The capacity for phenotypic evolution is dependent upon complex webs of functional interactions that connect genotype and phenotype. Wrinkly spreader (WS) genotypes arise repeatedly during the course of a model Pseudomonas adaptive radiation. Previous work showed that the evolution of WS variation was explained in part by spontaneous mutations in wspF, a component of the Wsp-signaling module, but also drew attention to the existence of unknown mutational causes. Here, we identify two new mutational pathways (Aws and Mws) that allow realization of the WS phenotype: in common with the Wsp module these pathways contain a di-guanylate cyclase-encoding gene subject to negative regulation. Together, mutations in the Wsp, Aws, and Mws regulatory modules account for the spectrum of WS phenotypegenerating mutations found among a collection of 26 spontaneously arising WS genotypes obtained from independent adaptive radiations. Despite a large number of potential mutational pathways, the repeated discovery of mutations in a small number of loci (parallel evolution) prompted the construction of an ancestral genotype devoid of known (Wsp, Aws, and Mws) regulatory modules to see whether the types derived from this genotype could converge upon the WS phenotype via a novel route. Such types-with equivalent fitness effects-did emerge, although they took significantly longer to do so. Together our data provide an explanation for why WS evolution follows a limited number of mutational pathways and show how genetic architecture can bias the molecular variation presented to selection.
Diversity in biological communities is a historical product of immigration, diversification and extinction, but the combined effect of these processes is poorly understood. Here we show that the order and timing of immigration controls the extent of diversification. When an ancestral bacterial genotype was introduced into a spatially structured habitat, it rapidly diversified into multiple niche-specialist types. However, diversification was suppressed when a niche-specialist type was introduced before, or shortly after, introduction of the ancestral genotype. In contrast, little suppression occurred when the same niche specialist was introduced relatively late. The negative impact of early arriving immigrants was attributable to the historically sensitive outcome of interactions involving neutral competition and indirect facilitation. Ultimately, the entire boom-and-bust dynamics of adaptive radiation were altered. These results demonstrate that immigration and diversification are tightly linked processes, with small differences in immigration history greatly affecting the evolutionary emergence of diversity.
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