Dataset Information

Species and sex-specific chemosensory gene expression in Anopheles coluzzii and An. quadriannulatus antennae.

ABSTRACT:

Background

Olfactory cues drive mosquito behaviors such as host-seeking, locating sugar sources and oviposition. These behaviors can vary between sexes and closely related species. For example, the malaria vector Anopheles coluzzii is highly anthropophilic, whereas An. quadriannulatus is not. These behavioral differences may be reflected in chemosensory gene expression.

Methods

The expression of chemosensory genes in the antennae of both sexes of An. coluzzii and An. quadriannulatus was compared using RNA-seq. The sex-biased expression of several genes in An. coluzzii was also compared using qPCR.

Results

The chemosensory expression is mostly similar in the male antennae of An. coluzzii and An. quadriannulatus, with only a few modest differences in expression. A handful of chemosensory genes are male-biased in both species; the highly expressed gustatory receptor AgGr33, odorant binding proteins AgObp25, AgObp26 and possibly AgObp10. Although the chemosensory gene repertoire is mostly shared between the sexes, several highly female-biased AgOrs, AgIrs, and one AgObp were identified, including several whose expression is biased towards the anthropophilic An. coluzzii. Additionally, the expression of several chemosensory genes is biased towards An. coluzzii in both sexes.

Conclusions

Chemosensory gene expression is broadly similar between species and sexes, but several sex- biased/specific genes were identified. These may modulate sex- and species-specific behaviors. Although the male behavior of these species remains poorly studied, the identification of sex- and species-specific chemosensory genes may provide fertile ground for future work.

SUBMITTER: Athrey G

PROVIDER: S-EPMC7178735 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Publications

Species and sex-specific chemosensory gene expression in Anopheles coluzzii and An. quadriannulatus antennae.

Athrey Giridhar G Popkin-Hall Zachary Z Cosme Luciano Veiga LV Takken Willem W Slotman Michel Andre MA

Parasites & vectors 20200422 1

<h4>Background</h4>Olfactory cues drive mosquito behaviors such as host-seeking, locating sugar sources and oviposition. These behaviors can vary between sexes and closely related species. For example, the malaria vector Anopheles coluzzii is highly anthropophilic, whereas An. quadriannulatus is not. These behavioral differences may be reflected in chemosensory gene expression.<h4>Methods</h4>The expression of chemosensory genes in the antennae of both sexes of An. coluzzii and An. quadriannulat ...[more]

PMID: 32321556

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Project description:BackgroundAnopheles (An.) coluzzii, one of Africa's primary malaria vectors, is highly anthropophilic. This human host preference contributes greatly to its ability to transmit malaria. In contrast, the closely related An. quadriannulatus prefers to feed on bovids and is not thought to contribute to malaria transmission. The diverged preference for host odor profiles between these sibling species is likely reflected in chemosensory gene expression levels in the olfactory organs. Therefore, we compared the transcriptomes of the antennae and maxillary palps between An. coluzzii and An. quadriannulatus, focusing on the major chemosensory gene families.ResultsWhile chemosensory gene expression is strongly correlated between the two species, various chemosensory genes show significantly enhanced expression in one of the species. In the antennae of An. coluzzii the expression of six olfactory receptors (Ors) and seven ionotropic receptors (Irs) is considerably enhanced, whereas 11 Ors and 3 Irs are upregulated in An. quadriannulatus. In the maxillary palps, leaving aside Irs with very low level of expression, one Ir is strongly enhanced in each species. In addition, we find divergence in odorant binding protein (Obp) gene expression, with several highly expressed Obps being enhanced in the antennae and palps of An. coluzzii. Finally, the expression of several gustatory receptors (Grs) in the palps appears to be species-specific, including a homolog of a sugar-sensing Drosophila Gr.ConclusionsA considerable number of Ors and Irs are differentially expressed between these two closely related species with diverging host preference. These chemosensory genes could play a role in the human host preference of the malaria vector An. coluzzii. Additionally, divergence in Obp expression between the two species suggests a possible role of these odor carrier proteins in determining host preference. Finally, divergence in chemosensory expression in the palps may point towards a possible role for the maxillary palps in host differentiation.

