Arsenophonus: A Double-Edged Sword of Aphid Defense against Parasitoids

SIMPLE SUMMARY: Endosymbiont interactions with hosts have significant effects on pests and beneficial species. A form of endosymbiosis is known as a mutually beneficial association. In this context, specific facultative endosymbiotic bacteria, such as Arsenophonus, play a defensive role by safeguarding aphids against parasitoids. This study on black cowpea aphids (BCAs) revealed that Arsenophonus does not prevent parasitism by two species of Aphidiinae wasps, Binodoxys angelicae and Lysiphlebus fabarum. However, the maturation and emergence of adult B. angelicae wasps were delayed when BCAs were parasitized. This delay limits the effectiveness of B. angelicae, reducing the number of emerged adult wasps and allowing other members of the BCA colony to survive. The role of Arsenophonus in the interaction between A. craccivora and its parasitoids is multifaceted and acts as a double-edged sword. ABSTRACT: It is widely accepted that endosymbiont interactions with their hosts have significant effects on the fitness of both pests and beneficial species. A particular type of endosymbiosis is that of beneficial associations. Facultative endosymbiotic bacteria are associated with elements that provide aphids with protection from parasitoids. Arsenophonus (Enterobacterales: Morganellaceae) is one such endosymbiont bacterium, with infections being most commonly found among the Hemiptera species. Here, black cowpea aphids (BCAs), Aphis craccivora Koch (Hemiptera: Aphididae), naturally infected with Arsenophonus, were evaluated to determine the defensive role of this bacterium in BCAs against two parasitoid wasp species, Binodoxys angelicae and Lysiphlebus fabarum (both in Braconidae: Aphidiinae). Individuals of the black cowpea aphids infected with Arsenophonus were treated with a blend of ampicillin, cefotaxime, and gentamicin (Arsenophonus-reduced infection, AR) and subsequently subjected to parasitism assays. The results showed that the presence of Arsenophonus does not prevent BCAs from being parasitized by either B. angelicae or L. fabarum. Nonetheless, in BCA colonies parasitized by B. angelicae, the endosymbiont delayed both the larval maturation period and the emergence of the adult parasitoid wasps. In brief, Arsenophonus indirectly limits the effectiveness of B. angelicae parasitism by decreasing the number of emerged adult wasps. Therefore, other members of the BCA colony can survive. Arsenophonus acts as a double-edged sword, capturing the complex dynamic between A. craccivora and its parasitoids.