The genomic landscape of metallic color variation in ground beetles

Abstract

AbstractThe metallic color variation of beetles is a spectacular feature that has inspired diverse human cultures. However, little is known about the genetic basis of this trait or its ecological importance. In this study, we characterize the geographical distribution, optical mechanism, genetic basis, and ecological and evolutionary importance of metallic color variation in theNebria ingenscomplex, an alpine ground beetle in the Sierra Nevada, California. We find that elytral color varies continuously across two allopatric species (from blackN. ingensto greenN. riversi), with hybrid populations showing intermediate coloration, and we demonstrate that the metallic color is generated from multilayer reflectors in the epicuticle of the elytra. By applying association mapping in natural populations (wild-GWAS) using high-density SNPs (1.2 million), we identify five promising candidate genes covarying with metallic variation, with known roles in cuticle formation and pigmentation pathways. Among these five genes, the geneyellow-like exhibits a heightened divergence pattern relative to the background genomic landscape and has been maintained despite gene flow. This finding, together with a significant correlation between color variation and water availability, suggests that metallic variation evolves as a local adaptation to environmental variation in theN. ingenscomplex.