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Canalized gene expression during development mediates caste differentiation in ants.

Bitao Qiu1,2, Xueqin Dai3,4, Panyi Li5

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Ant colonies exhibit specialized castes, with gene expression predicting phenotypes. Juvenile hormone signaling and canalized gene expression regulate caste development, ensuring colony robustness.

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Area of Science:

  • Evolutionary developmental biology
  • Insect genetics
  • Social insect biology

Background:

  • Ant colonies display distinct castes (reproductive and non-reproductive individuals) with early developmental differentiation, analogous to germ-soma segregation.
  • While epigenetic factors are implicated, the specific genes governing ant caste phenotypes throughout development remain largely unknown.

Purpose of the Study:

  • To identify the gene sets responsible for caste determination in ants.
  • To understand the developmental trajectories and canalization of caste phenotypes.
  • To investigate the role of juvenile hormone signaling in caste differentiation.

Main Methods:

  • Analysis of over 1,400 whole-genome transcriptomes from two ant species (Monomorium pharaonis and Acromyrmex echinatior).
  • Development and application of a novel backward prediction algorithm for phenotype prediction from transcriptomic data.
  • Quantification of gene-specific canalization levels and enrichment analysis for caste-biased genes.

Main Results:

  • Caste phenotypes were accurately predicted using genome-wide transcriptome profiling.
  • Caste differentiation becomes increasingly canalized during development, especially in gynes (future queens).
  • The juvenile hormone signaling pathway was identified as crucial for regulating body mass divergence between castes.
  • Canalized genes with gyne-biased expression were linked to ovary and wing functions, while worker-biased genes were associated with brain and behavioral functions.
  • Suppression of the gyne-biased gene Freja disrupted pupal development, leading to intermediate phenotypes.

Conclusions:

  • Developmental trajectories in ants are highly canalized, ensuring robust caste determination.
  • Natural selection actively maintains these canalized caste phenotypes, contributing to colony life cycle stability.
  • The study provides insights into the genetic architecture underlying social insect caste evolution.