“Indirect interactions shape selection in a multi-species foodweb”

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Denon Start, Arthur E. Weis, and Benjamin Gilbert (Mar 2019)

The DOI will be https://dx.doi.org/10.1086/701785

The tangled bank: Species interactions ripple across foodwebs to shape natural selection

Complex webs of species interactions shape patterns of natural selection

Eurosta galls on tall goldenrod. Galls differ in size and density, shaping patterns of enemy attack. Changing patterns of attack are ultimately responsible for creating differences in natural selection among populations.
(Credit: Tobias David Mankis)

Life on Earth does not live, die, or evolve in isolation. Instead, all organisms are embedded in an incredibly complex world filled with other species, whose numbers and traits are constantly shifting. All organisms have to navigate the trials and tribulations of this world, yet we are only beginning to understand how the complexity of natural ecological communities translates to the production of evolutionary patterns. How can we understand how constantly changing ecological communities will shape the form, function, and fitness of organisms, ultimately creating patterns of natural selection and evolutionary change?

Here, Denon Start, Arthur Weis, and Benjamin Gilbert (University of Toronto, ON, Canada) investigate how species interactions cascade through a foodweb, and how those cascading interactions shape natural selection. They begin by suggesting that traits and abundances determine patterns of species interactions, and that these same quantities shape evolutionary processes. Because of these common currencies (traits and abundances), we should be able to disentangle the relationships between ecological and evolutionary interactions.

Start et al. test this line of reasoning by manipulating species interactions in a natural foodweb at the Koffler Scientific Reserve (www.ksr.utoronto.ca). The foodweb is centered on a gall-forming fly, an organism that interacts with its host plant and other herbivores, and is attacked by a community of enemies. Changes to the traits and abundances of the gall-maker and the many interacting species shaped the strength of species interactions, and the resultant patterns of natural selection. Using indirect interactions grounded in units of traits and abundances is a first step in understanding how complex multi-species communities will shape patterns of natural selection, and by extension will facilitate the rapprochement of community ecology and evolutionary biology.


Abstract

Species do not live, interact, or evolve in isolation, but are instead members of complex ecological communities. In ecological terms, complex multi-species interactions can be understood by considering indirect effects that are mediated by changes in traits and abundances of intermediate species. Interestingly, traits and abundances are also central to our understanding of phenotypic selection, suggesting that indirect effects may be extended to understand evolution in complex communities. Here, we explore indirect ecological effects and their evolutionary corollary in a well-understood foodweb comprising a plant, its herbivores, and enemies that select for opposite defensive phenotypes in one of the herbivores. We show that ecological indirect interactions are mediated by changes to both the traits and abundances of intermediate species, and that these changes ultimately reduce enemy attack and weaken selection. We discuss the generality of the link between indirect effects and selection. We go on to argue that local adaptation and eco-evolutionary feedback may be less likely in complex multi-species foodwebs than in simpler food chains (e.g. coevolution). Overall, considering selection in complex interaction networks can facilitate the rapprochement of community ecology and evolution.