“Keystone individuals alter ecological and evolutionary consumer-resource dynamics”

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Denon Start (Feb 2018)

The DOI is http://dx.doi.org/10.1086/695322

A single individual with extreme traits changes populations, communities, and evolution

Second (left) and first (right) year galls (Eurosta solidaginis) on goldenrod. Notice that galls differ in height over very small spatial scales.
(Credit: Tobias David Mankis)

Variation among organisms’ characteristics (traits), whether among species, populations, or individuals, forms a central pillar of both ecology and evolution. Recently, work in community ecology has suggested that differences among individuals and populations can have enormous consequences for where species are found, their abundances, and how they interact with other species in the community. However, these studies have invariably considered differences in traits among populations (mean difference) or variation within a population (variance difference). As a result, we lack an ecological or evolutionary answer to the idiom ‘can one person really make a difference?’. Put otherwise, can the addition or removal of one specific individual from a population have large and irreplaceable effects on the ecology and evolution of the system?

Here, Denon Start (University of Toronto, ON, Canada) extends the keystone individual concept from behavioral ecology to encompass ecology and evolutionary biology. Applied to ecology and evolution, he defines the keystone individual concept as the idea that certain individuals, usually with extreme (unusual) trait values, have important consequences, and that replacing an extreme individual with a ‘normal’ individual would fundamentally change the ecological or evolutionary dynamics of the system.

He then explores this concept at the Koffler Scientific Reserve in southern Ontario, using a gall-maker and its natural enemies. He shows that the presence of a single individual with an extreme predator-attracting phenotype increases mortality, changes the composition of predator communities, and increases selection for anti-predator traits in the surrounding gall-maker population. In short, the presence of a single individual with an extreme phenotype fundamentally changes the way the rest of the population interacts with other species, and the consequences of those interactions for selection. Given the massive variation among individuals, and the importance of individuals for communities, keystone individuals are likely to be common in systems as diverse as insect herbivores and human infectious diseases.


Abstract

Intraspecific variation is central to our understanding of evolution and ecology, but these fields generally consider either the mean trait value or its variance. Alternatively, the keystone individual concept from behavioral ecology posits that a single individual with an extreme phenotype can have disproportionate and irreplaceable effects on group dynamics. Here, I generalize this concept to include non-behavioral traits and broader ecological and evolutionary dynamics. I test for the effects of individuals with extreme phenotypes on the ecology and evolution of a gall-forming fly and its natural enemies that select for opposite gall sizes. Specifically I introduce a putatively keystone predator-attracting individual gall-maker, hypothesizing that the presence of such an individual should (i) increase gall-maker population-level mortality, (ii) cause consumer communities to be dominated by species that are most attracted to the keystone individual, (iii) increase selection for traits conferring defense against the most common consumer, and (iv) weaken patterns of stabilizing selection. I find support for both the ecological and evolutionary consequences of single individuals with extreme phenotypes, suggesting that they can be considered keystone individuals. I discuss the generality of the keystone individual concept, suggesting likely consequences for ecology and evolution.

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