Molecular signatures of sexual communication in the phlebotomine sand flies

Paul V. Hickner, Nataliya Timoshevskaya, Ronald J. Nowling, Frédéric Labbé, Andrew D. Nguyen, Mary Ann McDowell, Carolina N. Spiegel, Zainulabeuddin Syed

Research output: Contribution to journalArticlepeer-review

2 Scopus citations

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.

Original languageEnglish
Article numbere0008967
Pages (from-to)1-18
Number of pages18
JournalPLoS Neglected Tropical Diseases
Volume14
Issue number12
DOIs
StatePublished - Dec 2020

Bibliographical note

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. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.” We thank Hugh M. Robertson (University of Illinois, Urbana-Champaign, IL) for his guidance on annotating the chemoreceptors, and David C. Rinker (Vanderbilt University, TN) for his recommendations for calculating gene copy number and VST. We would also like to thank Cleilton Sampaio de Farias (Instituto Federal do Acre, Brazil) for the map construction, and Felipe Vigoder (Universidade Federal do Rio de Janeiro, Brazil) for sharing the original recordings of the copulation songs displayed in Fig 2. We acknowledge the late Alexandre Peixoto, whose previous work inspired this research and who participated in the sampling strategy prior to his untimely death. L. longipalpis genome data were generated by Baylor College of Medicine Human Genome Sequencing Center in collaboration with Washington University in Saint Louis as part of the sand fly NHGRI project.

Publisher Copyright:
© 2020 Hickner et al.

ASJC Scopus subject areas

  • Public Health, Environmental and Occupational Health
  • Infectious Diseases

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