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Background <p>The evolution of castes in social insects is one of the most spectacular examples of phenotypic plasticity. However, this adaptive plasticity could instead be exploited by parasites to develop an extended phenotype. We characterize the timing and molecular changes induced by enigmatic twisted-wing insects to manipulate developing social wasps<i>.</i> These parasites reprogram short-lived female workers into phenotypes that are long-lived like queens, while hindering ovary development and cooperative behavior. Using differential gene expression analyses across developmental stages of naturally infected and uninfected brood coupled with experimental infections, we uncovered that parasites manipulate the developmental plasticity that determines caste bias.</p> Results <p>Parasite larvae infected most host larval instars. Across development, we identified 2341 differentially expressed genes (DEGs) between uninfected workers and gynes (future queens), 529 DEGs between infected and uninfected workers, and 2672 DEGs between infected workers and uninfected gynes. However, robust differences in the number of DEGs were unique to each host stage. Specifically, candidate genes linked caste bias to insulin and juvenile hormone pathways, immune responses, and neural development. Controlling for the effect of nutrition and social interactions in development through our infection experiment revealed that the parasites consistently targeted caste bias and neural genes. Finally, infecting long-lived gyne brood that is&#xa0;not targeted in nature showed minimal manipulation.</p> Conclusions <p>Our findings reveal how stage-specific targeting of caste plasticity initiates the reprogramming of hosts towards the long-lived extended phenotype. We propose leveraging emerging host-parasite systems to unravel the molecular mechanisms underlying adaptive developmental plasticity.</p>

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Transcriptomic analyses reveal how parasites exploit plasticity in caste and brain development of social wasps

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2026年8月5日

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  • Natasha A. Vacca,
  • Valeria Padilla-Choy,
  • Juan M. Ferro,
  • Floria M.K. Uy

摘要

Background

The evolution of castes in social insects is one of the most spectacular examples of phenotypic plasticity. However, this adaptive plasticity could instead be exploited by parasites to develop an extended phenotype. We characterize the timing and molecular changes induced by enigmatic twisted-wing insects to manipulate developing social wasps. These parasites reprogram short-lived female workers into phenotypes that are long-lived like queens, while hindering ovary development and cooperative behavior. Using differential gene expression analyses across developmental stages of naturally infected and uninfected brood coupled with experimental infections, we uncovered that parasites manipulate the developmental plasticity that determines caste bias.

Results

Parasite larvae infected most host larval instars. Across development, we identified 2341 differentially expressed genes (DEGs) between uninfected workers and gynes (future queens), 529 DEGs between infected and uninfected workers, and 2672 DEGs between infected workers and uninfected gynes. However, robust differences in the number of DEGs were unique to each host stage. Specifically, candidate genes linked caste bias to insulin and juvenile hormone pathways, immune responses, and neural development. Controlling for the effect of nutrition and social interactions in development through our infection experiment revealed that the parasites consistently targeted caste bias and neural genes. Finally, infecting long-lived gyne brood that is not targeted in nature showed minimal manipulation.

Conclusions

Our findings reveal how stage-specific targeting of caste plasticity initiates the reprogramming of hosts towards the long-lived extended phenotype. We propose leveraging emerging host-parasite systems to unravel the molecular mechanisms underlying adaptive developmental plasticity.