Population Genetic and Functional Analysis of a cis-Regulatory Polymorphism in the DrosophilamelanogasterMetallothionein A gene.

Timothy Ramnarine,Ana Catalán,Amanda Glaser-Schmitt,John Parsch

doi:10.3390/genes10020147

Timothy Ramnarine, Ana Catalán + Show 2 more

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https://doi.org/10.3390/genes10020147

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Abstract

Although gene expression can vary extensively within and among populations, the genetic basis of this variation and the evolutionary forces that maintain it are largely unknown. In Drosophila melanogaster, a 49-bp insertion/deletion (indel) polymorphism in the Metallothionein A (MtnA) gene is associated with variation in MtnA expression and oxidative stress tolerance. To better understand the functional and evolutionary significance of this polymorphism, we investigated it in several worldwide populations. In a German population, the deletion was present at a high and stable frequency over multiple seasons and years, and was associated with increased MtnA expression. There was, however, no evidence that the polymorphism was maintained by overdominant, seasonally fluctuating, or sexually antagonistic selection. The deletion was rare in a population from the species’ ancestral range in sub-Saharan Africa and is likely the result of non-African admixture, suggesting that it spread to high frequency following the species’ out-of-Africa expansion. Using data from a North American population, we found that the deletion was associated with MtnA expression and tolerance to oxidative stress induced by menadione sodium bisulfite. Our results are consistent with the deletion being selectively favored in temperate populations due to the increased MtnA expression and oxidative stress tolerance that it confers.

Highlights

The expansion of a species into new territories provides the opportunity for adaptation to novel environmental conditions
Using data from a North American population, we found that the deletion was associated with Metallothionein A (MtnA) expression and tolerance to oxidative stress induced by menadione sodium bisulfite
The deletion is associated with increased tolerance to oxidative stress in isofemale lines derived from Europe and Asia [18]. These results suggest a scenario in which the MtnA 30 untranslated region (UTR) deletion is selectively favored in temperate environments due to the increased oxidative stress tolerance that it confers, which is mediated by higher MtnA expression levels

Summary

Introduction

The expansion of a species into new territories provides the opportunity for adaptation to novel environmental conditions. Given its well-understood genetics and experimental tractability, Drosophila melanogaster has become a leading model organism for studying the molecular basis of adaptation. These studies typically involve the comparison of DNA sequence and/or gene expression variation between populations from the ancestral (sub-Saharan African) and derived (cosmopolitan) species ranges [1,2,3,4,5,6,7], or among multiple populations spanning an environmental gradient, such as a latitudinal cline [8,9,10]. Some genetic variants show repeated oscillations in frequency across seasons in temperate populations [15]

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