Odour of domestic dogs infected with Leishmania infantum is attractive to female but not male sand flies: Evidence for parasite manipulation

Author summary Visceral leishmaniasis (VL) is a disease caused by the Protist parasite Leishmania infantum. In Brazil and other South and Central American countries, the parasite is transmitted by the bite of infected female Lutzomyia longipalpis sand flies. The disease leads to thousands of human deaths every year. Domestic dogs are the reservoir of infection therefore understanding how the infection affects the attractiveness of dogs to the insect vector is important in understanding the epidemiology of the disease. Golden Hamsters infected with Le. infantum are more attractive than uninfected hamsters to Lu. longipalpis however, it is not known if the attractiveness of infected dogs is similarly altered. In this study we showed that the odour of infected dogs is significantly more attractive to female sand flies, that can transmit the pathogen, than it is to male sand flies which can not. This clear-cut difference in attraction of female and males suggests that the females are preferentially attracted by parasite infected hosts and may lead to enhanced infection and transmission opportunities for the parasite. Globally visceral leishmaniasis (VL) causes thousands of human deaths every year. In South America, the etiologic agent, Leishmania infantum, is transmitted from an infected canine reservoir to human hosts by the bite of the sand fly vector; predominantly Lutzomyia longipalpis. Previous evidence from model rodent systems have suggested that the odour of infected hosts is altered by the parasite making them more attractive to the vector leading to an increased biting rate and improved transmission prospects for the pathogen. However, there has been no assessment of the effect of Le infantum infection on the attractiveness of dogs, which are the natural reservoirs for human infection. Hair collected from infected and uninfected dogs residing in a VL endemic city in Brazil was entrained to collect the volatile chemical odours present in the headspace. Female and male Lu. longipalpis sand flies were offered a choice of odour entrained from infected and uninfected dogs in a series of behavioural experiments. Odour of uninfected dogs was equally attractive to male or female Lu. longipalpis when compared to a solvent control. Female Lu. longipalpis were significantly more attracted to infected dog odour than uninfected dog odour in all 15 experimental replicates (average 45.7 +/- 0.87 females attracted to infected odour; 23.9 +/- 0.82 to uninfected odour; paired T-test, P = 0.000). Male Lu. longipalpis did not significantly prefer either infected or uninfected odour (average 36.1 +/- 0.4 males to infected odour; 35.7 +/- 0.6 to uninfected odour; paired T-test, P = 0.722). A significantly greater proportion of females chose the infected dog odour compared to the males (paired T-test, P = 0.000). The results showed that the odour of dogs infected with Le. infantum was significantly more attractive to blood-seeking female sand flies than it was to male sand flies. This is strong evidence for parasite manipulation of the host odour in a natural transmission system and indicates that infected dogs may have a disproportionate significance in maintaining infection in the canine and human population.

Automated summary

Visceral leishmaniasis caused by the Protist parasite Leishmania infantum leads to thousands of human deaths annually in Brazil and other South and Central American countries. Research has shown that the odour of dogs infected with Le. infantum is significantly more attractive to female sand flies, potentially enhancing infection and transmission opportunities for the parasite. This suggests infected dogs may play a disproportionate role in maintaining infection in both canine and human populations.