Aedes aegypti exhibits a distinctive mode of late ovarian development

Insects live in almost every habitat on earth. To adapt to their diverse environments, insects have developed a myriad of different strategies for reproduction reflected in diverse anatomical and behavioral features that the reproductive systems of females exhibit. Yet, ovarian development remains largely uncharacterized in most species except Drosophila melanogaster (D. melanogaster), a high Diptera model. In this study, we investigated the detailed developmental process of the ovary in Aedes aegypti (Ae. aegypti), a major vector of various disease-causing pathogens that inhabits tropical and subtropical regions.

Compared with Drosophila melanogaster, a model of higher Diptera, the processes of pole cell formation and gonad establishment during embryonic stage are highly conserved in Ae. aegypti. However, Ae. aegypti utilizes a distinct strategy to form functional ovaries during larval/pupal development. First, during larval stage, Ae. aegypti primordial germ cells (PGCs) undergo a cyst-like proliferation with synchronized divisions and incomplete cytokinesis, leading to the formation of one tightly packed "PGC mass" containing several interconnected cysts, different from D. melanogaster PGCs that divide individually. This cyst-like proliferation is regulated by the target of rapamycin (TOR) pathway upon nutritional status. Second, ecdysone-triggered ovariole formation during metamorphosis exhibits distinct events, including "PGC mass" breakdown, terminal filament cell degeneration, and pre-ovariole migration. These unique developmental features might explain the structural and behavioral differences between Aedes and Drosophila ovaries. Importantly, both cyst-like proliferation and distinct ovariole formation are also observed in Culex quinquefasciatus and Anopheles sinensis, suggesting a conserved mode of ovarian development among mosquito species. In comparison with Drosophila, the ovarian development in Aedes and other mosquitoes might represent a primitive mode in the lower Diptera.

Our study reveals a new mode of ovarian development in mosquitoes, providing insights into a better understanding of the reproductive system and evolutionary relationship among insects.