Transcriptomic basis and evolution of the ant nurse-larval social interactome.

Development is often strongly regulated by interactions among close relatives, but the underlying molecular mechanisms are largely unknown. In eusocial insects, interactions between caregiving worker nurses and larvae regulate larval development and resultant adult phenotypes. Here, we begin to char...

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Main Authors: Michael R Warner, Alexander S Mikheyev, Timothy A Linksvayer
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-05-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1008156
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author Michael R Warner
Alexander S Mikheyev
Timothy A Linksvayer
author_facet Michael R Warner
Alexander S Mikheyev
Timothy A Linksvayer
author_sort Michael R Warner
collection DOAJ
description Development is often strongly regulated by interactions among close relatives, but the underlying molecular mechanisms are largely unknown. In eusocial insects, interactions between caregiving worker nurses and larvae regulate larval development and resultant adult phenotypes. Here, we begin to characterize the social interactome regulating ant larval development by collecting and sequencing the transcriptomes of interacting nurses and larvae across time. We find that the majority of nurse and larval transcriptomes exhibit parallel expression dynamics across larval development. We leverage this widespread nurse-larva gene co-expression to infer putative social gene regulatory networks acting between nurses and larvae. Genes with the strongest inferred social effects tend to be peripheral elements of within-tissue regulatory networks and are often known to encode secreted proteins. This includes interesting candidates such as the nurse-expressed giant-lens, which may influence larval epidermal growth factor signaling, a pathway known to influence various aspects of insect development. Finally, we find that genes with the strongest signatures of social regulation tend to experience relaxed selective constraint and are evolutionarily young. Overall, our study provides a first glimpse into the molecular and evolutionary features of the social mechanisms that regulate all aspects of social life.
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spelling doaj.art-6579957d29fa4c1da783fa7cf05864fb2022-12-21T23:36:24ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042019-05-01155e100815610.1371/journal.pgen.1008156Transcriptomic basis and evolution of the ant nurse-larval social interactome.Michael R WarnerAlexander S MikheyevTimothy A LinksvayerDevelopment is often strongly regulated by interactions among close relatives, but the underlying molecular mechanisms are largely unknown. In eusocial insects, interactions between caregiving worker nurses and larvae regulate larval development and resultant adult phenotypes. Here, we begin to characterize the social interactome regulating ant larval development by collecting and sequencing the transcriptomes of interacting nurses and larvae across time. We find that the majority of nurse and larval transcriptomes exhibit parallel expression dynamics across larval development. We leverage this widespread nurse-larva gene co-expression to infer putative social gene regulatory networks acting between nurses and larvae. Genes with the strongest inferred social effects tend to be peripheral elements of within-tissue regulatory networks and are often known to encode secreted proteins. This includes interesting candidates such as the nurse-expressed giant-lens, which may influence larval epidermal growth factor signaling, a pathway known to influence various aspects of insect development. Finally, we find that genes with the strongest signatures of social regulation tend to experience relaxed selective constraint and are evolutionarily young. Overall, our study provides a first glimpse into the molecular and evolutionary features of the social mechanisms that regulate all aspects of social life.https://doi.org/10.1371/journal.pgen.1008156
spellingShingle Michael R Warner
Alexander S Mikheyev
Timothy A Linksvayer
Transcriptomic basis and evolution of the ant nurse-larval social interactome.
PLoS Genetics
title Transcriptomic basis and evolution of the ant nurse-larval social interactome.
title_full Transcriptomic basis and evolution of the ant nurse-larval social interactome.
title_fullStr Transcriptomic basis and evolution of the ant nurse-larval social interactome.
title_full_unstemmed Transcriptomic basis and evolution of the ant nurse-larval social interactome.
title_short Transcriptomic basis and evolution of the ant nurse-larval social interactome.
title_sort transcriptomic basis and evolution of the ant nurse larval social interactome
url https://doi.org/10.1371/journal.pgen.1008156
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