The genetics and evolution of moth melanism in the absence of strong natural selection

Melanism is a common phenotypic variation in wild animals, and it provides valuable models for understanding how natural selection shapes biodiversity. The tea geometrid is prevailing in tea gardens of Asia and exhibits natural polymorphism in body and wing colors. Based on genetic linkage analysis, we mapped the melanism locus of this species to a 500 kb genomic interval, the 'cortex locus' that controls industrial melanism in distantly related moths in Britain. Investigations of different natural populations of tea geometrids and related species reveal the presence of multiple independent melanic loci within this highly variable hotspot region. Functional studies suggest that the major effector within this locus is the conserved microRNA, mir-193, which produces melanin pigment during pupal stages. By examining the evolutionary and ecological contexts of melanism in tea geometrids, we find that, in the apparent absence of strong natural selection such as camouflage advantage, potential reproductive disadvantages might contribute to the low genetic diversity and the minor fraction of melanic morphs in wild populations. Our study synthesizes genetic and ecological information to propose an evolutionary scenario in which a highly variable hotspot locus may fuel the repeated occurrence of non-adaptive phenotypic variations, ultimately shaping the biodiversity in nature.