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Open Access Highly Accessed Research article

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

David C Rinker1, Xiaofan Zhou2, Ronald Jason Pitts2, The AGC Consortium, Antonis Rokas12 and Laurence J Zwiebel123*

Author Affiliations

1 Center for Human Genetics Research, Vanderbilt University Medical Center, Nashville, Tennessee, USA

2 Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee, USA

3 Department of Pharmacology, Vanderbilt Brain Institute, Program in Developmental Biology and Institutes of Chemical Biology and Global Health, Vanderbilt University Medical Center, Nashville, Tennessee, USA

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BMC Genomics 2013, 14:749  doi:10.1186/1471-2164-14-749

Published: 1 November 2013

Abstract

Background

Two 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.

Results

To 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.

Conclusion

This 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.

Keywords:
Anopheles; Mosquito; Antenna; Transcriptome; Olfaction; Malaria; Host-seeking; Odorant receptor; Molecular evolution; RNAseq