How do phenology, plasticity, and evolution determine the fitness consequences of climate change for montane butterflies?

Abstract

Species have responded to climate change via seasonal (phenological) shifts, morphological plasticity, and evolutionary adaptation, but how these responses contribute to changes and variation in population fitness are poorly understood. We assess the interactions and relative importance of these responses for fitness in a montane butterfly, Colias eriphyle, along an elevational gradient. Because environmental temperatures affect developmental rates of each life stage, populations along the gradients differ in phenological timing and the number of generations each year. Our focal phenotype, wing solar absorptivity of adult butterflies, exhibits local adaptation across elevation and responds plastically to developmental temperatures. We integrate climatic data for the past half-century with microclimate, developmental, biophysical, demographic, and evolutionary models for this system to predict how phenology, plasticity, and evolution contribute to phenotypic and fitness variation along the gradient. We predict that phenological advancements incompletely compensate for climate warming, and also influence morphological plasticity. Climate change is predicted to increase mean population fitness in the first seasonal generation at high elevation, but decrease mean fitness in the summer generations at low elevation. Phenological shifts reduce the interannual variation in directional selection and morphology, but do not have consistent effects on variation in mean fitness. Morphological plasticity and its evolution can substantially increase population fitness and adaptation to climate change at low elevations, but environmental unpredictability limits adaptive plastic and evolutionary responses at high elevations. Phenological shifts also decrease the relative fitness advantages of morphological plasticity and evolution. Our results illustrate how the potential contributions of phenological and morphological plasticity and of evolution to climate change adaptation can vary along environmental gradients and how environmental variability will limit adaptive responses to climate change in montane regions.

Keywords: adaptation; climate change; ectotherms; evolution; fitness consequences; phenology; plasticity.

Figure 1

Flow diagram for the modeling framework. Climate and weather at each elevation determine the microclimatic conditions experienced by larvae, pupae, and adults at each site. Microclimate determines developmental rates of larvae and pupae, which determine phenology. The focal trait, wing melanin, is initially determined by elevation differences among sites and is also influenced by microclimate due to the plastic effects of pupal temperatures (Tpupal). We model how wing melanin influences adult temperatures (Tadult) and ultimately performance in given microclimates and then use performance to estimate fitness. Fitness differences among individuals exhibiting variation in wing melanin can generate selection and cause evolutionary changes in the mean and plasticity of wing melanin in the next generation based on Kingsolver and Buckley (2017)

Figure 2

Predicted seasonal phenology and pupal temperatures across years. Climate and weather differences along the elevation gradient (top row = panels a–c: 3.0 km; middle row = d–f: 2.4 km; bottom row = g–i: 1.8 km) determine phenology and pupal temperatures (dashed lines: fixed phenology, varying phenology: solid lines). First column (panels a, d, g): the mean Julian date of appearance for larvae (orange), pupae (green), and adults (purple; gray shading: pupal duration). The short dashed line depicts the fixed phenology. Second column (panels b, e, h): The annual mean pupal temperature (Tpupal, in °C) during the first (blue), second (orange), and third (red) generations differs between the varying and fixed phenology scenarios. Third column (panels c, f, i): phenological shifts can counter increases in pupal temperatures in warm years. The x‐axis depicts the temperature anomaly each year during the average dates of pupation (i.e., if the average Julian dates for pupation are 150–155, average T for days 150–155 each year – average T for days 150–155 across all years). Thus, positive values indicate that temperatures during the fixed phenology are warmer than average. The y‐axis depicts the shift in pupal temperatures resulting from the varying phenology (i.e., Tpupal for varying phenology – Tpupal for fixed phenology). A gray line corresponds to phenology perfectly tracking pupal temperatures (slope = −1). We depict significant (p < .05) temporal trends

Figure 3

Predicted directional selection, mean absorptivity, and mean fitness across years. For the case with observed plasticity and no evolution, we depict the directional selection gradient (β) on absorptivity (wing melanin, panels a, d, g), mean absorptivity (panels b, e, h), and mean fitness (panels c, f, i) across elevations (top row = panels a–c: 3.0 km; middle row = d–f: 2.4 km; bottom row = g–i: 1.8 km). We depict each elevation under both variable (blue: first, orange: second, red: third) and fixed phenology (light blue: first, gold: second, pink: third). We depict significant (p < .05) temporal trends

Figure 4

Optimal reaction norms. Optimal reaction norms (optimal absorptivity as a function of mean pupal temperature in each generation) across years for the fixed (panels a, c, e) and variable (panels b, d, f) phenology for each elevation (top row = panels a–b: 3.0 km; middle row = c–d: 2.4 km; bottom row = e–f: 1.8 km). The observed reaction norm (dashed black line) is also included

Figure 5

Geometric mean population fitness as a function of year. The population fitness under fixed phenology for each site (top row = panels a–c: 3.0 km; middle row = d–f: 2.4 km; bottom row = g–i: 1.8 km) varies among scenarios (see methods and legend, left column). We additionally depict geometric mean fitness relative to the case of constant absorptivity for the cases of fixed phenology (panels b, e, h) and varying phenology (panels c, f, i)