A Peptide Signaling System that Rapidly Enforces Paternity in the Aedes aegypti Mosquito

Abstract

Female Aedes aegypti mosquitoes typically mate only once with one male in their lifetime, a behavior known as "monandry" [1]. This single mating event provisions the female with sufficient sperm to fertilize the >500 eggs she will produce during her ∼4- to 6-week lifespan in the laboratory [2]. Successful mating induces lifetime refractoriness to subsequent insemination by other males, enforcing the paternity of the first male [3-5]. Ae. aegypti mate in flight near human hosts [6], and females become refractory to remating within seconds [1, 3, 4], suggesting the existence of a rapid mechanism to prevent female remating. In this study, we implicate HP-I, an Aedes- and male-specific peptide transferred to females [7], and its cognate receptor in the female, NPYLR1 [8], in rapid enforcement of paternity. HP-I mutant males were ineffective in enforcing paternity when a second male was given access to the female within 1hr. NPYLR1 mutant females produced mixed paternity offspring at high frequency, indicating acceptance of multiple mates. Synthetic HP-I injected into wild-type, but not NPYLR1 mutant, virgins reduced successful matings. Asian tiger mosquito (Ae. albopictus) HP-I peptides potently activated Ae. aegypti NPYLR1. Invasive Ae. albopictus males are known to copulate with and effectively sterilize Ae. aegypti females by causing them to reject future mates [9]. Cross-species transfer of sperm and active seminal fluid proteins including HP-I may contribute to this phenomenon. This signaling system promotes rapid paternity enforcement within Ae. aegypti but may promote local extinction in areas where they compete with Ae. albopictus.