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      Evolution of mosquito preference for humans linked to an odorant receptor

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          Abstract

          Female mosquitoes are major vectors of human disease and the most dangerous are those that preferentially bite humans. A ‘domestic’ form of the mosquito Aedes aegypti has evolved to specialize in biting humans and is the major worldwide vector of dengue, yellow fever, and Chikungunya viruses. The domestic form coexists with an ancestral, animal-biting ‘forest’ form along the coast of Kenya. We collected the two forms, established laboratory colonies, and document striking divergence in preference for human versus animal odour. We further show that the evolution of preference for human odour in domestic mosquitoes is tightly linked to increases in the expression and ligand-sensitivity of the odorant receptor AaegOr4, which we found recognises a compound present at high levels in human odour. Our results provide a rare example of a gene contributing to behavioural evolution and provide insight into how disease-vectoring mosquitoes came to specialise on humans.

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          Most cited references 69

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          An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases.

          Germ-line transformation via transposable elements is a powerful tool to study gene function in Drosophila melanogaster. However, some inherent characteristics of transposon-mediated transgenesis limit its use for transgene analysis. Here, we circumvent these limitations by optimizing a phiC31-based integration system. We generated a collection of lines with precisely mapped attP sites that allow the insertion of transgenes into many different predetermined intergenic locations throughout the fly genome. By using regulatory elements of the nanos and vasa genes, we established endogenous sources of the phiC31 integrase, eliminating the difficulties of coinjecting integrase mRNA and raising the transformation efficiency. Moreover, to discriminate between specific and rare nonspecific integration events, a white gene-based reconstitution system was generated that enables visual selection for precise attP targeting. Finally, we demonstrate that our chromosomal attP sites can be modified in situ, extending their scope while retaining their properties as landing sites. The efficiency, ease-of-use, and versatility obtained here with the phiC31-based integration system represents an important advance in transgenesis and opens up the possibility of systematic, high-throughput screening of large cDNA sets and regulatory elements.
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            Streaming fragment assignment for real-time analysis of sequencing experiments

            We present eXpress, a software package for highly efficient probabilistic assignment of ambiguously mapping sequenced fragments. eXpress uses a streaming algorithm with linear run time and constant memory use. It can determine abundances of sequenced molecules in real time, and can be applied to ChIP-seq, metagenomics and other large-scale sequencing data. We demonstrate its use on RNA-seq data, showing greater efficiency than other quantification methods.
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              The molecular basis of odor coding in the Drosophila antenna.

              We have undertaken a functional analysis of the odorant receptor repertoire in the Drosophila antenna. Each receptor was expressed in a mutant olfactory receptor neuron (ORN) used as a "decoder," and the odor response spectrum conferred by the receptor was determined in vivo by electrophysiological recordings. The spectra of these receptors were then matched to those of defined ORNs to establish a receptor-to-neuron map. In addition to the odor response spectrum, the receptors dictate the signaling mode, i.e., excitation or inhibition, and the response dynamics of the neuron. An individual receptor can mediate both excitatory and inhibitory responses to different odorants in the same cell, suggesting a model of odorant receptor transduction. Receptors vary widely in their breadth of tuning, and odorants vary widely in the number of receptors they activate. Together, these properties provide a molecular basis for odor coding by the receptor repertoire of an olfactory organ.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                4 December 2014
                13 November 2014
                13 May 2015
                : 515
                : 7526
                : 222-227
                Affiliations
                [1 ]Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, NY 10065 USA
                [2 ]Howard Hughes Medical Institute
                [3 ]Unit of Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural Sciences, Box 102, Sundsvägen 14, 230 53, Alnarp, Sweden
                [4 ]Center for Virus Research, Kenya Medical Research Institute, P.O. Box 54840 - 00200, Off Mbagathi Way, Nairobi, Kenya
                Author notes
                Correspondence and requests for materials should be addressed to L.B.V. ( Leslie.Vosshall@ 123456rockefeller.edu )
                [†]

                Present address: Princeton Neuroscience Institute and Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544 USA (C.S.M.); Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138 USA (F.B.); Plant Protection Research Institute, Agricultural Research Council, Private Bag X134, Queenswood 0121, South Africa (A.B.O.); Harvard College, Harvard University, Cambridge, MA 02138 (S.A.S.).

                Article
                NIHMS635307
                10.1038/nature13964
                4286346
                25391959

                Reprints and permissions information is available at www.nature.com/reprints.

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