The Lutzomyia longipalpis complex: a brief natural history of aggregation-sex pheromone communication

Abstract

In this paper we review the natural history of pheromone communication and the current diversity of aggregation-sex pheromones in the sand fly Lutzomyia longipalpis. This species complex is the main vector of Leishmania infantum, the agent of visceral leishmaniasis in the Americas. The identification of variation in pheromone chemotypes combined with molecular and sound analyses have all contributed to our understanding of the extent of divergence among cryptic members of this complex. The importance of chemical signals as pre-mating barriers and drivers of speciation is discussed. Moreover, the importance of aggregation-sex pheromones as sexually selected signals is highlighted with evidence from the literature suggesting their potential role in species and mate recognition as well as mate assessment. The distinct evolutionary forces possibly involved are briefly reviewed and discussed in the context of this intriguing insect.

Keywords: Aggregation pheromone; Evolution; Lutzomyia longipalpis; Sand flies; Sex pheromone; Species complex.

Fig. 1

Morphological variation in the abdominal tergal pale spot patterns in males of Lutzomyia. longipalpis. a Single pale spot on the fourth abdominal tergite (phenotype named one spot phenotype, 1S). b Two pale spots on the third and fourth abdominal tergites (phenotype named two spot phenotypes, 2S). c Intermediate forms with one whole spot on the fourth abdominal tergite and a half spot on the third tergite (phenotype named intermediate form phenotype, INS). Yellow arrows indicate the pale spot

Fig. 2

Geographical locations of the different Lutzomyia longipalpis aggregation-sex pheromone chemotypes in Americas. This map was created using Qgis Pisa version 2.10.1, coordinate system: SAD 69 and database: ZEE/AC, 2006

Fig. 3

Lutzomyia longipalpis aggregation-sex pheromone communication system. a The aggregation-sex pheromones is produced by males in glands located in the pale spots in the third and/or fourth abdominal tergites. b Scanning Electron microscopy (SEM) of the cuticular papules with a central pore disseminating structures located in pale spots. The secretion is produced by pheromone gland cells grouped beneath the cuticle showed in light microscopy (LM). Details of two large columnar secretory cells can be observed in this transmission electron microscopy (TEM). Each gland cell is connected to the exterior via a small cuticular duct and present two distinct parts: a basal region with vacuoles containing lipids (L) and an apical region with an end apparatus and a small reservoir (SR). c The main component of the pheromone differs among populations and represent different chemotypes. d The pheromone is perceived by the paired ascoid sensilla present in antennae of both male and female showed in SEM. The pheromone functions for male as an aggregation pheromone and as sex pheromone by female

Fig. 4

Phylogenetic tree of the family Psychodidae including the different subtribes of the subfamily Phlebotominae indicating the presence (•) or the absence (o) of papule in the abdominal tergites of different groups as well as the lack of studies (x). Modified from Galati et al. [123]