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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...
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Published in: | Genome biology and evolution 2021-12, Vol.13 (12) |
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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. |
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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.</description><identifier>ISSN: 1759-6653</identifier><identifier>EISSN: 1759-6653</identifier><identifier>DOI: 10.1093/gbe/evab261</identifier><identifier>PMID: 34850870</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Animals ; Bees - genetics ; Cytochrome P-450 Enzyme System - genetics ; Evolution, Molecular ; Male ; Multigene Family ; Phylogeny</subject><ispartof>Genome biology and evolution, 2021-12, Vol.13 (12)</ispartof><rights>The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. 2021</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.</rights><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c412t-90a7fa7a18b7779caf5018557b758fe70db514ab4284961b0f35438b2b8a7fc53</citedby><cites>FETCH-LOGICAL-c412t-90a7fa7a18b7779caf5018557b758fe70db514ab4284961b0f35438b2b8a7fc53</cites><orcidid>0000-0002-9215-014X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8670302/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8670302/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,1598,27903,27904,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34850870$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Hoffmann, Federico</contributor><creatorcontrib>Darragh, Kathy</creatorcontrib><creatorcontrib>Nelson, David R</creatorcontrib><creatorcontrib>Ramírez, Santiago R</creatorcontrib><title>The Birth-and-Death Evolution of Cytochrome P450 Genes in Bees</title><title>Genome biology and evolution</title><addtitle>Genome Biol Evol</addtitle><description>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.</description><subject>Animals</subject><subject>Bees - genetics</subject><subject>Cytochrome P-450 Enzyme System - genetics</subject><subject>Evolution, Molecular</subject><subject>Male</subject><subject>Multigene Family</subject><subject>Phylogeny</subject><issn>1759-6653</issn><issn>1759-6653</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><recordid>eNp9kE1PAjEQhhujEURP3k1PXsxKu_3cC4kgogmJHvDctMuUXQNbsl1I-PeuAQlePM0k87zvJA9Ct5Q8UpKx_sJBH7bWpZKeoS5VIkukFOz8ZO-gqxi_CJGSS3aJOoxrQbQiXTSYFYCHZd0Uia3myTPYpsDjbVhumjJUOHg82jUhL-qwAvzBBcETqCDissJDgHiNLrxdRrg5zB76fBnPRq_J9H3yNnqaJjmnaZNkxCpvlaXaKaWy3HpBqBZCOSW0B0XmTlBuHU81zyR1xDPBmXap020wF6yHBvve9catYJ5D1dR2adZ1ubL1zgRbmr-XqizMImyNloowkrYFD_uCvA4x1uCPWUrMj0bTajQHjS19d_ruyP56a4H7PRA263-bvgHiN3tE</recordid><startdate>20211201</startdate><enddate>20211201</enddate><creator>Darragh, Kathy</creator><creator>Nelson, David R</creator><creator>Ramírez, Santiago R</creator><general>Oxford University Press</general><scope>TOX</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-9215-014X</orcidid></search><sort><creationdate>20211201</creationdate><title>The Birth-and-Death Evolution of Cytochrome P450 Genes in Bees</title><author>Darragh, Kathy ; Nelson, David R ; Ramírez, Santiago R</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c412t-90a7fa7a18b7779caf5018557b758fe70db514ab4284961b0f35438b2b8a7fc53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>Bees - genetics</topic><topic>Cytochrome P-450 Enzyme System - genetics</topic><topic>Evolution, Molecular</topic><topic>Male</topic><topic>Multigene Family</topic><topic>Phylogeny</topic><toplevel>online_resources</toplevel><creatorcontrib>Darragh, Kathy</creatorcontrib><creatorcontrib>Nelson, David R</creatorcontrib><creatorcontrib>Ramírez, Santiago R</creatorcontrib><collection>Oxford Open</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genome biology and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Darragh, Kathy</au><au>Nelson, David R</au><au>Ramírez, Santiago R</au><au>Hoffmann, Federico</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Birth-and-Death Evolution of Cytochrome P450 Genes in Bees</atitle><jtitle>Genome biology and evolution</jtitle><addtitle>Genome Biol Evol</addtitle><date>2021-12-01</date><risdate>2021</risdate><volume>13</volume><issue>12</issue><issn>1759-6653</issn><eissn>1759-6653</eissn><abstract>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.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>34850870</pmid><doi>10.1093/gbe/evab261</doi><orcidid>https://orcid.org/0000-0002-9215-014X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Bees - genetics Cytochrome P-450 Enzyme System - genetics Evolution, Molecular Male Multigene Family Phylogeny |
title | The Birth-and-Death Evolution of Cytochrome P450 Genes in Bees |
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