Project description:BackgroundThe malaria mosquito Anopheles gambiae has a high preference for human hosts, a characteristic that contributes greatly to its capacity for transmitting human malaria. A sibling species, An. quadriannulatus, has a quite different host preference and feeds mostly on bovids. For this reason it does not contribute to human malaria transmission. Host seeking in mosquitoes is modulated by the olfactory system, which is primarily housed in the antennae and maxillary palps. Therefore, the detection of differing host odors by sibling species may be reflected in the expression level of the olfactory genes involved. Accordingly, we compared the transcriptomes of the antennae and maxillary palps of An. gambiae and An. quadriannulatus.ResultsWe identified seven relatively abundant olfactory receptors, nine ionotropic receptors and three odorant binding proteins that are substantially up-regulated in An. gambiae antennae. Interestingly, we find that the maxillary palps of An. gambiae contain a species-specific olfactory receptor, Or52, and five An. gambiae-specific gustatory receptors (AgGr48-52) that are relatively abundant. These five gustatory receptors are also expressed in An. gambiae antennae, although at lower level, indicating a likely role in olfaction, rather than gustation. We also document an approximately three-fold higher overall expression of olfaction genes in the maxillary palps of An. quadriannulatus, indicating an important role of this organ in the olfaction system of this species. Finally, the expression of the CO2 receptor genes is five to six-fold higher in the zoophilic An. quadriannulatus, implying a much higher sensitivity for detecting CO2.ConclusionsThese results identify potential human host preference genes in the malaria vector An. gambiae. Interestingly, species-specific expression of several gustatory receptors in the olfactory organs indicate a role in olfaction rather than gustation. Additionally, a more expansive role for maxillary palps in olfaction is implicated than previously thought, albeit more so in the zoophilic An. quadriannulatus.

Project description:Sex chromosome dosage differences between females and males are a significant form of natural genetic variation in many species. Like many species with chromosomal sex determination, Drosophila females have two X chromosomes, while males have one X and one Y. Fusions of sex chromosomes with autosomes have occurred along the lineage leading to D. pseudoobscura and D. miranda. The resulting neo-sex chromosomes are gradually evolving the properties of sex chromosomes, and neo-X chromosomes are becoming targets for the molecular mechanisms that compensate for differences in X chromosome dose between sexes. We have previously shown that D. melanogaster possess at least two dosage compensation mechanisms: the well- characterized MSL-mediated dosage compensation active in most somatic tissues, and another system active during early embryogenesis prior to the onset of MSL-mediated dosage compensation. To better understand the developmental constraints on sex chromosome gene expression and evolution, we sequenced mRNA from individual male and female embryos of D. pseudoobscura and D. miranda, from ∼0.5 to 8 hours of development. Autosomal expression levels are highly conserved between these species. But, unlike D. melanogaster, we observe a general lack of dosage compensation in D. pseudoobscura and D. miranda prior to the onset of MSL-mediated dosage compensation. Thus, either there has been a lineage-specific gain or loss in early dosage compensation mechanism(s) or increasing X chromosome dose may strain dosage compensation systems and make them less effective. The extent of female bias on the X chromosomes decreases through developmental time with the establishment of MSL-mediated dosage compensation, but may do so more slowly in D. miranda than D. pseudoobscura. These results also prompt a number of questions about whether species with more sex-linked genes have more sex-specific phenotypes, and how much transcript level variance is tolerable during critical stages of development.

Dataset Information

Species and sex-specific chemosensory gene expression in Anopheles coluzzii and An. quadriannulatus antennae.

Background

Methods

Results

Conclusions

Publications

Species and sex-specific chemosensory gene expression in Anopheles coluzzii and An. quadriannulatus antennae.

Similar Datasets

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