Evolutionary genomics of ecological specialization

Abstract

We used a combination of genomic techniques to monitor chromosomal evolution across hundreds of generations as Escherichia coli adapted to growth-limiting concentrations of either lactulose, methyl-galactoside, or a 72:28 mixture of the two. DNA microarrays identified 8 unique duplications and 16 unique deletions among 42 evolvants from 23 chemostat experiments. Each mutation was confirmed by sequencing PCR-amplified flanking genomic DNA and, except for one deletion, an insertion sequence was found at the break point. vPCR of insertion sequences identified these same mutations and 16 additional insertions (all confirmed by sequencing). The pattern of genomic evolution is highly reproducible. Statistical analyses show that duplications at lac and mutations in mgl are adaptations specific to lactulose and to methyl-galactoside, respectively. Adaptation to mixed sugars is characterized by similar mutations, but lac duplications and mgl mutations usually arise in different backgrounds, producing ecological specialists for each sugar. This suggests that an antagonistic pleiotropic tradeoff between duplications at lac and mutations in mgl retards the evolution of generalists. Other mutations that repeatedly appear in replicate experiments are adaptations to the chemostat environment and are not specific to one or the other sugar.

Fig. 1.

Duplications at lac always involve IS elements. Horizontal lines represent the extent of each duplication with the terminal IS elements located in base pairs on the MG1655 chromosome and DD numbers identifying the evolvants. Duplications above the chromosome are found in descendants of TD2, those below in descendants of TD10. Resident elements (bold typeface) are labeled above (TD2) and below (TD10) the chromosome. The lac operon is boxed in.

Fig. 2.

Four types of deletions always involve IS elements. Horizontal lines represent the extent of each deletion with the terminal IS elements located in base pairs on the MG1655 chromosome and DD numbers identifying the evolvants. Resident elements (bold typeface) are labeled above the chromosome. Unique to TD10 is IS3-a, which is associated with type III deletions and lac duplications in strains DD2255 and DD2268 but only with a type III deletion in DD2259.