The evolution of a pleiotropic fitness tradeoff in Pseudomonas fluorescens

Abstract

The evolution of ecological specialization is expected to carry a cost, due to either antagonistic pleiotropy or mutation accumulation. In general, it has been difficult to distinguish between these two possibilities. Here, we demonstrate that the experimental evolution of niche-specialist genotypes of the bacterium Pseudomonas fluorescens that colonize the air-broth interface of spatially structured microcosms is accompanied by pleiotropic fitness costs in terms of reduced carbon catabolism. Prolonged selection in spatially structured microcosms caused the cost of specialization to decline without loss of the benefits associated with specialization. The decline in the cost of specialization can be explained by either compensatory adaptation within specialist lineages or clonal competition among specialist lineages. These results provide a possible explanation of conflicting accounts for the cost of specialization.

Fig. 1.

Biolog profile of WS genotypes. The substrates shown here either always support the growth of the ancestral SM genotype (ancestral substrates) or never support the growth of this genotype (novel substrates). Blank boxes, substrates that support substantial growth of WS genotypes; gray boxes, substrates that support weak growth of WS genotypes; black boxes, substrates that do not support visible growth of WS genotypes.

Fig. 2.

The evolution of the WS metabolic profile. (A) Phenotypic clustering of WS genotypes and ancestral SM. Each tip corresponds to a single genotype. WS genotypes from continued selection lines are in bold. Numbers in brackets denote the number of catabolic defects expressed by each genotype, such that the value of ancestral SM is 0 by definition. Letters (A, B, and C) denote the three principle phenotypic clusters. (B) Mean (± SE) number catabolic defects of WS genotypes belonging to the three principle clusters identified in A.

Fig. 3.

Competitive fitness and catabolic performance. Plotted points show the competitive fitness of WS genotypes that evolve after 1 week of selection and catabolic defects, measured as the number of ancestral Biolog substrates that fail to support vigorous growth of WS genotypes. Dashed lines show linear regressions of fitness on catabolic performance. (A) Fitness was assayed as the ability of a WS genotype to invade a population of the ancestral broth-colonizing genotype from an initial frequency of ≈1% over a 2-day competition period. (B) Fitness was assayed as the competitive ability of a WS genotype against a randomly chosen WS tester genotype at an initial frequency of 1:1 over a 1-day competition period.