Community and Ecosystem Genetics: A Consequence of the Extended Phenotype

Abstract

We present evidence that the heritable genetic variation within individual species, especially dominant and keystone species, has community and ecosystem consequences. These consequences represent extended phenotypes, i.e., the effects of genes at levels higher than the population. Using diverse examples from microbes to vertebrates, we demonstrate that the extended phenotype can be traced from the individuals possessing the trait, to the community, and to ecosystem processes such as leaf litter decomposition and N mineralization. In our development of a community genetics perspective, we focus on intraspecific genetic variation because the extended phenotypes of these genes can be passed from one generation to the next, which provides a mechanism for heritability. In support of this view, common‐garden experiments using synthetic crosses of a dominant tree show that their progeny tend to support arthropod communities that resemble those of their parents. We also argue that the combined interactions of extended phenotypes contribute to the among‐community variance in the traits of individuals within communities. The genetic factors underlying this among‐community variance in trait expression, particularly those involving genetic interactions among species, constitute community heritability. These findings have diverse implications. (1) They provide a genetic framework for understanding community structure and ecosystem processes. The effects of extended phenotypes at these higher levels need not be diffuse; they may be direct or may act in relatively few steps, which enhances our ability to detect and predict their effects. (2) From a conservation perspective, we introduce the concept of the minimum viable interacting population (MVIP), which represents the size of a population needed to maintain genetic diversity at levels required by other interacting species in the community. (3) Genotype × environment interactions in dominant and keystone species can shift extended phenotypes to have unexpected consequences at community and ecosystem levels, an issue that is especially important as it relates to global change. (4) Documenting community heritability justifies a community genetics perspective and is an essential first step in demonstrating community evolution. (5) Community genetics requires and promotes an integrative approach, from genes to ecosystems, that is necessary for the marriage of ecology and genetics. Few studies span from genes to ecosystems, but such integration is probably essential for understanding the natural world. Corresponding Editor: A. A. Agrawal

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