Enhanced attraction of sand fly vectors of Leishmania infantum to dogs infected with zoonotic visceral leishmaniasis

Author summary Zoonotic visceral leishmaniasis is a neglected tropical disease caused by the parasite Leishmania infantum. In the Western Mediterranean basin, Phlebotomus perniciosus and Phlebotomus perfiliewi are the main vectors of L. infantum, and dogs are the main reservoir host of the parasite. In Northern Africa, ZVL affect mostly children less than 5 years. Understanding the chemical ecology governing the relationships between the vector, the parasite and the reservoir host is of major epidemiological importance. Previous studies based on rodent models have shown that the infection with L. infantum enhanced the attractiveness towards Lutzomyia longipaplis, the main vector of ZVL in the Americas. In this study, we reported for the first time that infected dogs are highly attractive to both male and female P. perniciosus under laboratory and filed conditions compared to uninfected dogs. Similar patterns were observed with wild populations of P. perfiliewi. Our results provided strong evidence that the parasite manipulate the reservoir hosts to enhance its transmission success by the vector. Background The sand fly Phlebotomus perniciosus is the main vector of Leishmania infantum, etiological agent of zoonotic visceral leishmaniasis in the Western Mediterranean basin. Dogs are the main reservoir host of this disease. The main objective of this study was to determine, under both laboratory and field conditions, if dogs infected with L. infantum, were more attractive to female P. perniciosus than uninfected dogs. Methodology/Principal findings We carried out a series of host choice experiments and found that infected dogs were significantly more attractive to P. perniciosus than uninfected dogs in the laboratory as well as in the field. Significantly more P. perniciosus fed on infected dogs than on uninfected dogs. However, the fecundity of P. perniciosus fed on infected dogs was adversely impacted compared to uninfected dogs by lowering the number of laid eggs. Phlebotomus perfiliewi, the second most abundant sand fly species in the field site and a competent vector of L. infantum had similar trends of attractivity as P. perniciosus toward infected dogs under field conditions. Conclusions The results strongly suggest that L. infantum causes physiological changes in the reservoir host which lead to the host becoming more attractive to both male and female P. perniciosus. These changes are likely to improve the chance of successful transmission because of increased contact with infected hosts and therefore, infected dogs should be particularly targeted in the control of zoonotic visceral leishmaniasis in North Africa.