title: A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health.
abstract: Honey bee colony losses are triggered by interacting stress factors consistently associated with high loads of parasites and/or pathogens. A wealth of biotic and abiotic stressors are involved in the induction of this complex multifactorial syndrome, with the parasitic mite Varroa destructor and the associated deformed wing virus (DWV) apparently playing key roles. The mechanistic basis underpinning this association and the evolutionary implications remain largely obscure. Here we narrow this research gap by demonstrating that DWV, vectored by the Varroa mite, adversely affects humoral and cellular immune responses by interfering with NF-κB signaling. This immunosuppressive effect of the viral pathogen enhances reproduction of the parasitic mite. Our experimental data uncover an unrecognized mutualistic symbiosis between Varroa and DWV, which perpetuates a loop of reciprocal stimulation with escalating negative effects on honey bee immunity and health. These results largely account for the remarkable importance of this mite-virus interaction in the induction of honey bee colony losses. The discovery of this mutualistic association and the elucidation of the underlying regulatory mechanisms sets the stage for a more insightful analysis of how synergistic stress factors contribute to colony collapse, and for the development of new strategies to alleviate this problem.
authors.affiliation: Dipartimento di Agraria, Laboratorio di Entomologia "E. Tremblay," Università degli Studi di Napoli "Federico II," 80055 Portici (NA), Italy;
authors.forename: Gennaro
authors.initials: G
authors.lastname: Di Prisco
authors.affiliation: Dipartimento di Scienze AgroAlimentari Ambientali e Animali, Università degli Studi di Udine, 33100 Udine, Italy.
authors.forename: Desiderato
authors.initials: D
authors.lastname: Annoscia
authors.affiliation: Dipartimento di Agraria, Laboratorio di Entomologia "E. Tremblay," Università degli Studi di Napoli "Federico II," 80055 Portici (NA), Italy;
authors.forename: Marina
authors.initials: M
authors.lastname: Margiotta
authors.affiliation: Dipartimento di Agraria, Laboratorio di Entomologia "E. Tremblay," Università degli Studi di Napoli "Federico II," 80055 Portici (NA), Italy;
authors.forename: Rosalba
authors.initials: R
authors.lastname: Ferrara
authors.affiliation: Dipartimento di Agraria, Laboratorio di Entomologia "E. Tremblay," Università degli Studi di Napoli "Federico II," 80055 Portici (NA), Italy;
authors.forename: Paola
authors.initials: P
authors.lastname: Varricchio
authors.affiliation: Dipartimento di Scienze AgroAlimentari Ambientali e Animali, Università degli Studi di Udine, 33100 Udine, Italy.
authors.forename: Virginia
authors.initials: V
authors.lastname: Zanni
authors.affiliation: Dipartimento di Agraria, Laboratorio di Entomologia "E. Tremblay," Università degli Studi di Napoli "Federico II," 80055 Portici (NA), Italy;
authors.forename: Emilio
authors.initials: E
authors.lastname: Caprio
authors.affiliation: Dipartimento di Scienze AgroAlimentari Ambientali e Animali, Università degli Studi di Udine, 33100 Udine, Italy francesco.nazzi@uniud.it f.pennacchio@unina.it.
authors.forename: Francesco
authors.initials: F
authors.lastname: Nazzi
authors.affiliation: Dipartimento di Agraria, Laboratorio di Entomologia "E. Tremblay," Università degli Studi di Napoli "Federico II," 80055 Portici (NA), Italy; francesco.nazzi@uniud.it f.pennacchio@unina.it.
authors.forename: Francesco
authors.initials: F
authors.lastname: Pennacchio
mesh_terms: D000818:Animals; D001516:Bees / Q000276:immunology* / Q000469:parasitology / Q000821:virology; D008925:Mites / Q000502:physiology*; D013559:Symbiosis
keywords: Apis mellifera; Varroa destructor; deformed wing virus; honeybee colony losses; mutualistic symbiosis