Vitellogenin-like A-associated shifts in social cue responsiveness regulate behavioral task specialization in an ant

PLoS Biol. 2018 Jun 6;16(6):e2005747. doi: 10.1371/journal.pbio.2005747. eCollection 2018 Jun.

Abstract

Division of labor and task specialization explain the success of human and insect societies. Social insect colonies are characterized by division of labor, with workers specializing in brood care early and foraging later in life. Theory posits that this task switching requires shifts in responsiveness to task-related cues, yet experimental evidence is weak. Here, we show that a Vitellogenin (Vg) ortholog identified in an RNAseq study on the ant T. longispinosus is involved in this process: using phylogenetic analyses of Vg and Vg-like genes, we firstly show that this candidate gene does not cluster with the intensively studied honey bee Vg but falls into a separate Vg-like A cluster. Secondly, an experimental knockdown of Vg-like A in the fat body caused a reduction in brood care and an increase in nestmate care in young ant workers. Nestmate care is normally exhibited by older workers. We demonstrate experimentally that this task switch is at least partly based on Vg-like A-associated shifts in responsiveness from brood to worker cues. We thus reveal a novel mechanism leading to early behavioral maturation via changes in social cue responsiveness mediated by Vg-like A and associated pathways, which proximately play a role in regulating division of labor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aging / genetics
  • Aging / physiology
  • Animals
  • Ants / genetics
  • Ants / physiology*
  • Bees / genetics
  • Bees / physiology
  • Behavior, Animal / physiology*
  • Cues
  • Fat Body / physiology
  • Female
  • Gene Knockdown Techniques
  • Gene Regulatory Networks
  • Genes, Insect
  • Hymenoptera / genetics
  • Hymenoptera / physiology
  • Insect Proteins / antagonists & inhibitors
  • Insect Proteins / genetics
  • Insect Proteins / physiology*
  • Male
  • Models, Biological
  • Multigene Family
  • Phylogeny
  • Social Behavior
  • Species Specificity
  • Vitellogenins / antagonists & inhibitors
  • Vitellogenins / genetics
  • Vitellogenins / physiology*

Substances

  • Insect Proteins
  • Vitellogenins

Associated data

  • Dryad/10.5061/dryad.s114355

Grants and funding

Rhineland-Palatinate’s Ministry of Education, Science, Further Education and Cultural Affairs (grant number GeneRed). Received by SF and BF. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Edmund Niles Huyck Preserve (Research Grants in 2014, 2015, 2016). Received by PK, BF, SF. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.