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Domestication Explains Two-Thirds of Differential-Gene-Expression Variance between Domestic and Wild Animals; The Remaining One-Third Reflects Intraspecific and Interspecific Variation

SIMPLE SUMMARY: Before genomes were sequenced, zoologists had discovered destabilizing selection as a general pattern of animal domestication that in foxes and minks had yielded fur colors never seen in the wild. Today, known genomes of humans and domestic and wild animals arouse interest in a commo...

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Autores principales: Chadaeva, Irina, Ponomarenko, Petr, Kozhemyakina, Rimma, Suslov, Valentin, Bogomolov, Anton, Klimova, Natalya, Shikhevich, Svetlana, Savinkova, Ludmila, Oshchepkov, Dmitry, Kolchanov, Nikolay A., Markel, Arcady, Ponomarenko, Mikhail
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8465180/
https://www.ncbi.nlm.nih.gov/pubmed/34573632
http://dx.doi.org/10.3390/ani11092667
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author Chadaeva, Irina
Ponomarenko, Petr
Kozhemyakina, Rimma
Suslov, Valentin
Bogomolov, Anton
Klimova, Natalya
Shikhevich, Svetlana
Savinkova, Ludmila
Oshchepkov, Dmitry
Kolchanov, Nikolay A.
Markel, Arcady
Ponomarenko, Mikhail
author_facet Chadaeva, Irina
Ponomarenko, Petr
Kozhemyakina, Rimma
Suslov, Valentin
Bogomolov, Anton
Klimova, Natalya
Shikhevich, Svetlana
Savinkova, Ludmila
Oshchepkov, Dmitry
Kolchanov, Nikolay A.
Markel, Arcady
Ponomarenko, Mikhail
author_sort Chadaeva, Irina
collection PubMed
description SIMPLE SUMMARY: Before genomes were sequenced, zoologists had discovered destabilizing selection as a general pattern of animal domestication that in foxes and minks had yielded fur colors never seen in the wild. Today, known genomes of humans and domestic and wild animals arouse interest in a common whole-genome pattern of animal domestication that may at least explain differences between the effects of natural and artificial environments on organisms. Accordingly, here we identified genes differing in expression between tame and aggressive rats (a laboratory domestication model) to compare them with all such known changes of genes’ activity (available in databases) in other domestic versus wild animals (e.g., dogs versus wolves). The results show that the majority of these genes changed their expression similarly among all the domestic versus wild animals studied, i.e., explained two-thirds of the variance, while the remaining one-third reflected animal intraspecific and interspecific variation, just as the gold standard of variation in nature. Accordingly, here we found that the artificial environment of domestic animals alters activities of genes in the same direction as that seen in corresponding human genes during human diseases, whereas the natural environment maintains a normal gene expression pattern in wild animals (matching human health). ABSTRACT: Belyaev’s concept of destabilizing selection during domestication was a major achievement in the XX century. Its practical value has been realized in commercial colors of the domesticated fox that never occur in the wild and has been confirmed in a wide variety of pet breeds. Many human disease models involving animals allow to test drugs before human testing. Perhaps this is why investigators doing transcriptomic profiling of domestic versus wild animals have searched for breed-specific patterns. Here we sequenced hypothalamic transcriptomes of tame and aggressive rats, identified their differentially expressed genes (DEGs), and, for the first time, applied principal component analysis to compare them with all the known DEGs of domestic versus wild animals that we could find. Two principal components, PC1 and PC2, respectively explained 67% and 33% of differential-gene-expression variance (hereinafter: log(2) value) between domestic and wild animals. PC1 corresponded to multiple orthologous DEGs supported by homologs; these DEGs kept the log(2) value sign from species to species and from tissue to tissue (i.e., a common domestication pattern). PC2 represented stand-alone homologous DEG pairs reversing the log(2) value sign from one species to another and from tissue to tissue (i.e., representing intraspecific and interspecific variation).
