Wild African Drosophila melanogaster Are Seasonal Specialists on Marula Fruit

Mansourian, Suzan; Enjin, Anders; Jirle, Erling; Ramesh, Vedika; Rehermann, Guillermo; Becher, Paul G.; Pool, John E.; Stensmyr, Marcus C.

doi:10.1016/j.cub.2018.10.033

Cited by 92 publications

(118 citation statements)

References 39 publications

Supporting

Mentioning

114

Contrasting

Order By: Relevance

“…Here we found the same correlation between pairwise SSR similarities and pairwise sequence similarities for ab2Blike responses and the corresponding Or85a sequences as well. However, D. suzukii showed overall much less similarity regarding both SSR and sequence data as compared to the other species (red dots; Supplementary Figure 10 C,D), which indicates that Or85a (ab2B) may have been replaced by another receptor protein 42 . Notably, we identified the lowest sequence similarities within the transmembrane regions 1 and 3 (Supplementary Figure 10 E,F), suggesting that these regions of the protein might be involved in speciation events across the Drosophila genus, as was previously suggested from analyses of the melanogaster clade 15 .…”

Section: Receptor Sequence Alignments Across the Sophophora Subgenusmentioning

confidence: 98%

“…Thus, at this stage, we cannot definitively say whether the variation in ab2B is (a) due to a drastic ligand shift in the receptor expression (i.e. protein sequence variation), (b) due to the replacement with a new or duplicated olfactory receptor 42 , or lastly, (c) whether these changes are the result of non-functional pseudogenes. However, at least in D. suzukii, we have shown that the ab2B neuron, despite this acute shift in ligand spectrum, remains a fully functional OSN type.…”

Section: Functional Ligand Spectra For Sensillum Types Across Sophophoramentioning

confidence: 98%

See 1 more Smart Citation

Evolution of a pest: towards the complete neuroethology of Drosophila suzukii and the subgenus Sophophora

Keesey

Zhang

Depetris-Chauvin

et al. 2019

Preprint

View full text Add to dashboard Cite

Comparative analysis of multiple genomes has been used extensively to examine the evolution of chemosensory receptors across the genus Drosophila. However, few studies have delved into functional characteristics, as most have relied exclusively on genomic data alone, especially for non-model species. In order to increase our understanding of olfactory evolution, we have generated a comprehensive assessment of the olfactory functions associated with the antenna and palps for Drosophila suzukii as well as several other members of the subgenus Sophophora, thus creating a functional olfactory landscape across a total of 20 species. Here we identify and describe several common elements of evolution, including consistent changes in ligand spectra as well as relative receptor abundance, which appear heavily correlated with the known phylogeny. We also combine our functional ligand data with protein orthologue alignments to provide a high-throughput evolutionary assessment and predictive model, where we begin to examine the underlying mechanisms of evolutionary changes utilizing both genetics and odorant binding affinities. In addition, we document that only a few receptors frequently vary between species, and we evaluate the justifications for evolution to reoccur repeatedly within only this small subset of available olfactory sensory neurons.

show abstract

Section: Receptor Sequence Alignments Across the Sophophora Subgenusmentioning

confidence: 98%

Section: Functional Ligand Spectra For Sensillum Types Across Sophophoramentioning

confidence: 98%

Evolution of a pest: towards the complete neuroethology of Drosophila suzukii and the subgenus Sophophora

Keesey

Zhang

Depetris-Chauvin

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…Studies on wild populations of D. melanogaster in Zimbabwe show that these African flies feed and oviposit almost exclusively on marula fruit (Sclerocarya birrea), a citrus-like endemic fruit. This specialization is not observed in sympatric D. simulans (Mansourian et al, 2018). Ethyl isovalerate produced by the marula fruit acts as an olfactory cue for oviposition site preference by activating ab3A neurons, which project to the DM2 glomerulus and express a distinct Or22a/Or22b variant in this fly population.…”

Section: Co-evolution Of Chemosensation and Host Plant Selectionmentioning

confidence: 74%

“…Ethyl isovalerate produced by the marula fruit acts as an olfactory cue for oviposition site preference by activating ab3A neurons, which project to the DM2 glomerulus and express a distinct Or22a/Or22b variant in this fly population. Even laboratory-reared flies of the Canton-S strain still favor marula fruit in preference assays (Mansourian et al, 2018). Thus, specialization on marula of African D. melanogaster may be ancestral to the generalist host plant relationships of cosmopolitan D. melanogaster, illustrating plasticity and evolvability of insect-host plant relationships.…”

