes developed at warm vs. cool temperature) to nonplastic (Lacey & Herr, 2005;Lacey et al, 2010).…”

“…Because phenotypic differences in plasticity involve differential responses to cool temperature (Lacey et al, 2010), we predicted that the plasticity QTLs would colocalize only with the cool-environment QTLs. Then we mapped QTLs associated with floral reflectance and flowering time under warm and cool conditions in order to characterize the genetic architecture underlying the evolutionary divergence of P. lanceolata populations in these traits and in their plasticities.…”