Molecular Signatures of Sexual Communication in the Phlebotomine Sand Flies

Authors

Paul V. Hickner, University of Kentucky
Nataliya Timoshevskaya, University of KentuckyFollow
Ronald J. Nowling, Milwaukee School of Engineering
Frédéric Labbé, University of Notre Dame
Andrew D. Nguyen, University of Notre Dame
Mary Ann McDowell, University of Notre Dame
Carolina N. Spiegel, Fluminense Federal University, Brazil
Zainulabeuddin Syed, University of KentuckyFollow

Abstract

Phlebotomine sand flies employ an elaborate system of pheromone communication wherein males produce pheromones that attract other males to leks (thus acting as an aggregation pheromone) and females to the lekking males (sex pheromone). In addition, the type of pheromone produced varies among populations. Despite the numerous studies on sand fly chemical communication, little is known of their chemosensory genome. Chemoreceptors interact with chemicals in an organism’s environment to elicit essential behaviors such as the identification of suitable mates and food sources. Thus, they play important roles during adaptation and speciation. Major chemoreceptor gene families, odorant receptors (ORs), gustatory receptors (GRs) and ionotropic receptors (IRs) together detect and discriminate the chemical landscape. Here, we annotated the chemoreceptor repertoire in the genomes of Lutzomyia longipalpis and Phlebotomus papatasi, major phlebotomine vectors in the New World and Old World, respectively. Comparison with other sequenced Diptera revealed a large and unique expansion where over 80% of the ~140 ORs belong to a single, taxonomically restricted clade. We next conducted a comprehensive analysis of the chemoreceptors in 63 L. longipalpis individuals from four different locations in Brazil representing allopatric and sympatric populations and three sex-aggregation pheromone types (chemotypes). Population structure based on single nucleotide polymorphisms (SNPs) and gene copy number in the chemoreceptors corresponded with their putative chemotypes, and corroborate previous studies that identified multiple populations. Our work provides genomic insights into the underlying behavioral evolution of sexual communication in the L. longipalpis species complex in Brazil, and highlights the importance of accounting for the ongoing speciation in central and South American Lutzomyia that could have important implications for vectorial capacity.

Document Type

Article

Publication Date

12-28-2020

Notes/Citation Information

Published in PLOS Neglected Tropical Diseases, v. 14, issue 12, e0008967.

© 2020 Hickner et al.

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Digital Object Identifier (DOI)

https://doi.org/10.1371/journal.pntd.0008967

Funding Information

This research work was supported by funding from National Institute of Food and Agriculture, US Department of Agriculture (under HATCH Project 2353077000) to Z.S.

Related Content

The data underlying the results presented in the study are all uploaded along with this m/s. and also available on https://doi.org/10.1101/2020.08.11.247155.

The preprint of this article is available from bioRxiv.

Repository Citation

Hickner, Paul V.; Timoshevskaya, Nataliya; Nowling, Ronald J.; Labbé, Frédéric; Nguyen, Andrew D.; McDowell, Mary Ann; Spiegel, Carolina N.; and Syed, Zainulabeuddin, "Molecular Signatures of Sexual Communication in the Phlebotomine Sand Flies" (2020). Biology Faculty Publications. 204.
https://uknowledge.uky.edu/biology_facpub/204