Symposium: “Evolution as a coexistence mechanism: Does genetic architecture matter?”

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Sebastian J. Schreiber, Swati Patel, and Casey terHorst (Mar 2018)

The DOI will be http://dx.doi.org/10.1086/695832

Synergistic pleitropy and dominance in defensive alleles promote polymorphic prey and predator coexistence

Evolution of shared interactions can promote biodiversity

A fundamental principle in ecology is the competitive exclusion principle. Like two gladiatorial combatants in the Colosseum, this principle asserts that when two species compete for a single resource, one species will be driven extinct (the loser) and one will persist (the winner). Competition for resources, whether that be pathogens competing for hosts, herbivores competing for plants, or predators competing for prey, is ubiquitous in nature. Yet many of these competing species coexist. How can this be? Using mathematical models, Sebastian Schreiber, a Professor of Evolution and Ecology at the University of California, Davis, and his co-authors show that evolution of defenses by the exploited species provides one possible answer. This new coexistence mechanism requires that genotypes defended against one of the competitors are poorly defended against the other competitor. This trade-off can lead to a complicated rock-paper-scissor dynamic, in which no resource genotype or competitor ever has the upper hand against everybody else. Namely, when one competitor is more abundant in the system, the genotype best defended against this competitor becomes abundant. Unable to exploit this well defended genotype, this competitor species decreases in abundance as the other competitor becomes more common. Thus, the cycle continues as the genotype best defended against this other competitor becomes more abundant. Whether this mechanism is effective for enabling coexistence, however, depends on the details of the genetics underlying the defensive trait. In light of recent empirical evidence that evolution can occur quickly, the work of Schreiber and colleagues raises the tantalizing possibility that species may coexist due to the evolution of others rather than evolution of their own traits.


Abstract

Species sharing a prey or a predator species may go extinct due to exploitative or apparent competition. We examine whether evolution of the shared species acts as a coexistence mechanism and to what extent the answer depends on the genetic architecture underlying trait evolution. In our models of exploitative and apparent competition, the shared species evolves its defense or prey use. Evolving species are either haploid or diploid. A single locus pleiotropically determines prey nutritional quality and predator attack rates. When pleiotropy is sufficiently antagonistic (e.g. nutritional prey are harder to capture), eco-evolutionary assembly culminates in one of two stable states supporting only two species. When pleiotropy is weakly antagonistic or synergistic, assembly is intransitive: species-genotype pairs are cyclically displaced by rare invasions of the missing genotypes or species. This intransitivity allows for coexistence if, along its equilibria, the geometric mean of recovery rates exceeds the geometric mean of loss rates of the rare genotypes or species. By affecting these rates, synergistic pleiotropy can mediate coexistence, while antagonistic pleiotropy does not. For diploid populations experiencing weak antagonistic pleiotropy, superadditive allelic contributions to fitness can mitigate coexistence via an eco-evolutionary storage effect. Density-dependence and mutations also promote coexistence. These results highlight how the efficacy of evolution as a coexistence mechanism may depend on the underlying genetic architecture.