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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.

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Antennal gene expression is significantly associated with preference for humansa, Schematic of isolation of strongly human- and guinea pig-preferring F2 females. b, Live host olfactometer preference of parent colonies (n = 4 - 7 trials, mean ± s.e.m.) and F2 hybrids (n = 1). c-d, Differential antennal gene expression in colonies (c) and F2 hybrids (d) measured via RNAseq (FDR = 0.05). Filled and open arrowheads point to Or4 and Or103, respectively. e, Summary of differential gene expression in c-d. f, Numbers of detectable (fpkm≥ 1) (top row) or differentially expressed (bottom 3 rows) olfactory receptors (ORs), ionotropic receptors (IRs), and odorant-binding proteins (OBPs) (% of total genes shown in parentheses). Asterisks indicate significant enrichment relative to % of all detectable genes (χ2P < 0.0001). g, Heat maps of ligand-selective OR genes with log10fpkm expression > 0.83 in domestic (top) or > 0.84 in forest (bottom) colonies, with two ORs differentially (solid lines) or not differentially expressed (dashed lines) indicated.
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Figure 3: Antennal gene expression is significantly associated with preference for humansa, Schematic of isolation of strongly human- and guinea pig-preferring F2 females. b, Live host olfactometer preference of parent colonies (n = 4 - 7 trials, mean ± s.e.m.) and F2 hybrids (n = 1). c-d, Differential antennal gene expression in colonies (c) and F2 hybrids (d) measured via RNAseq (FDR = 0.05). Filled and open arrowheads point to Or4 and Or103, respectively. e, Summary of differential gene expression in c-d. f, Numbers of detectable (fpkm≥ 1) (top row) or differentially expressed (bottom 3 rows) olfactory receptors (ORs), ionotropic receptors (IRs), and odorant-binding proteins (OBPs) (% of total genes shown in parentheses). Asterisks indicate significant enrichment relative to % of all detectable genes (χ2P < 0.0001). g, Heat maps of ligand-selective OR genes with log10fpkm expression > 0.83 in domestic (top) or > 0.84 in forest (bottom) colonies, with two ORs differentially (solid lines) or not differentially expressed (dashed lines) indicated.

Mentions: Novel chemosensory preferences in insects are sometimes accompanied by changes in the peripheral chemosensory system16-20. We reasoned that altered gene expression in antennae may contribute to preference, and profiled differential gene expression in this major olfactory organ using RNAseq. To identify general differences between forms, we compared forest versus domestic colonies (Fig. 2h). To determine which of these differences are genetically associated with host preference21, we crossed two representative colonies and compared pools of strongly human- versus guinea pig-preferring F2 hybrids (Fig. 3a-b).


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)

Antennal gene expression is significantly associated with preference for humansa, Schematic of isolation of strongly human- and guinea pig-preferring F2 females. b, Live host olfactometer preference of parent colonies (n = 4 - 7 trials, mean ± s.e.m.) and F2 hybrids (n = 1). c-d, Differential antennal gene expression in colonies (c) and F2 hybrids (d) measured via RNAseq (FDR = 0.05). Filled and open arrowheads point to Or4 and Or103, respectively. e, Summary of differential gene expression in c-d. f, Numbers of detectable (fpkm≥ 1) (top row) or differentially expressed (bottom 3 rows) olfactory receptors (ORs), ionotropic receptors (IRs), and odorant-binding proteins (OBPs) (% of total genes shown in parentheses). Asterisks indicate significant enrichment relative to % of all detectable genes (χ2P < 0.0001). g, Heat maps of ligand-selective OR genes with log10fpkm expression > 0.83 in domestic (top) or > 0.84 in forest (bottom) colonies, with two ORs differentially (solid lines) or not differentially expressed (dashed lines) indicated.
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Related In: Results  -  Collection

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Figure 3: Antennal gene expression is significantly associated with preference for humansa, Schematic of isolation of strongly human- and guinea pig-preferring F2 females. b, Live host olfactometer preference of parent colonies (n = 4 - 7 trials, mean ± s.e.m.) and F2 hybrids (n = 1). c-d, Differential antennal gene expression in colonies (c) and F2 hybrids (d) measured via RNAseq (FDR = 0.05). Filled and open arrowheads point to Or4 and Or103, respectively. e, Summary of differential gene expression in c-d. f, Numbers of detectable (fpkm≥ 1) (top row) or differentially expressed (bottom 3 rows) olfactory receptors (ORs), ionotropic receptors (IRs), and odorant-binding proteins (OBPs) (% of total genes shown in parentheses). Asterisks indicate significant enrichment relative to % of all detectable genes (χ2P < 0.0001). g, Heat maps of ligand-selective OR genes with log10fpkm expression > 0.83 in domestic (top) or > 0.84 in forest (bottom) colonies, with two ORs differentially (solid lines) or not differentially expressed (dashed lines) indicated.
Mentions: Novel chemosensory preferences in insects are sometimes accompanied by changes in the peripheral chemosensory system16-20. We reasoned that altered gene expression in antennae may contribute to preference, and profiled differential gene expression in this major olfactory organ using RNAseq. To identify general differences between forms, we compared forest versus domestic colonies (Fig. 2h). To determine which of these differences are genetically associated with host preference21, we crossed two representative colonies and compared pools of strongly human- versus guinea pig-preferring F2 hybrids (Fig. 3a-b).

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