The brain atlas of a subsocial bee reflects that of eusocial Hymenoptera
The evolutionary transition from solitary life to group‐living in a society with cooperative brood care, reproductive division of labor and morphological castes is associated with increased cognitive demands for task‐specialization. Associated with these demands, the brains of eusocial Hymenoptera d...
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description | The evolutionary transition from solitary life to group‐living in a society with cooperative brood care, reproductive division of labor and morphological castes is associated with increased cognitive demands for task‐specialization. Associated with these demands, the brains of eusocial Hymenoptera divide transcriptomic signatures associated with foraging and reproduction to different populations of cells and also show diverse astrocyte and Kenyon cell types compared with solitary non‐hymenopteran insects. The neural architecture of subsocial bees, which represent evolutionary antecedent states to eusocial Hymenoptera, could then show how widely this eusocial brain is conserved across aculeate Hymenoptera. Using single‐nucleus transcriptomics, we have created an atlas of neuron and glial cell types from the brain of a subsocial insect, the small carpenter bee (Ceratina calcarata). The proportion of C. calcarata neurons related to the metabolism of classes of neurotransmitters is similar to that of other insects, whereas astrocyte and Kenyon cell types show highly similar gene expression patterns to those of eusocial Hymenoptera. In the winter, the transcriptomic signature across the brain reflected diapause. When the bee was active in the summer, however, genes upregulated in neurons reflected foraging, while the gene expression signature of glia associated with reproductive functions. Like eusocial Hymenoptera, we conclude that neural components for foraging and reproduction in C. calcarata are compartmentalized to different parts of its brain. Cellular examination of the brains of other solitary and subsocial insects can show the extent of neurobiological conservation across levels of social complexity.
Single‐cell gene expression was used to develop the first brain atlas for a small carpenter bee describing neurons and glia cell types for this species. Astrocytes and Kenyon cell types are conserved across Hymenoptera in comparison to Diptera. Gene expression related to foraging and reproduction are separated to different brain cell populations. |
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Single‐cell gene expression was used to develop the first brain atlas for a small carpenter bee describing neurons and glia cell types for this species. Astrocytes and Kenyon cell types are conserved across Hymenoptera in comparison to Diptera. Gene expression related to foraging and reproduction are separated to different brain cell populations.</description><identifier>ISSN: 1601-1848</identifier><identifier>ISSN: 1601-183X</identifier><identifier>EISSN: 1601-183X</identifier><identifier>DOI: 10.1111/gbb.70007</identifier><identifier>PMID: 39513483</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Animals ; Bees - genetics ; Biological Evolution ; Brain ; Brain - metabolism ; Brain architecture ; brain evolution ; Brood care ; Castes ; cell type evolution ; Ceratina calcarata ; Diapause ; Division of labor ; Gene expression ; Glial cells ; Hymenoptera ; Insects ; Neuroglia - metabolism ; Neuronal-glial interactions ; Neurons - metabolism ; neurotransmitters ; Original ; single cell ; Social Behavior ; sociality ; Transcriptome ; Transcriptomics</subject><ispartof>Genes, brain and behavior, 2024-12, Vol.23 (6), p.e70007-n/a</ispartof><rights>2024 The Author(s). published by International Behavioural and Neural Genetics Society and John Wiley & Sons Ltd.</rights><rights>2024 The Author(s). Genes, Brain and Behavior published by International Behavioural and Neural Genetics Society and John Wiley & Sons Ltd.</rights><rights>2024. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3347-b909565d85ed07870c0dc47099c4c92c82899132c4d27cd16a169f7f17b12e263</cites><orcidid>0000-0002-6441-5155 ; 0000-0003-3180-9251 ; 0000-0001-5328-1377</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/PMC11544451/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11544451/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,1416,11553,27915,27916,45565,45566,46043,46467,53782,53784</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39513483$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Pyenson, Benjamin C.</creatorcontrib><creatorcontrib>Huisken, Jesse L.</creatorcontrib><creatorcontrib>Gupta, Nandini</creatorcontrib><creatorcontrib>Rehan, Sandra M.</creatorcontrib><title>The brain atlas of a subsocial bee reflects that of eusocial Hymenoptera</title><title>Genes, brain and behavior</title><addtitle>Genes Brain Behav</addtitle><description>The evolutionary transition from solitary life to group‐living in a society with cooperative brood care, reproductive division of labor and morphological castes is associated with increased cognitive demands for task‐specialization. Associated with these demands, the brains of eusocial Hymenoptera divide transcriptomic signatures associated with foraging and reproduction to different populations of cells and also show diverse astrocyte and Kenyon cell types compared with solitary non‐hymenopteran insects. The neural architecture of subsocial bees, which represent evolutionary antecedent states to eusocial Hymenoptera, could then show how widely this eusocial brain is conserved across aculeate Hymenoptera. Using single‐nucleus transcriptomics, we have created an atlas of neuron and glial cell types from the brain of a subsocial insect, the small carpenter bee (Ceratina calcarata). The proportion of C. calcarata neurons related to the metabolism of classes of neurotransmitters is similar to that of other insects, whereas astrocyte and Kenyon cell types show highly similar gene expression patterns to those of eusocial Hymenoptera. In the winter, the transcriptomic signature across the brain reflected diapause. When the bee was active in the summer, however, genes upregulated in neurons reflected foraging, while the gene expression signature of glia associated with reproductive functions. Like eusocial Hymenoptera, we conclude that neural components for foraging and reproduction in C. calcarata are compartmentalized to different parts of its brain. Cellular examination of the brains of other solitary and subsocial insects can show the extent of neurobiological conservation across levels of social complexity.
