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The Birth-and-Death Evolution of Cytochrome P450 Genes in Bees.

ABSTRACT: The birth-and-death model of multigene family evolution describes how gene families evolve and diversify through duplication and deletion. The cytochrome P450s are one of the most diverse and well-studied multigene families, involved in both physiological and xenobiotic functions. Extensive studies of insect P450 genes have demonstrated their role in insecticide resistance. Bees are thought to experience toxin exposure through their diet of nectar and pollen, as well as the resin-collecting behavior exhibited by some species. Here, we describe the repertoire of P450 genes in the orchid bee Euglossa dilemma. Male orchid bees form perfume bouquets used in courtship displays by collecting volatile compounds, resulting in exposure to compounds known to be toxic. In addition, we conducted phylogenetic and selection analyses across ten bee species encompassing three bee families. We find that social behavior and resin collection are not correlated with the repertoire of P450 present in a bee species. However, our analyses revealed that P450 clades can be classified as stable and unstable, and that genes involved in xenobiotic metabolism are more likely to belong to unstable clades. Furthermore, we find that unstable clades are under more dynamic evolutionary pressures and exhibit signals of adaptive evolution. This work highlights the complexity of multigene family evolution, revealing that multiple factors contribute to the diversification, stability, and dynamics of this gene family. Furthermore, we provide a resource for future detailed studies investigating the function of different P450s in economically important bee species.

SUBMITTER: Darragh K

PROVIDER: S-EPMC8670302 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Genes vary greatly in their long-term phylogenetic stability and there exists no general explanation for these differences. The cytochrome P450 (CYP450) gene superfamily is well suited to investigating this problem because it is large and well studied, and it includes both stable and unstable genes. CYP450 genes encode oxidase enzymes that function in metabolism of endogenous small molecules and in detoxification of xenobiotic compounds. Both types of enzymes have been intensively studied. My analysis of ten nearly complete vertebrate genomes indicates that each genome contains 50-80 CYP450 genes, which are about evenly divided between phylogenetically stable and unstable genes. The stable genes are characterized by few or no gene duplications or losses in species ranging from bony fish to mammals, whereas unstable genes are characterized by frequent gene duplications and losses (birth-death evolution) even among closely related species. All of the CYP450 genes that encode enzymes with known endogenous substrates are phylogenetically stable. In contrast, most of the unstable genes encode enzymes that function as xenobiotic detoxifiers. Nearly all unstable CYP450 genes in the mouse and human genomes reside in a few dense gene clusters, forming unstable gene islands that arose by recurrent local gene duplication. Evidence for positive selection in amino acid sequence is restricted to these unstable CYP450 genes, and sites of selection are associated with substrate-binding regions in the protein structure. These results can be explained by a general model in which phylogenetically stable genes have core functions in development and physiology, whereas unstable genes have accessory functions associated with unstable environmental interactions such as toxin and pathogen exposure. Unstable gene islands in vertebrates share some functional properties with bacterial genomic islands, though they arise by local gene duplication rather than horizontal gene transfer.

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The Birth-and-Death Evolution of Cytochrome P450 Genes in Bees.

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