Research Article: Multi-modal Analysis of Courtship Behaviour in the Old World Leishmaniasis Vector Phlebotomus argentipes

Date Published: December 4, 2014

Publisher: Public Library of Science

Author(s): Daniel P. Bray, Khatijah Yaman, Beryl A. Underhilll, Fraser Mitchell, Victoria Carter, James G. C. Hamilton, Paulo Filemon Pimenta.

Abstract: BackgroundThe sand fly Phlebotomus argentipes is arguably the most important vector of leishmaniasis worldwide. As there is no vaccine against the parasites that cause leishmaniasis, disease prevention focuses on control of the insect vector. Understanding reproductive behaviour will be essential to controlling populations of P. argentipes, and developing new strategies for reducing leishmaniasis transmission. Through statistical analysis of male-female interactions, this study provides a detailed description of P. argentipes courtship, and behaviours critical to mating success are highlighted. The potential for a role of cuticular hydrocarbons in P. argentipes courtship is also investigated, by comparing chemicals extracted from the surface of male and female flies.Principal FindingsP. argentipes courtship shared many similarities with that of both Phlebotomus papatasi and the New World leishmaniasis vector Lutzomyia longipalpis. Male wing-flapping while approaching the female during courtship predicted mating success, and touching between males and females was a common and frequent occurrence. Both sexes were able to reject a potential partner. Significant differences were found in the profile of chemicals extracted from the surface of males and females. Results of GC analysis indicate that female extracts contained a number of peaks with relatively short retention times not present in males. Extracts from males had higher peaks for chemicals with relatively long retention times.ConclusionsThe importance of male approach flapping suggests that production of audio signals through wing beating, or dispersal of sex pheromones, are important to mating in this species. Frequent touching as a means of communication, and the differences in the chemical profiles extracted from males and females, may also indicate a role for cuticular hydrocarbons in P. argentipes courtship. Comparing characteristics of successful and unsuccessful mates could aid in identifying the modality of signals involved in P. argentipes courtship, and their potential for use in developing new strategies for vector control.

Partial Text: Visceral leishmaniasis (VL) is a debilitating disease estimated to cause 20,000–40,000 deaths worldwide each year [1]. The Indian subcontinent is one of the areas most affected by VL, with over 140,000 cases per year estimated to occur in India alone [1]. The etiologic agent in this region is the protozoan parasite Leishmania donovani (Kinetoplastida: Trypanosomatidae), with the sand fly Phlebotomus argentipes (Diptera: Psychodidae) the proven or suspected vector in Bangladesh, India, Nepal and Sri Lanka [2]. As there is no vaccine against VL, and cost and drug resistance limit effectiveness of treatment in India [3], control of the sand fly vector remains a priority for reducing transmission [4]. To be successful these programmes require a thorough understanding of the behaviour of the insect vector [5], not least because many human activities can significantly alter sand fly behaviour and potential risk of transmission. Agricultural practices, for example, may lead to creation of new habitats for sand flies [6]. Insecticide spraying for control can lead to unintentional diversion of sand flies away from normal resting sites in animal houses, potentially increasing the biting risk to humans [7], [8].

Courtship behaviour in P. argentipes shared several similarities with both P. papatasi and the new world leishmaniasis vector L. longipalpis. The core progression of behaviours comprised the male wing-flapping while approaching the female, before touching her with the legs or antennae prior to attempting copulation. This builds on a previous description of the ‘courtship dance’ of P. argentipes, described as involving males hopping, swinging the terminalia and wing-flapping [14]. Both female and male P. argentipes engaged in wing-flapping behaviour during courtship, with male approach flapping a significant predictor of copulation success. While integral to P. argentipes courtship, the function of wing-flapping in this species is currently unknown. In L. longipalpis, male wing-flapping has been hypothesised to aid in dispersal of attractive sex pheromones released from abdominal tergites [15], [31]. These pheromones attract female L. longipalpis to aggregations of males formed on or above host animals [32]. Male P. argentipes also form mating aggregations on cows or other animals, and perform wing-flapping behaviours prior to the arrival of females [10], [13]. It is therefore possible that male P. argentipes also release an attractive sex pheromone to aid females in locating these aggregations. Male P. argentipes also performed abdomen bending during courtship, a behaviour previously reported from Phlebotomus papatasi[19], Phlebotomus longipes[33]Phlebotomus martini[34] and Lutzomyia vexator[35]. This could conceivably also function in pheromone release from abdominal tergites, the site of production of pheromones in L. longipalpis, [36]. There is behavioural evidence of chemically mediated attraction of females to males in both P. argentipes and P. papatasi[13], [20]. However, to date no sex pheromone, or likely sex pheromone-producing structure, has been identified in any of the abdomen-bending sand flies [37], and L. longipalpis (which does produce pheromones) does not perform this behaviour [16].



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