Comparative Population Analysis of Metallothionein Promoter Alleles Suggests Stress-induced Microevolution in the Field

Abstract

We investigate a model system for microevolution of transcriptional regulation: metallothionein expression in springtails. A previous survey of the metallothionein promoter in Orchesella cincta (Collembola) revealed nine alleles with differential basal activities and responses to cadmium and oxidative stress. In this study, 23 woodlands, with a divergent degree of pollution, were sampled, and heavy metals were measured. When grouped to their contamination degree, they were discriminated best on the pmtD2 metallothionein promoter allele frequency, which was higher in populations from heavily polluted sites. Taken together with previous work showing high inducibility of the pmtD2 promoter allele by Cd in a reporter assay, this suggests a fitness advantage of the pmtD2 allele in polluted sites. Redundancy analysis revealed associations between allele frequencies and specific metals in the environment, resulting in a subdivision between pollution associated alleles and others. A positive relationship between the pmtD2 allele frequency and the Cd content of the soil as well as between pmtE and Ni in the litter emerged. An increase of genetic diversity was observed with increasing Pb in the soil, reached through substitution of the pmtA1 allele, suggesting balancing selection. Our results illustrate that environmental factors can exert selection on promoter polymorphisms and cause adaptation through altered transcriptional regulation.