Evolutionary origin and distribution of leucine-rich repeat-containing G protein-coupled receptors in insects.

ABSTRACT

Leucine-rich repeat-containing G protein-coupled receptors (LGRs) are crucial for animal growth and development. They were categorized into four types (A, B, C1, and C2) based on their sequence and domain structures. Despite the widespread distribution of LGRs across bilaterians, a thorough investigation of their distribution and evolutionary history remains elusive. Recent studies insect LGRs, especially the emergence of type C2 LGRs in various hemimetabolous insects, had prompted our study to address these problems. Initially, we traced the origins of LGRs by exploiting data from 99 species spanning 11 metazoan phyla, and discovered that type A and B LGRs originated from sponges, while type C LGRs originated from cnidarians. Subsequently, through comprehensive genomic and transcriptomic analyses across 565 species across 25 orders of insects, we found that both type A and C1 LGRs divided into two gene clusters. These clusters can be traced back to basal Insecta and an early ancestor of the Arthropoda, respectively. Furthermore, the absence of type B LGRs in wingless insects suggests a role in wing development, while the absence of type C2 LGRs in holometabolous insects hints at novel functions unrelated to insect metamorphosis. According to the origin of LGRs and the investigation of LGRs in insects, we speculated that type A and B LGRs appeared first among four types of LGRs, type A evolved into type C LGRs later, and type A and C1 LGRs independently duplicated during the evolutionary process. This study provides a more comprehensive view of the evolution of LGR genes than previously available, and sheds light on the evolutionary history and significance of LGRs in insect biology.