Tomas Kay, Joanito Liberti, Thomas O Richardson, Sean K McKenzie, Chelsea A Weitekamp, Christine La Mendola, Matthias Rüegg, Lucie Kesner, Natasha Szombathy, Sean McGregor, Jonathan Romiguier, Philipp Engel, Laurent Keller
{"title":"社会网络位置是蚂蚁行为、微生物群组成和大脑基因表达的主要预测因子。","authors":"Tomas Kay, Joanito Liberti, Thomas O Richardson, Sean K McKenzie, Chelsea A Weitekamp, Christine La Mendola, Matthias Rüegg, Lucie Kesner, Natasha Szombathy, Sean McGregor, Jonathan Romiguier, Philipp Engel, Laurent Keller","doi":"10.1371/journal.pbio.3002203","DOIUrl":null,"url":null,"abstract":"<p><p>The physiology and behavior of social organisms correlate with their social environments. However, because social environments are typically confounded by age and physical environments (i.e., spatial location and associated abiotic factors), these correlations are usually difficult to interpret. For example, associations between an individual's social environment and its gene expression patterns may result from both factors being driven by age or behavior. Simultaneous measurement of pertinent variables and quantification of the correlations between these variables can indicate whether relationships are direct (and possibly causal) or indirect. Here, we combine demographic and automated behavioral tracking with a multiomic approach to dissect the correlation structure among the social and physical environment, age, behavior, brain gene expression, and microbiota composition in the carpenter ant Camponotus fellah. Variations in physiology and behavior were most strongly correlated with the social environment. Moreover, seemingly strong correlations between brain gene expression and microbiota composition, physical environment, age, and behavior became weak when controlling for the social environment. Consistent with this, a machine learning analysis revealed that from brain gene expression data, an individual's social environment can be more accurately predicted than any other behavioral metric. These results indicate that social environment is a key regulator of behavior and physiology.</p>","PeriodicalId":20240,"journal":{"name":"PLoS Biology","volume":"21 7","pages":"e3002203"},"PeriodicalIF":7.8000,"publicationDate":"2023-07-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10399779/pdf/","citationCount":"0","resultStr":"{\"title\":\"Social network position is a major predictor of ant behavior, microbiota composition, and brain gene expression.\",\"authors\":\"Tomas Kay, Joanito Liberti, Thomas O Richardson, Sean K McKenzie, Chelsea A Weitekamp, Christine La Mendola, Matthias Rüegg, Lucie Kesner, Natasha Szombathy, Sean McGregor, Jonathan Romiguier, Philipp Engel, Laurent Keller\",\"doi\":\"10.1371/journal.pbio.3002203\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>The physiology and behavior of social organisms correlate with their social environments. However, because social environments are typically confounded by age and physical environments (i.e., spatial location and associated abiotic factors), these correlations are usually difficult to interpret. For example, associations between an individual's social environment and its gene expression patterns may result from both factors being driven by age or behavior. Simultaneous measurement of pertinent variables and quantification of the correlations between these variables can indicate whether relationships are direct (and possibly causal) or indirect. Here, we combine demographic and automated behavioral tracking with a multiomic approach to dissect the correlation structure among the social and physical environment, age, behavior, brain gene expression, and microbiota composition in the carpenter ant Camponotus fellah. Variations in physiology and behavior were most strongly correlated with the social environment. Moreover, seemingly strong correlations between brain gene expression and microbiota composition, physical environment, age, and behavior became weak when controlling for the social environment. Consistent with this, a machine learning analysis revealed that from brain gene expression data, an individual's social environment can be more accurately predicted than any other behavioral metric. These results indicate that social environment is a key regulator of behavior and physiology.</p>\",\"PeriodicalId\":20240,\"journal\":{\"name\":\"PLoS Biology\",\"volume\":\"21 7\",\"pages\":\"e3002203\"},\"PeriodicalIF\":7.8000,\"publicationDate\":\"2023-07-24\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10399779/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"PLoS Biology\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1371/journal.pbio.3002203\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2023/7/1 0:00:00\",\"PubModel\":\"eCollection\",\"JCR\":\"Q1\",\"JCRName\":\"BIOCHEMISTRY & MOLECULAR BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"PLoS Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1371/journal.pbio.3002203","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2023/7/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
Social network position is a major predictor of ant behavior, microbiota composition, and brain gene expression.
The physiology and behavior of social organisms correlate with their social environments. However, because social environments are typically confounded by age and physical environments (i.e., spatial location and associated abiotic factors), these correlations are usually difficult to interpret. For example, associations between an individual's social environment and its gene expression patterns may result from both factors being driven by age or behavior. Simultaneous measurement of pertinent variables and quantification of the correlations between these variables can indicate whether relationships are direct (and possibly causal) or indirect. Here, we combine demographic and automated behavioral tracking with a multiomic approach to dissect the correlation structure among the social and physical environment, age, behavior, brain gene expression, and microbiota composition in the carpenter ant Camponotus fellah. Variations in physiology and behavior were most strongly correlated with the social environment. Moreover, seemingly strong correlations between brain gene expression and microbiota composition, physical environment, age, and behavior became weak when controlling for the social environment. Consistent with this, a machine learning analysis revealed that from brain gene expression data, an individual's social environment can be more accurately predicted than any other behavioral metric. These results indicate that social environment is a key regulator of behavior and physiology.
期刊介绍:
PLOS Biology is an open-access, peer-reviewed general biology journal published by PLOS, a nonprofit organization of scientists and physicians dedicated to making the world's scientific and medical literature freely accessible. The journal publishes new articles online weekly, with issues compiled and published monthly.
ISSN Numbers:
eISSN: 1545-7885
ISSN: 1544-9173