Single‐cell gene expression was used to develop the first brain atlas for a small carpenter bee describing neurons and glia cell types for this species. Astrocytes and Kenyon cell types are conserved across Hymenoptera in comparison to Diptera. Gene expression related to foraging and reproduction are separated to different brain cell populations.</description><subject>Animals</subject><subject>Bees - genetics</subject><subject>Biological Evolution</subject><subject>Brain</subject><subject>Brain - metabolism</subject><subject>Brain architecture</subject><subject>brain evolution</subject><subject>Brood care</subject><subject>Castes</subject><subject>cell type evolution</subject><subject>Ceratina calcarata</subject><subject>Diapause</subject><subject>Division of labor</subject><subject>Gene expression</subject><subject>Glial cells</subject><subject>Hymenoptera</subject><subject>Insects</subject><subject>Neuroglia - metabolism</subject><subject>Neuronal-glial interactions</subject><subject>Neurons - metabolism</subject><subject>neurotransmitters</subject><subject>Original</subject><subject>single cell</subject><subject>Social Behavior</subject><subject>sociality</subject><subject>Transcriptome</subject><subject>Transcriptomics</subject><issn>1601-1848</issn><issn>1601-183X</issn><issn>1601-183X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp1kUFLJDEQhYO4qDt68A9Ig5fdwzipJN1JTqKizoLgZQRvIZ2udlp6OmPS7TL_3uiMg7tgXaqgPh716hFyDPQMUk2eyvJMUkrlDjmAgsIYFH_c3c5C7ZOfMT5TCpIr2CP7XOfAheIHZDqbY1YG23SZ7VsbM19nNotDGb1rbJuViFnAukXXx6yf2_4dwGGzna4W2Pllj8Eekh-1bSMebfqIPNxcz66m47v72z9XF3djx7mQ41JTnRd5pXKsqFSSOlo5IanWTjjNnGJKa-DMiYpJV0FhodC1rEGWwJAVfETO17rLoVxg5bDrg23NMjQLG1bG28b8u-mauXnyrwYgF0Ik3yPya6MQ_MuAsTeLJjpsW9uhH6LhwBRnnINI6Ol_6LMfQpf8JUpo0Joxnajfa8oFH2P61vYaoOY9IJMCMh8BJfbk6_lb8jORBEzWwN-mxdX3Sub28nIt-QYNTJhv</recordid><startdate>202412</startdate><enddate>202412</enddate><creator>Pyenson, Benjamin C.</creator><creator>Huisken, Jesse L.</creator><creator>Gupta, Nandini</creator><creator>Rehan, Sandra M.</creator><general>Blackwell Publishing Ltd</general><general>John Wiley & Sons, Inc</general><scope>24P</scope><scope>WIN</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>7QG</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6441-5155</orcidid><orcidid>https://orcid.org/0000-0003-3180-9251</orcidid><orcidid>https://orcid.org/0000-0001-5328-1377</orcidid></search><sort><creationdate>202412</creationdate><title>The brain atlas of a subsocial bee reflects that of eusocial Hymenoptera</title><author>Pyenson, Benjamin C. ; Huisken, Jesse L. ; Gupta, Nandini ; Rehan, Sandra M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3347-b909565d85ed07870c0dc47099c4c92c82899132c4d27cd16a169f7f17b12e263</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Bees - genetics</topic><topic>Biological Evolution</topic><topic>Brain</topic><topic>Brain - metabolism</topic><topic>Brain architecture</topic><topic>brain evolution</topic><topic>Brood care</topic><topic>Castes</topic><topic>cell type evolution</topic><topic>Ceratina calcarata</topic><topic>Diapause</topic><topic>Division of labor</topic><topic>Gene expression</topic><topic>Glial cells</topic><topic>Hymenoptera</topic><topic>Insects</topic><topic>Neuroglia - metabolism</topic><topic>Neuronal-glial interactions</topic><topic>Neurons - metabolism</topic><topic>neurotransmitters</topic><topic>Original</topic><topic>single cell</topic><topic>Social Behavior</topic><topic>sociality</topic><topic>Transcriptome</topic><topic>Transcriptomics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Pyenson, Benjamin C.</creatorcontrib><creatorcontrib>Huisken, Jesse L.</creatorcontrib><creatorcontrib>Gupta, Nandini</creatorcontrib><creatorcontrib>Rehan, Sandra M.