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Abstract DNA methylation at the fifth position of cytosine (5-methylcytosine, 5mC) is a crucial epigenetic modification for regulating gene expression, but little is known about how it regulates gene expression in insects. Here, we pursue the detailed molecular mechanism by which DNMT1-mediated 5mC maintenance regulates female reproduction in the German cockroach, Blattella germanica. Our results show that Dnmt1 knockdown decreases the level of 5mC in the ovary, upregulating numerous genes during choriogenesis, especially the transcription factor ftz-f1. The hypomethylation at the ftz-f1 promoter region increases and prolongs ftz-f1 expression in ovarian follicle cells during choriogenesis, which consequently causes aberrantly high levels of 20-hydroxyecdysone and excessively upregulates the extracellular matrix remodeling gene Mmp1. These changes further impair choriogenesis and disrupt fertilization by causing anoikis of the follicle cells, a shortage of chorion proteins, and malformation of the sponge-like bodies. This study significantly advances our understanding of how DNA 5mC modification regulates female reproduction in insects.

The American cockroach, Periplaneta americana (Insecta: Blattodea: Solumblattodea: Blattidae), is an urban hygiene pest but also a model organism for physiology and neuroscience study. However, the current description of the developmental process of the American cockroach is insufficient. In this study, we provide a life table of the American cockroach in a stable environment, including embryonic development, nymphal instars and adult reproduction. Our results show that there are 14 nymphal instars of the American cockroach in groups with sufficient living materials and space. The secondary sexual characteristics are evident in last-instar nymphs and adults, namely, the complete absence of the anal stylus in females. The entire embryonic development process was divided into 20 stages on the basis of lateral-view observations of the embryos. The formation of the embryo involves the fusion of paired blastoderm regions with higher cellular density, similar to that in other insects of Polyneoptera. With respect to reproduction, the gamogenetic females produced their first ootheca earlier than the parthenogenic females, and the frequency of oviposition was higher for the former throughout adulthood. Interestingly, group living seems to improve the parthenogenesis success rate in the American cockroach.