Heterochromatin protein 1 (HP1) dysfunction drives male-biased sex ratio in Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae) via paternal genome elimination during mitosis.

BACKGROUND: A male-biased sex ratio (MBS) is a widespread phenomenon in nature, which contributes to inbreeding avoidance, more efficient resource allocation, and the regulation of population dynamics. The factors driving MBS primarily involve genetic and chromosomal mechanisms, environmental conditions, and the influence of endosymbiotic microorganisms. However, the underlying molecular mechanism remains largely elusive. This study aims to investigate the role of Heterochromatin protein 1 (HP1) in driving an extreme MBS in the parasitic wasp Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae). RESULTS: An extremely male-biased T. dendrolimi line was identified from field collections, with a male offspring proportion of 80-100% (vs. 20-30% in the bisexual line). In this line, HP1 expression was significantly downregulated to 9% in male individuals compared to their counterparts in the bisexual line (p < 0.001). RNAi knockdown of HP1 in male pupae efficiently reduced its expression to 17%, 13%, and 21% of control levels at 12-, 24-, and 48 h post-injection, respectively (p < 0.01). HP1 depletion resulted in chromatin condensation defects and exclusive production of male offspring due to the haplodiploid sex-determination system, resembling those observed in male-biased line. Paternal origin of the abnormal chromatin was confirmed by internal transcribed spacer 2 of the ribosomal DNA (ITS2) sequence analysis. CONCLUSION: Our findings demonstrate that HP1 is a crucial regulator of chromatin dynamics underlying paternal genome elimination and sex ratio determination. This discovery not only advances our understanding of sex ratio manipulation in Hymenoptera but also identifies HP1 as a promising molecular target for enhancing the efficiency of parasitic wasps in biological pest control.