Differences in spatial versus temporal reaction norms for spring and autumn phenological events

Abstract

For species to stay temporally tuned to their environment, they use cues such as the accumulation of degree-days. The relationships between the timing of a phenological event in a population and its environmental cue can be described by a population-level reaction norm. Variation in reaction norms along environmental gradients may either intensify the environmental effects on timing (cogradient variation) or attenuate the effects (countergradient variation). To resolve spatial and seasonal variation in species' response, we use a unique dataset of 91 taxa and 178 phenological events observed across a network of 472 monitoring sites, spread across the nations of the former Soviet Union. We show that compared to local rates of advancement of phenological events with the advancement of temperature-related cues (i.e., variation within site over years), spatial variation in reaction norms tend to accentuate responses in spring (cogradient variation) and attenuate them in autumn (countergradient variation). As a result, among-population variation in the timing of events is greater in spring and less in autumn than if all populations followed the same reaction norm regardless of location. Despite such signs of local adaptation, overall phenotypic plasticity was not sufficient for phenological events to keep exact pace with their cues-the earlier the year, the more did the timing of the phenological event lag behind the timing of the cue. Overall, these patterns suggest that differences in the spatial versus temporal reaction norms will affect species' response to climate change in opposite ways in spring and autumn.

Keywords: chilling; climate change; heating; phenology; plasticity.

Fig. 1.

Schematic illustration showing slopes of phenology on temperature. Adapted with permission from ref. . A corresponds to phenological plasticity with respect to temperature and no local adaptation. B reveals phenological plasticity with respect to temperature plus cogradient local adaptation. C reveals phenological plasticity with respect to temperature plus countergradient local adaptation. For each scenario, we have included two examples of events showing this type of pattern in our data. For the exact climatic cues related to these biotic events, see SI Appendix, Table S1. In each plot, the red lines correspond to the within-population reaction norms through time (i.e., temporal slopes within locations), and the blue line corresponds to the between-population reaction norm (i.e., spatial slopes). If all populations respond alike, then the same reaction norm will apply across all locations, and individuals will respond in the same way to the cue no matter where they were, and no matter whether we examine responses within or between locations. If this was the case, then the reaction norm would be the same within (red lines) and between locations, and the blue and the red slopes would be parallel (i.e., their slopes identical). This scenario is depicted in A. What we use as our estimate of local adaptation is the difference between the two, i.e., whether the slope of reaction norms within populations differs from that across populations. If the temporal slopes are estimated at a relatively short time scale (as compared to the generation length of the focal organisms), then we can assume that within-location variation in the timing of the event reflects phenotypic responses alone, not evolutionary change over time. This component is then, per definition, due to phenotypic plasticity as such, i.e., to how individuals of a constant genetic makeup respond to annual variation in their environment. By comparison, the spatial slope (i.e., the blue line) is a sum of two parts: first, it reflects the mean of how individuals of a constant genetic makeup respond to annual variation in their environment, i.e., the temporal reaction norm defined above. These means are shown by the red dots in A–C. However, second, if populations differentiate across sites, then we will see variation in their response to long-term conditions, with an added element in the spatial slope reflecting mean plasticity plus local adaptation. Therefore, if the spatial slope differs from the temporal slope, this reveals local adaptation (see Materials and Methods for further details). Such local adaptation in phenological response may take two forms. 1) The magnitude of phenological change might vary along environmental gradients in ways that intensify the environmental effects on phenological traits, a process known as cogradient variation (Fig. 1B). In such a case, the covariance between the genetic influences on phenological traits and the environmental influences is positive. Under this scenario, variation in the environmental cue over space and time will cause larger variation in phenological timing than if all populations were to follow the same reaction norm regardless of location. 2) Genotypes might counteract environmental effects, thereby diminishing the change in mean trait expression across the environmental gradient. In such a case, the effect of variation in the environmental cue over space and time will be smaller than if all populations were to follow the same reaction norm regardless of location. This latter scenario, termed countergradient variation, occurs when genetic and environmental influences on phenotypic traits oppose one another (C).

Fig. 2.

Study sites and spatiotemporal patterns in climatic and phenological data. A shows the depth of the data and the spatial distribution of monitoring sites, with the size of the symbol proportional to the number of events scored locally. Since the selection of sites differed between events (39), in A, we have pooled sites located within 300 km from each other for illustration purposes. B shows the mean timing (day of year) of a phenological event: the onset of blooming in dandelion (Taraxacum officinale). C shows the mean timing (day of year) of a climatic event: the day of the year when the temperature sum providing the highest temporal slope for the onset of blooming in dandelion was first exceeded, computed as the mean over the years considered in B. For a worked-through example estimating reaction norms and metrics of local adaptation (Δb) for this species, see SI Appendix, Text S1.

Fig. 3.

The relationship between the mean timing of an event (day of year) and the slope of phenology on dates of achieving specific degree-day sums. Shown are spatial (A) and temporal (B) slopes (i.e., temporal slopes within populations), with C showing the difference between them, Δb, as an estimate of local adaptation (see main text and Fig. 1 for details). Phenological events are shown by filled circles, with the trophic level in question identified by color: primary producers are shown in green, primary consumers in yellow, secondary consumers in black, and saprotrophs in orange. A quadrat around the circle identifies species for which the 95% HPD does not overlap with 0. For visual comparison, a black line has been added to A–C at a slope value of 0 (indicating no relationship), and a red line has been added at a slope value of 1 (indicating a perfect relationship, i.e., a shift of 1 d in the timing of the event with a shift of 1 d in the date of achieving the degree-day sum in question). Dashed curves refer to model estimates provided in SI Appendix, Table S2. For the degree sum related to individual events, see SI Appendix.