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spelling pubmed-84651802021-09-27 Domestication Explains Two-Thirds of Differential-Gene-Expression Variance between Domestic and Wild Animals; The Remaining One-Third Reflects Intraspecific and Interspecific Variation Chadaeva, Irina Ponomarenko, Petr Kozhemyakina, Rimma Suslov, Valentin Bogomolov, Anton Klimova, Natalya Shikhevich, Svetlana Savinkova, Ludmila Oshchepkov, Dmitry Kolchanov, Nikolay A. Markel, Arcady Ponomarenko, Mikhail Animals (Basel) Article SIMPLE SUMMARY: Before genomes were sequenced, zoologists had discovered destabilizing selection as a general pattern of animal domestication that in foxes and minks had yielded fur colors never seen in the wild. Today, known genomes of humans and domestic and wild animals arouse interest in a common whole-genome pattern of animal domestication that may at least explain differences between the effects of natural and artificial environments on organisms. Accordingly, here we identified genes differing in expression between tame and aggressive rats (a laboratory domestication model) to compare them with all such known changes of genes’ activity (available in databases) in other domestic versus wild animals (e.g., dogs versus wolves). The results show that the majority of these genes changed their expression similarly among all the domestic versus wild animals studied, i.e., explained two-thirds of the variance, while the remaining one-third reflected animal intraspecific and interspecific variation, just as the gold standard of variation in nature. Accordingly, here we found that the artificial environment of domestic animals alters activities of genes in the same direction as that seen in corresponding human genes during human diseases, whereas the natural environment maintains a normal gene expression pattern in wild animals (matching human health). ABSTRACT: Belyaev’s concept of destabilizing selection during domestication was a major achievement in the XX century. Its practical value has been realized in commercial colors of the domesticated fox that never occur in the wild and has been confirmed in a wide variety of pet breeds. Many human disease models involving animals allow to test drugs before human testing. Perhaps this is why investigators doing transcriptomic profiling of domestic versus wild animals have searched for breed-specific patterns. Here we sequenced hypothalamic transcriptomes of tame and aggressive rats, identified their differentially expressed genes (DEGs), and, for the first time, applied principal component analysis to compare them with all the known DEGs of domestic versus wild animals that we could find. Two principal components, PC1 and PC2, respectively explained 67% and 33% of differential-gene-expression variance (hereinafter: log(2) value) between domestic and wild animals. PC1 corresponded to multiple orthologous DEGs supported by homologs; these DEGs kept the log(2) value sign from species to species and from tissue to tissue (i.e., a common domestication pattern). PC2 represented stand-alone homologous DEG pairs reversing the log(2) value sign from one species to another and from tissue to tissue (i.e., representing intraspecific and interspecific variation). MDPI 2021-09-10 /pmc/articles/PMC8465180/ /pubmed/34573632 http://dx.doi.org/10.3390/ani11092667 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Chadaeva, Irina
Ponomarenko, Petr
Kozhemyakina, Rimma
Suslov, Valentin
Bogomolov, Anton
Klimova, Natalya
Shikhevich, Svetlana
Savinkova, Ludmila
Oshchepkov, Dmitry
Kolchanov, Nikolay A.
Markel, Arcady
Ponomarenko, Mikhail
Domestication Explains Two-Thirds of Differential-Gene-Expression Variance between Domestic and Wild Animals; The Remaining One-Third Reflects Intraspecific and Interspecific Variation
title Domestication Explains Two-Thirds of Differential-Gene-Expression Variance between Domestic and Wild Animals; The Remaining One-Third Reflects Intraspecific and Interspecific Variation
title_full Domestication Explains Two-Thirds of Differential-Gene-Expression Variance between Domestic and Wild Animals; The Remaining One-Third Reflects Intraspecific and Interspecific Variation
title_fullStr Domestication Explains Two-Thirds of Differential-Gene-Expression Variance between Domestic and Wild Animals; The Remaining One-Third Reflects Intraspecific and Interspecific Variation
title_full_unstemmed Domestication Explains Two-Thirds of Differential-Gene-Expression Variance between Domestic and Wild Animals; The Remaining One-Third Reflects Intraspecific and Interspecific Variation
title_short Domestication Explains Two-Thirds of Differential-Gene-Expression Variance between Domestic and Wild Animals; The Remaining One-Third Reflects Intraspecific and Interspecific Variation
title_sort domestication explains two-thirds of differential-gene-expression variance between domestic and wild animals; the remaining one-third reflects intraspecific and interspecific variation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8465180/
https://www.ncbi.nlm.nih.gov/pubmed/34573632
http://dx.doi.org/10.3390/ani11092667
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