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.