Section: Co-evolution Of Chemosensation and Host Plant Selectionmentioning

confidence: 99%

Chemosensation and Evolution of Drosophila Host Plant Selection

Anholt

2020

iScience

View full text Add to dashboard Cite

“…The best-studied of these is Or22a, which has been evolutionarily lost by gene deletion in S. flava but not in S. pallida (19). In several drosophilids, Or22a is tuned to different ecologically relevant esters: ethyl-hexanoate in D. melanogaster (16), methylhexanoate in D. sechellia (42), 3-methyl-2-butenyl acetate in D. erecta (17), and isobutyl acetate in D. suzukii (43). Similarly, Ir75b is respectively tuned to butyric acid in D. melanogaster and to hexanoic acid in D. sechellia (15).…”

Section: Discussionmentioning

confidence: 99%

Evolution of olfactory receptors tuned to mustard oils in herbivorous Drosophilidae

Matsunaga

Reisenman

Goldman-Huertas

et al. 2019

Preprint

View full text Add to dashboard Cite

248): 21 Plant toxins are effective defenses because they are aversive to most insects. The same 22 molecules, however, are co-opted as host-finding cues by specialist herbivores. Although such 23 behavioral shifts are central to our understanding of herbivorous insect diversification, it is not 24 well understood how these behaviors evolve. We addressed this in Scaptomyza flava, a 25 herbivorous drosophilid fly within a lineage that shifted to feeding on toxic mustard plants 26 (Brassicales) less than 10 million years ago. S flava lost the ancestral attraction to yeast volatiles 27 and the attendant chemoreceptors used to detect these odors. Here we report that S. flava, but not 28 its close microbe-feeding relatives Drosophila melanogaster and S. pallida, is attracted to 29 mustard host-plant odors, including volatile mustard oils (isothiocyanates or ITCs). Our genomic 30 analysis uncovered three S. flava paralogs of an olfactory receptor gene (Or67b) that likely 31 experienced recent positive selection. We then tested whether these chemoreceptors could 32 underlie the observed attraction to volatile ITCs. Our in vivo recordings revealed that two of the 33 S. flava Or67b proteins (Or67b1 and Or67b3) -but not the homologous Ors from microbe-34 feeding relatives -responded selectively and sensitively to volatile ITCs. These Ors are the first 35 ITC chemoreceptors other than TRP channel family (e.g., the TrpA1 'wasabi' receptor) known 36 from any animal. Remarkably, S. flava Or67b3 was sufficient to drive olfactory attraction toward 37 butyl ITC when expressed in an attractive olfactory circuit. Our study illuminates that ancestrally 38 aversive chemicals can be co-opted as attractants through gene duplication, leading to the origin 39 of hedonic valence shifts in herbivorous insects. 40 41 42Significance Statement (120) 43 Plant toxins trigger aversive olfactory (volatile-mediated) and gustatory (contact-mediated) 44 responses in animals. Paradoxically, toxic plants are often colonized by specialist insects that co-45 opt these toxins as host-plant finding cues. The mechanisms underlying these behavioral shifts, 46 from indifference or repulsion to plant chemicals, to attraction, remain unclear. To address this, 47 we used a fly lineage, Scaptomyza, that switched from yeast-feeding to feeding on mustard plants 48 less than 10 million years ago. We found that S. flava is attracted to mustard-plant odors and 49 volatile mustard oils (isothiocyanates or ITCs) such as 'wasabi', a behavior enabled by the 50 evolution of genes encoding odorant receptors highly sensitive to ITCs. Our study illuminates 51 how insects colonize toxic host plants through duplication and ecological repurposing of genes 52 encoding pre-existing chemoreceptors. 53 54 55 56 57 Many plant compounds used in food, agriculture and medicine originally evolved as 58 toxins that deter and repel enemies (1). Among the most well-known compounds are those 59 reactive electrophiles that induce the sensation of pain, such as diallyl disulfide a...

show abstract

Wild African Drosophila melanogaster Are Seasonal Specialists on Marula Fruit

Cited by 92 publications

References 39 publications

Evolution of a pest: towards the complete neuroethology of Drosophila suzukii and the subgenus Sophophora

Evolution of a pest: towards the complete neuroethology of Drosophila suzukii and the subgenus Sophophora

Chemosensation and Evolution of Drosophila Host Plant Selection

Evolution of olfactory receptors tuned to mustard oils in herbivorous Drosophilidae

Contact Info

Product

Resources

About