Abstract
BACKGROUND: The Chinese mitten crab (Eriocheir sinensis), an economically critical migratory species inhabiting both freshwater and marine environments, is susceptible to parasitization by the rhizocephalan barnacle Polyascus sp. in estuarine ecosystems. In this study, E. sinensis was found to be parasitized by Polyascus sp. in the freshwater waters of the Anqing section of the Yangtze River, which manifested itself as restricted growth and development, hindered gonadal development, and apparent changes in sexual characteristics. METHODS: Morphological analysis, serological testing, and eyestalk transcriptome analysis were conducted on male and female parasitized and non-parasitized crabs to investigate the molecular mechanisms by which Polyascus sp. affects host growth and reproduction. RESULTS: The study revealed that parasitized hosts of both sexes were significantly smaller than normal individuals and exhibited gonadal atrophy. Male hosts displayed feminization of secondary sexual characteristics, whereas females showed no significant alterations. Testosterone and ecdysterone levels decreased in male hosts, whereas estradiol levels declined in female hosts. Transcriptomic profiling revealed differentially expressed genes predominantly associated with metabolic processes, stimulus response, signal transduction, and reproduction. Thirteen key candidate genes related to parasite-induced suppression of host molting and growth, fourteen key candidate genes involved in male reproductive regulation, and ten candidate genes affecting female gonadal development were identified. Key genes involved in gonadal development-including 5-HT1B, CHH, MIH, JHE1, Dmrt family, cytochrome P450 family, Abd-A, and Antp exhibited sex-specific expression patterns. Additionally, critical growth-related genes such as Dib, HR38, and Cht3 exhibited significant alterations in hosts of both sexes. Polyascus sp. parasitism suppresses gonadal development and growth in both sexes, employing distinct regulatory strategies. It uses a "neuroendocrine disruption and reproductive gene regulation" strategy to regulate reproductive development in male hosts, while influencing female reproductive metabolism through a "Nutrient Hijacking-Hormonal Suppression" mechanism. Additionally, the parasitism disrupts host growth via "molting inhibition". These findings elucidate the sex-specific metabolic, reproductive, and growth disruption strategies of Polyascus sp., providing new insights into host-parasite interactions in decapod crustaceans.