Divergent enhancer haplotype of ebony on inversion In(3R)Payne associated with pigmentation variation in a tropical population of Drosophila melanogaster

Abstract

The pattern and intensity of pigmentation have direct impact on individual fitness through various ecological factors. In a Drosophila melanogaster population from southern Japan, thoracic trident pigmentation intensity of most of the strains could be classified into Dark or Light-type. The expression level variation of the ebony gene correlated well with this phenotype and the allelic differences in expression indicated that the variation is partly due to cis-regulatory changes. In the ∼13 kb gene region, we identified 17 nucleotide sites and 2 indels that were in complete association with the thoracic trident pigmentation intensity. Interestingly, 11 out of 19 sites located within ∼0.5 kb of the core epidermis enhancer. These sites had no obvious association with the abdominal pigmentation intensity in the previously analysed African populations from Uganda and Kenya, which suggested that multiple potential mutational pathways in the cis-regulatory control region of a single gene could lead to similar phenotypic variation within this species. We also found that the Light-type enhancer haplotype is strongly linked to a cosmopolitan inversion, In(3R)Payne, which is predominant in warmer climatic regions in both hemispheres. The sequence pattern suggested that the strong linkage may be due to selective forces related to thermal adaptation. The inferred selection for lighter pigmentation in the Japanese population is in the opposite direction of the previously reported case of selection for darker individuals in African populations. Nevertheless, both adaptive changes involved cis-regulatory changes of ebony, which shows that this gene is likely to be a common target of natural selection.