The origin and molecular evolution of two multigene families: G-protein coupled receptors and glycoside hydrolase families

Multigene family is a group of genes that arose from a common ancestor by gene duplication. Gene duplications are a major driving force of new function acquisition. Multigene family thus has a fundamental role in adaptation. To elucidate their molecular evolutionary mechanisms, I chose two multigene families: chemosensory receptors and glycoside hydrolases. I have identified complete repertoires of trace amine-associated receptors (TAARs), a member of chemosensory receptors, from 38 metazoan genomes. An ancestral-type TAAR emerged before the divergence between gnathostomes (jawed vertebrates) and sea lamprey (jawless fish). Primary amine detecting TAARs (TAAR1-4) are found to be older and have evolved under strong functional constraints. In contrast, tertiary amine detectors (TAAR5-9) emerged later, experienced higher rates of gene duplications, and experienced positive selection that could have affected ligand-binding activities and specificities. Expansions of tertiary amine detectors must have played important roles in terrestrial adaptations of therian mammals. During the primate evolution, TAAR gene losses are found to be a major trend. Relaxed selective constraints found in primate lineages of TAARs support dispensability of these primate genes. Reduced predator exposures owing to the start of arboreal life by ancestoral primates may attribute to this change. For another type of multigene family, glycoside hydrolase (GH) genes were identified in the western corn rootworm, Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae). Three GH family genes (GH45, GH48, and GH28) were found only in two coleopteran superfamilies (Chrysomeloidea and Curculionoidea) among insects (except for hemipteran GH28s), indicating their origin from horizontal gene transfer (HGT). Several independent HGTs in fungi and other insects were also detected. Two multigene families in this study are characterized with frequent gene duplications and losses, the birth-and-death process. A high rate of HGTs found in the GH family gene evolution must have accelerated functional evolution. In conclusion, this study showed that birth-and-death process, positive selection, and HGTs, all play a critical role in driving the evolution of multigene families and allow organismal adaptation to novel environmental niches