Not juvenilization: parasitic intersexuality in horsehair worm-infected insect hosts occurs only after host sexual differentiation

Abstract Parasite-induced interference in the development of insect sexual characteristics, resulting in intersexuality, provides valuable insights into the regulation of insect sexual differentiation. Horsehair worms are known to induce intersexuality in male mantids, leading to feminized wings and antennae. This phenomenon has been hypothesized to result from juvenilization, as insect sexual differentiation has traditionally been considered a cell-autonomous process, implying that parasites do not interfere with it directly. To investigate whether horsehair worm-induced intersexuality is linked to the host’s sexual differentiation process, we examined antennal morphology throughout post-embryonic development and the timing of the worm’s effects on the antennae. Our results revealed that sexual dimorphism in the antennal sensilla of Hierodula patellifera (Audinet-Serville, 1839) did not appear until the adult stage. In artificially infected male mantids, feminized antennae were observed an average of 22.26 d post-infection with the horsehair worm Chordodes formosanus Chiu, 2011. These feminized antennae were only observed in adult hosts, whereas last-instar males, which had not yet undergone sexual differentiation, showed no such changes. Additionally, red pigment patches typically associated with female abdomens from the third instar onward were observed in some infected males during late instar and adult stages. The timing of feminized antennae in infected males suggests that parasitic effects occur only after the host has undergone sexual differentiation. These findings indicate that parasitic intersexuality is linked to the regulation of the host’s sexual differentiation pathways rather than being a result of simple juvenilization.