Antennal transcriptome profiles of anopheline mosquitoes reveal human host olfactory specialization in Anopheles gambiae.

David C Rinker,Xiaofan Zhou,Antonis Rokas,Ronald Jason Pitts,Laurence J Zwiebel

doi:10.1186/1471-2164-14-749

David C Rinker, Xiaofan Zhou + Show 3 more

Open Access

https://doi.org/10.1186/1471-2164-14-749

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Abstract

BackgroundTwo sibling members of the Anopheles gambiae species complex display notable differences in female blood meal preferences. An. gambiae s.s. has a well-documented preference for feeding upon human hosts, whereas An. quadriannulatus feeds on vertebrate/mammalian hosts, with only opportunistic feeding upon humans. Because mosquito host-seeking behaviors are largely driven by the sensory modality of olfaction, we hypothesized that hallmarks of these divergent host seeking phenotypes will be in evidence within the transcriptome profiles of the antennae, the mosquito’s principal chemosensory appendage.ResultsTo test this hypothesis, we have sequenced antennal mRNA of non-bloodfed females from each species and observed a number of distinct quantitative and qualitative differences in their chemosensory gene repertoires. In both species, these gene families show higher rates of sequence polymorphisms than the overall rates in their respective transcriptomes, with potentially important divergences between the two species. Moreover, quantitative differences in odorant receptor transcript abundances have been used to model potential distinctions in volatile odor receptivity between the two sibling species of anophelines.ConclusionThis analysis suggests that the anthropophagic behavior of An. gambiae s.s. reflects the differential distribution of olfactory receptors in the antenna, likely resulting from a co-option and refinement of molecular components common to both species. This study improves our understanding of the molecular evolution of chemoreceptors in closely related anophelines and suggests possible mechanisms that underlie the behavioral distinctions in host seeking that, in part, account for the differential vectorial capacity of these mosquitoes.

Highlights

Two sibling members of the Anopheles gambiae species complex display notable differences in female blood meal preferences
The sole non-vector member of this species complex, An. quadriannulatus is competent for P. falciparum infection [3,4] and molecular evidence suggests that the karyotype for this species derived directly from that of the main vector An. gambiae s.s. [5]
Based upon our phylogenetic analysis (Additional file 1: Dataset S1), chemosensory genes can be classified into 253 orthologous groups (OGs), including 75 OGs of ORs, 61 OGs of GRs, 43 OGs of IRs, and 74 OGs of OBPs (Figure 1), where each OG represents a single gene in the most recent common ancestor (MRCA) of the two species

Summary

Introduction

Two sibling members of the Anopheles gambiae species complex display notable differences in female blood meal preferences. The sole non-vector member of this species complex, An. quadriannulatus is competent for P. falciparum infection [3,4] and molecular evidence suggests that the karyotype for this species derived directly from that of the main vector An. gambiae s.s. An. quadriannulatus is still considered to be a non-vector because its zoophagic [6,7], or at least highly opportunistic [8], host-preference effectively disrupts the human-to-human cycle of transmission required by P. falciparum. There is reason to suspect that species-specific, phenotypic variation between olfactory mediated behaviors may be informed by examining variation displayed by chemosensory genes, in terms of both molecular sequence and transcript abundance [27,28,29,30]

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