Abstract

BackgroundPhlebotomine sand flies (Diptera, Nematocera) are important vectors of several pathogens, including Leishmania parasites, causing serious diseases of humans and dogs. Despite their importance as disease vectors, most aspects of sand fly biology remain unknown including the molecular basis of their reproduction and sex determination, aspects also relevant for the development of novel vector control strategies.ResultsUsing comparative genomics/transcriptomics data mining and transcriptional profiling, we identified the sex determining genes in phlebotomine sand flies and proposed the first model for the sex determination cascade of these insects. For all the genes identified, we produced manually curated gene models, developmental gene expression profile and performed evolutionary molecular analysis. We identified and characterized, for the first time in a Nematocera species, the transformer (tra) homolog which exhibits both conserved and novel features. The analysis of the tra locus in sand flies and its expression pattern suggest that this gene is able to autoregulate its own splicing, as observed in the fruit fly Ceratitis capitata and several other insect species.ConclusionsOur results permit to fill the gap about sex determination in sand flies, contribute to a better understanding of this developmental pathway in Nematocera and open the way for the identification of sex determining orthologs in other species of this important Diptera sub-order. Furthermore, the sex determination genes identified in our work also provide the opportunity of future biotechnological applications to control natural population of sand flies, reducing their impact on public health.

Highlights

  • Phlebotomine sand flies (Diptera, Nematocera) are important vectors of several pathogens, including Leishmania parasites, causing serious diseases of humans and dogs

  • Identification of PpeSxl, Ppetra, Ppetra-2, Ppedsx, and Ppefru sex determining genes in the sand fly Phlebotomus perniciosus In the Old World, the sand fly Phlebotomus perniciosus (Diptera, Nematocera) is the main vector of Leishmania infantum (Kinetoplastida: Trypanosomatidae), the parasitic protozoan that causes visceral and cutaneous leishmaniasis in humans and canine reservoir host, as well as of various known and emerging arboviruses considered relevant from an European public health perspective (Toscana Virus, Naples Virus, Sicilian Virus) [35]

  • By querying PpeTRA against the genomes and transcriptomes of the Phlebotominae species, we identified the tra ortholog in P. papatasi (Ppatra), P. bergeroti (Pbetra) and P. duboscqi (Pdutra); this approach could not identify any tra ortholog in the genomes/transcriptomes of the three New World sand fly species (L. longipalpis, L. (Nyssomyia) umbratilis and L. (Nyssomyia) neivai)

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Summary

Introduction

Phlebotomine sand flies (Diptera, Nematocera) are important vectors of several pathogens, including Leishmania parasites, causing serious diseases of humans and dogs. Sex determination is the process by which early embryos of metazoan species with sexual reproduction operate a binary decision between two conditions: male or female development. This key decision results in individuals that can be identified as males, females, or in some cases hermaphrodites and, in species with a genetic sex determination system, underlies genomic differences between sexes. Drosophila melanogaster (Diptera, Drosophilidae) is the model species where sex determination is known at the higher level of molecular resolution (Fig. 1) In this species, sex determination is controlled by five main genes, Sex-lethal (Sxl), transformer (tra), transformer-2 (tra-2), doublesex (dsx) and fruitless (fru), hierarchically organized in a regulative cascade: Sxl - > tra + tra-2 - > dsx, fru. This cascade is Petrella et al BMC Genomics (2019) 20:522

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