Academic journal article Genetics

Adaptive Divergence in Experimental Populations of Pseudomonas Fluorescens. IV. Genetic Constraints Guide Evolutionary Trajectories in a Parallel Adaptive Radiation

Academic journal article Genetics

Adaptive Divergence in Experimental Populations of Pseudomonas Fluorescens. IV. Genetic Constraints Guide Evolutionary Trajectories in a Parallel Adaptive Radiation

Article excerpt

ABSTRACT

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 phenotype-generating 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.

UNDERSTANDING-and importantly, predicting- phenotypic evolution requires knowledge of the factors that affect the translation of mutation into phenotypic variation-the raw material of adaptive evolution. While much is known about mutation rate (e.g., DRAKE et al. 1998; Hudson et al. 2002), knowledge of the processes affecting the translation of DNA sequence variation into phenotypic variation is minimal.

Advances in knowledge on at least two fronts suggest that progress in understanding the rules governing the generation of phenotypic variation is possible (STERN and ORGOGOZO 2009). The first stems from increased awareness of the genetic architecture underlying specific adaptive phenotypes and recognition of the fact that the capacity for evolutionary change is likely to be constrained by this architecture (SCHLICHTING and MURREN 2004; HANSEN 2006). The second is the growing number of reports of parallel evolution (e.g., Pigeon et al. 1997; FFRENCH-CONSTANT et al. 1998; ALLENDER et al. 2003; COLOSIMO et al. 2004; ZHONG et al. 2004; BOUGHMAN et al. 2005; SHINDO et al. 2005; KRONFORST et al. 2006; WOODS et al. 2006; ZHANG 2006; BANTINAKI et al. 2007;McGREGOR et al. 2007;OSTROWSKI et al. 2008)-that is, the independent evolution of similar or identical features in two or more lineages-which suggests the possibility that evolution may follow a limited number of pathways (SCHLUTER 1996). Indeed, giving substance to this idea are studies that show thatmutations underlying parallel phenotypic evolution are nonrandomly distributed and typically clustered in homologous genes (STERN and ORGOGOZO 2008).

While the nonrandom distribution of mutations during parallel genetic evolutionmay reflect constraints due to genetic architecture, some have argued that the primary cause is strong selection (e.g., WICHMAN et al. 1999; WOODS et al. 2006). A means of disentangling the roles of population processes (selection) from genetic architecture is necessary for progress (MAYNARD SMITH et al. 1985; BRAKEFIELD 2006); also necessary is insight into precisely how genetic architecture might bias the production of mutations presented to selection.

Despite their relative simplicity, microbial populations offer opportunities to advance knowledge. The wrinkly spreader (WS) morphotype is one of many different niche specialist genotypes that emerge when experimental populations of Pseudomonas fluorescens are propagated in spatially structured microcosms (RAINEY and TRAVISANO 1998). …

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