</creatorcontrib><collection>Wiley-Blackwell Open Access Titles</collection><collection>Wiley Free Content</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genes, brain and behavior</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Pyenson, Benjamin C.</au><au>Huisken, Jesse L.</au><au>Gupta, Nandini</au><au>Rehan, Sandra M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The brain atlas of a subsocial bee reflects that of eusocial Hymenoptera</atitle><jtitle>Genes, brain and behavior</jtitle><addtitle>Genes Brain Behav</addtitle><date>2024-12</date><risdate>2024</risdate><volume>23</volume><issue>6</issue><spage>e70007</spage><epage>n/a</epage><pages>e70007-n/a</pages><issn>1601-1848</issn><issn>1601-183X</issn><eissn>1601-183X</eissn><abstract>The evolutionary transition from solitary life to group‐living in a society with cooperative brood care, reproductive division of labor and morphological castes is associated with increased cognitive demands for task‐specialization. Associated with these demands, the brains of eusocial Hymenoptera divide transcriptomic signatures associated with foraging and reproduction to different populations of cells and also show diverse astrocyte and Kenyon cell types compared with solitary non‐hymenopteran insects. The neural architecture of subsocial bees, which represent evolutionary antecedent states to eusocial Hymenoptera, could then show how widely this eusocial brain is conserved across aculeate Hymenoptera. Using single‐nucleus transcriptomics, we have created an atlas of neuron and glial cell types from the brain of a subsocial insect, the small carpenter bee (Ceratina calcarata). The proportion of C. calcarata neurons related to the metabolism of classes of neurotransmitters is similar to that of other insects, whereas astrocyte and Kenyon cell types show highly similar gene expression patterns to those of eusocial Hymenoptera. In the winter, the transcriptomic signature across the brain reflected diapause. When the bee was active in the summer, however, genes upregulated in neurons reflected foraging, while the gene expression signature of glia associated with reproductive functions. Like eusocial Hymenoptera, we conclude that neural components for foraging and reproduction in C. calcarata are compartmentalized to different parts of its brain. Cellular examination of the brains of other solitary and subsocial insects can show the extent of neurobiological conservation across levels of social complexity.
Single‐cell gene expression was used to develop the first brain atlas for a small carpenter bee describing neurons and glia cell types for this species. Astrocytes and Kenyon cell types are conserved across Hymenoptera in comparison to Diptera. Gene expression related to foraging and reproduction are separated to different brain cell populations.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>39513483</pmid><doi>10.1111/gbb.70007</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-6441-5155</orcidid><orcidid>https://orcid.org/0000-0003-3180-9251</orcidid><orcidid>https://orcid.org/0000-0001-5328-1377</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Bees - genetics Biological Evolution Brain Brain - metabolism Brain architecture brain evolution Brood care Castes cell type evolution Ceratina calcarata Diapause Division of labor Gene expression Glial cells Hymenoptera Insects Neuroglia - metabolism Neuronal-glial interactions Neurons - metabolism neurotransmitters Original single cell Social Behavior sociality Transcriptome Transcriptomics |
title | The brain atlas of a subsocial bee reflects that of eusocial Hymenoptera |
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