Discussion
Extreme events are increasingly common and can have corresponding consequences for ecological (Fey et al. 2017, Anderson et al. 2017) and evolutionary (Siepielski and Benkman 2007, Little et al. 2019) processes. However, the non-local eco-evolutionary consequences of extreme events have not been explored. I show that an extreme event has different consequences for species interactions, selection, demography, and evolution in different populations (all Figures). Consequently, the extreme event increased heterogeneity of species interaction (β-diversity; Fig. 2) and spatial variation in selection (Fig. 3), with down-stream eco-evolutionary consequences (Fig. 5). We know that extreme events can have important consequences for local ecological and evolutionary dynamics. The work presented here shows that Black Swan events can also create characteristic landscape-level patterns of eco-evolutionary heterogeneity, with potential importance for the maintenance of regional biodiversity.
The extreme wind event had key consequences for survival and species interaction. The extreme event described here is somewhat unusual—the vast majority of extreme events increase death (Anderson et al. 2017), while the extreme event here reduced antagonistic interactions and thus mortality (Fig. 1A & 2). More intriguingly, while the extreme wind event homogenized the proportion of galls being knocked over (Fig. 1A), it nevertheless increased spatial heterogeneity in survival and bird attack (Fig. 1A & 2A). This occurred because when most stems were knocked down, the distance of a population from the treeline had a larger effect on attack rates—a mean change in one environmental condition altered the effect of another environmental condition on ecological interactions (Fig. 2B). Similar counterintuitive effects of extreme events are likely to occur whenever multiple factors interact to shape ecological processes—the complexity of interaction networks and their variations may serve to amplify, dampen, or qualitatively alter the effects of extreme events (Siepielski and Benkman 2007, Ledger et al. 2013, Woodward et al. 2016, terHorst et al. 2018). Indeed, species interactions are often influenced by multiple interacting environmental factors and can serve as ‘biotic multipliers’ of an environmental change (Zarnetske et al. 2012). In short, to understand the consequences of Black Swan events, it is not enough to test for the direct effects of the environmental change on an ecological or evolutionary outcome (e.g. does a heatwave increase or decrease mortality). Instead, we require a greater understanding of how extreme events shape species interactions (Siepielski and Benkman 2007), and the consequences of those interaction changes for populations and communities.
Extreme events can have direct and indirect consequences on patterns of natural selection. In the simplest case, an extreme event can directly select for different phenotypes. For instance, selection induced by tropical cyclones favors aggressiveness in colonies of spiders (Little et al. 2019). Conversely, extreme events can alter selection by having cascading effects on a focal population via species interactions (Siepielski and Benkman 2007). In our case, the greater heterogeneity in bird attack and survival created by the extreme wind event caused correspondingly variable patterns of natural selection (Fig. 3). Interestingly, this pattern is opposite to what is traditionally expected—extreme events occurring across all populations should homogenize interactions and selection, while extreme events occurring in some but not other local communities should create heterogeneity (Pruitt et al. 2019). As a result, extreme events may impose strong and highly variable selection. While strong selection in some years can drive patterns of local adaptation (Siepielski and Benkman 2007), greater spatial variation in selection can exacerbate among-population differences and potentially contribute to the regional maintenance of genetic and phenotypic diversity. As above, we cannot understand the causes of selection in response to extreme events without considering species interactions and indirect environmental effects in multiple populations.
The effect of Black Swan events on ecological and evolutionary change are linked and complex. Extreme events should have a large impact on survival and population density in the next generation, creating a correspondingly strong pattern of selection and evolutionary change (Benkman 2013). Indeed, following the high survival associated with the extreme wind event, population density of Eurosta increased. Large differences in mean survival also drove evolutionary change—galls tended to increase or decrease in size in line with the direction of selection (Fig. 4) which itself was created by differences in survival and bird attack (Fig. 3B). On the one hand, it is unsurprising that multiple ecological quantities (survival and species interactions) affected selection and evolutionary change (Arnold and Wade 1984, Benkman 2013). On the other hand, it does suggest a need to simultaneously account for population and community dynamics when forecasting evolutionary change (terHorst et al. 2018, Start et al. 2019), including in response to extreme events.
Here I have demonstrated an eco-evolutionary response to an extreme event, but are such responses common and important? The answer to the first question is pedantic—extreme events are almost definitionally rare, so eco-evolutionary responses to such events should be correspondingly uncommon (Anderson et al. 2017). However, when rare extreme events do occur, I argue that they can have important consequences for eco-evolutionary processes. For instance, extreme events can trigger extinctions (Nunes and Logares 2012), alter community structure (Shafi and Yarranton 1973), shift population dynamics (Anderson et al. 2017), and drive patterns of adaptation (Siepielski and Benkman 2007). In some instances, this occurs because extreme values have an outsized effect on eco-evolutionary patterns. For instance, the long run fitness (and frequency) of a given genotype depends on geometric mean fitness, inflating the importance of rare but extreme events that affect fitness in some generations (Saether and Engen 2015). However, the effects of extreme events may also stem from other mechanisms, for instance by triggering permanent extirpations or tipping a system into an alternative stable state (Holmgren et al. 2006, Fabina et al. 2015). I argue that extreme events should have strong eco-evolutionary consequences, but that we need more long-term datasets to gain a better understanding of the mechanisms translating a Black Swan to an eco-evolutionary outcome.
I have demonstrated that extreme events can have counterintuitive effects on eco-evolutionary heterogeneity. There are two key-takeaways from my work. First, in order to understand the effects of Black Swan events on population demography and evolutionary change, we need to understand how the multiple interactive effects of environmental factors and species interactions shape selection; interaction networks can amplify, dampen, or qualitatively alter the eco-evolutionary consequences of extreme events. Second, because of the complex interactions among species and environmental factors shaping selection and evolutionary responses, extreme events can create spatially heterogeneous eco-evolutionary patterns, even when those extreme events homogenize abiotic conditions. While it is tempting to view Black Swan events as a harsh filter with homogenizing effects (Shafi and Yarranton 1973, Nunes and Logares 2012), the complexity of nature belies such generalization. In order to understand the consequences of Black Swan events, we need to integrate our understanding of community ecology and evolutionary biology.