Limits...
Evolution of mosquito preference for humans linked to an odorant receptor.

McBride CS, Baier F, Omondi AB, Spitzer SA, Lutomiah J, Sang R, Ignell R, Vosshall LB - Nature (2014)

Bottom Line: A 'domestic' form of the mosquito Aedes aegypti has evolved to specialize in biting humans and is the main worldwide vector of dengue, yellow fever, and chikungunya viruses.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 recognizes 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 specialize on humans.

View Article: PubMed Central - PubMed

Affiliation: 1] Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, New York 10065, USA [2] Howard Hughes Medical Institute, 1230 York Avenue, New York, New York 10065, USA.

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 main worldwide vector of dengue, yellow fever, and chikungunya viruses. The domestic form coexists with an ancestral, 'forest' form that prefers to bite non-human animals and is found along the coast of Kenya. We collected the two forms, established laboratory colonies, and document striking divergence in preference for human versus non-human 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 recognizes 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 specialize on humans.

Show MeSH

Related in: MedlinePlus

Or4 responds to sulcatone, a human odoranta, Schematic of gas chromatography-coupled single sensillum recording (GC-SSR). FID = flame ionization detector. b, Sample GC-SSR output, with SSR trace at the top showing large-amplitude spikes (black) from the Or4-expressing neuron and FID output showing elution times of human volatiles (middle trace) and sulcatone (bottom trace). c, Magnified sections of sample total ion chromatogram traces from GC-mass spectrometry (GC-MS) analysis of human (top) and guinea pig (bottom) sleeves. d, Summary of sulcatone and benzaldehyde emission from unworn, human, and guinea pig sleeves (n = 4 - 5 replicates per group; violin plots clipped at the range of data; median: black dot; 1st and 3rd quartile: bounds of black bar). Violins labelled with different letters are statistically different (pairwise Wilcoxon tests with Bonferroni correction; ns = not significant). e, Summary of sulcatone and benzaldehyde levels in human and animal odour collections (n = 1 collection from 1 - 20 individuals per species).
© Copyright Policy - permissions-link
Related In: Results  -  Collection


getmorefigures.php?uid=PMC4286346&req=5

Figure 4: Or4 responds to sulcatone, a human odoranta, Schematic of gas chromatography-coupled single sensillum recording (GC-SSR). FID = flame ionization detector. b, Sample GC-SSR output, with SSR trace at the top showing large-amplitude spikes (black) from the Or4-expressing neuron and FID output showing elution times of human volatiles (middle trace) and sulcatone (bottom trace). c, Magnified sections of sample total ion chromatogram traces from GC-mass spectrometry (GC-MS) analysis of human (top) and guinea pig (bottom) sleeves. d, Summary of sulcatone and benzaldehyde emission from unworn, human, and guinea pig sleeves (n = 4 - 5 replicates per group; violin plots clipped at the range of data; median: black dot; 1st and 3rd quartile: bounds of black bar). Violins labelled with different letters are statistically different (pairwise Wilcoxon tests with Bonferroni correction; ns = not significant). e, Summary of sulcatone and benzaldehyde levels in human and animal odour collections (n = 1 collection from 1 - 20 individuals per species).

Mentions: An olfactory receptor could modulate host preference by mediating attraction or repulsion to specific host odours, so we asked whether Or4 is activated by a component of human or guinea pig odour. We expressed the genome reference allele of Or4 heterologously in a Drosophila olfactory neuron lacking a ligand-selective OR26, and tested responses to fractionated host odour from guinea pigs and humans (Fig. 4a). Or4 did not respond to any fraction of guinea pig odour (data not shown), but responded consistently to a fraction of human odour corresponding to 6-methyl-5-hepten-2-one, commonly called sulcatone (Fig. 4b).


Evolution of mosquito preference for humans linked to an odorant receptor.

McBride CS, Baier F, Omondi AB, Spitzer SA, Lutomiah J, Sang R, Ignell R, Vosshall LB - Nature (2014)

Or4 responds to sulcatone, a human odoranta, Schematic of gas chromatography-coupled single sensillum recording (GC-SSR). FID = flame ionization detector. b, Sample GC-SSR output, with SSR trace at the top showing large-amplitude spikes (black) from the Or4-expressing neuron and FID output showing elution times of human volatiles (middle trace) and sulcatone (bottom trace). c, Magnified sections of sample total ion chromatogram traces from GC-mass spectrometry (GC-MS) analysis of human (top) and guinea pig (bottom) sleeves. d, Summary of sulcatone and benzaldehyde emission from unworn, human, and guinea pig sleeves (n = 4 - 5 replicates per group; violin plots clipped at the range of data; median: black dot; 1st and 3rd quartile: bounds of black bar). Violins labelled with different letters are statistically different (pairwise Wilcoxon tests with Bonferroni correction; ns = not significant). e, Summary of sulcatone and benzaldehyde levels in human and animal odour collections (n = 1 collection from 1 - 20 individuals per species).
© Copyright Policy - permissions-link
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4286346&req=5

Figure 4: Or4 responds to sulcatone, a human odoranta, Schematic of gas chromatography-coupled single sensillum recording (GC-SSR). FID = flame ionization detector. b, Sample GC-SSR output, with SSR trace at the top showing large-amplitude spikes (black) from the Or4-expressing neuron and FID output showing elution times of human volatiles (middle trace) and sulcatone (bottom trace). c, Magnified sections of sample total ion chromatogram traces from GC-mass spectrometry (GC-MS) analysis of human (top) and guinea pig (bottom) sleeves. d, Summary of sulcatone and benzaldehyde emission from unworn, human, and guinea pig sleeves (n = 4 - 5 replicates per group; violin plots clipped at the range of data; median: black dot; 1st and 3rd quartile: bounds of black bar). Violins labelled with different letters are statistically different (pairwise Wilcoxon tests with Bonferroni correction; ns = not significant). e, Summary of sulcatone and benzaldehyde levels in human and animal odour collections (n = 1 collection from 1 - 20 individuals per species).
Mentions: An olfactory receptor could modulate host preference by mediating attraction or repulsion to specific host odours, so we asked whether Or4 is activated by a component of human or guinea pig odour. We expressed the genome reference allele of Or4 heterologously in a Drosophila olfactory neuron lacking a ligand-selective OR26, and tested responses to fractionated host odour from guinea pigs and humans (Fig. 4a). Or4 did not respond to any fraction of guinea pig odour (data not shown), but responded consistently to a fraction of human odour corresponding to 6-methyl-5-hepten-2-one, commonly called sulcatone (Fig. 4b).

Bottom Line: A 'domestic' form of the mosquito Aedes aegypti has evolved to specialize in biting humans and is the main worldwide vector of dengue, yellow fever, and chikungunya viruses.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 recognizes 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 specialize on humans.

View Article: PubMed Central - PubMed

Affiliation: 1] Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, New York 10065, USA [2] Howard Hughes Medical Institute, 1230 York Avenue, New York, New York 10065, USA.

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 main worldwide vector of dengue, yellow fever, and chikungunya viruses. The domestic form coexists with an ancestral, 'forest' form that prefers to bite non-human animals and is found along the coast of Kenya. We collected the two forms, established laboratory colonies, and document striking divergence in preference for human versus non-human 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 recognizes 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 specialize on humans.

Show MeSH
Related in: MedlinePlus