Population variation in early development can determine ecological resilience in response to environmental change

Abstract

As climate change transforms seasonal patterns of temperature and precipitation, germination success at marginal temperatures will become critical for the long-term persistence of many plant species and communities. If populations vary in their environmental sensitivity to marginal temperatures across a species' geographical range, populations that respond better to future environmental extremes are likely to be critical for maintaining ecological resilience of the species. Using seeds from two to six populations for each of nine species of Mediterranean plants, we characterized patterns of among-population variation in environmental sensitivity by quantifying genotype-by-environment interactions (G × E) for germination success at temperature extremes, and under two light regimes representing conditions below and above the soil surface. For eight of nine species tested at hot and cold marginal temperatures, we observed substantial among-population variation in environmental sensitivity for germination success, and this often depended on the light treatment. Importantly, different populations often performed best at different environmental extremes. Our results demonstrate that ongoing changes in temperature regime will affect the phenology, fitness, and demography of different populations within the same species differently. We show that quantifying patterns of G × E for multiple populations, and understanding how such patterns arise, can test mechanisms that promote ecological resilience.

Keywords: Mediterranean ecosystems; climate change; ecological resilience; environmental sensitivity; genotype-by-environment interactions; germination success; intraspecific variation; seed ecology.

Figure 1

Photographs of the nine study species and the populations sampled across northern Sicily. Numbers match population numbers in Table 1. Inset shows the location in continental Europe. Modified from base map © Sémhur/Wikimedia Commons/CC‐BY‐SA‐3.0.

Figure 2

Germination probability for nine species (Centaurea aeolica, Erysimum etnense, Euphorbia characias, Euphorbia dendroides, Euphorbia rigida, Glaucium flavum, Jacobaea maritima, Matthiola fruticulosa, and Silene fruticosa) under different temperatures for continuous dark (closed circles with solid lines) and 12 h : 12 h, light : dark photoperiod (open circles with broken lines). Error bars represent 95% confidence intervals, and grey shading represents the marginal temperatures tested in subsequent analyses. Glaucium flavum showed very strict temperature‐dependent germination, meaning we focused on the central temperatures for this species.

Figure 3

Estimates of germination performance at marginal temperatures for all populations sampled (dashed lines) for (a) Jacobaea maritima and (b) Silene fruticosa. Trade‐offs in germination performance are evident when populations differ in slope, suggesting that different populations perform better at opposite temperature extremes.

Figure 4

Genotype‐by‐environment interaction (G × E) for species sampled with fewer than five populations: (a) Centaurea aeolica; (b) Erysimum etnense; (c) Euphorbia characias; (d) Euphorbia dendroides; (e) Euphorbia rigida; (f) Glaucium flavum; (g) Matthiola fruticulosa. Vertical grey lines represent the split between the marginal cold and hot temperatures. Error bars represent 95% confidence intervals. Asterisks represent the tests where populations show trade‐offs between hot and cold temperatures.

Figure 5

Associating natural environmental conditions with patterns of genotype‐by‐environment interaction (G × E) for all nine species (Centaurea aeolica, Erysimum etnense, Euphorbia characias, Euphorbia dendroides, Euphorbia rigida, Glaucium flavum, Jacobaea maritima, Matthiola fruticulosa, and Silene fruticosa). Overall, species showed tendencies for positive trends, suggesting sites from warmer areas performed relatively better at warmer temperature extremes but relatively worse at lower temperature extremes.