Odour of domestic dogs infected withLeishmania infantumis attractive to female but not male sand flies: evidence for parasite manipulation
Authors: Staniek Monica E. , Hamilton James G.C. 
Published: November 2020

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 blood-feeding activity 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, the effect ofLe. infantuminfection on the attractiveness of naturally infected dogs which are integral to human infection, has not been assessed.

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 maleLu. longipalpissand flies were offered a choice of infected or uninfected odour in a series of behavioural experiments. Control experiments established that female and maleLu. longipalpiswere equally attracted to uninfected dog odour, femaleLu. longipalpiswere 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). MaleLu. longipalpisdid 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 show that dogs infected withLe. infantumare significantly more attractive to blood-feeding female than 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 canine and human infection.

Author Summary

Visceral leishmaniasis (VL) is a disease caused by the Protist parasiteLeishmania infantum. In Brazil and other South and Central American countries, the parasite is transmitted by the blood-feeding activity of infected femaleLutzomyia longipalpissand flies. The disease leads to thousands of human cases and deaths every year. Domestic dogs are the reservoir of infection for humans therefore understanding the effect of infection on dogs is important in developing an understanding of the epidemiology of the disease. Although previous studies on rodent models ofLe. infantuminfection have shown that infected Golden Hamsters are more attractive toLu. longipalpisthe attractiveness of naturally infected dogs to the insect vector has not been previously been investigated. In this study we showed that the odour of infected dogs is significantly more attractive to female sand flies which can transmit the pathogen than to male sand flies which do 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.