Sugar sensation and mechanosensation in the egg-laying preference shift of Drosophila suzukii
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Wang, Carlson, and colleagues investigate sensory adaptations in the fruit pest Drosophila suzukii, which prefers ripe over overripe fruit. This study focuses on changes in sensory pathways for sugars and food texture, which may contribute to ecological shifts. Several interesting physiological and molecular adaptations are observed in D. suzukii, but it remains unclear whether these observed changes account for behavioral changes.
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Abstract
The agricultural pest Drosophila suzukii differs from most other Drosophila species in that it lays eggs in ripe, rather than overripe, fruit. Previously, we showed that changes in bitter taste sensation accompanied this adaptation (Dweck et al., 2021). Here, we show that D. suzukii has also undergone a variety of changes in sweet taste sensation. D. suzukii has a weaker preference than Drosophila melanogaster for laying eggs on substrates containing all three primary fruit sugars: sucrose, fructose, and glucose. Major subsets of D. suzukii taste sensilla have lost electrophysiological responses to sugars. Expression of several key sugar receptor genes is reduced in the taste organs of D. suzukii . By contrast, certain mechanosensory channel genes, including no mechanoreceptor potential C , are expressed at higher levels in the taste organs of D. suzukii , which has a higher preference for stiff substrates. Finally, we find that D. suzukii responds differently from D. melanogaster to combinations of sweet and mechanosensory cues. Thus, the two species differ in sweet sensation, mechanosensation, and their integration, which are all likely to contribute to the differences in their egg-laying preferences in nature.
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Author Response
Reviewer #3 (Public Review):
This paper focuses on characterizing differences between D. suzukii and D. melanogaster preferences for laying eggs on substrates of varying sugar content and stiffness. The authors demonstrate that D. suzukii show a weaker preference for multiple sugars in oviposition choice assays, that D. suzukii show a loss of sugar responsiveness in some labellar sensilla, and that some GR-encoding genes are expressed at much lower levels compared to. D. melanogaster in the legs and labellum. Intriguingly, a number of mechanosensory channel genes are upregulated In D. suzukii legs and labellum. The authors show that D. suzukii females prefer stiffer oviposition substrates compared to D. melanogaster and the balance of sweetness/texture preference differs between the two species. This is consistent …
Author Response
Reviewer #3 (Public Review):
This paper focuses on characterizing differences between D. suzukii and D. melanogaster preferences for laying eggs on substrates of varying sugar content and stiffness. The authors demonstrate that D. suzukii show a weaker preference for multiple sugars in oviposition choice assays, that D. suzukii show a loss of sugar responsiveness in some labellar sensilla, and that some GR-encoding genes are expressed at much lower levels compared to. D. melanogaster in the legs and labellum. Intriguingly, a number of mechanosensory channel genes are upregulated In D. suzukii legs and labellum. The authors show that D. suzukii females prefer stiffer oviposition substrates compared to D. melanogaster and the balance of sweetness/texture preference differs between the two species. This is consistent with their ecological niches, with D. suzukii generally preferring to lay eggs in ripe fruit and D. melanogaster generally preferring overripe fruit.
This paper builds on previous work from this group (Dweck et al., 2021) and others (Karageorgi et al., 2017 and others) that previously demonstrated that D. suzukii prefer to lay eggs on stiffer substrates compared to D. melanogaster, will tolerate more bitter substrates and show reduced expression of several bitter GR genes. This manuscript appropriately acknowledges this work and the findings are consistent with these studies.
The manuscript is well-written, the experiments are well-controlled, the figures clearly convey the experimental findings, the data support the authors conclusions, and the statistical analysis is appropriate.
The weakest point of the paper is the lack of connection drawn between the sequencing, electrophysiological, and behavioral data. For example, the electrophysiological responses to glucose appear to be the same in both species in Figure 3 but the behavioral responses in Figure 2 are different between the two species. The authors do not provide any speculation as to what could account for this seeming discrepancy.
The revised ms. contains the following statement: " The weaker behavioral responses to glucose observed in D. suzukii could derive from weaker responses of untested taste neurons. Multiple taste organs, including the pharynx as well as the labellum and legs, contribute to oviposition behavior; sensory neurons of the ovipositor appear to play an important role as well (Yang et al., 2008; Joseph et al., 2012; Chen et al., 2022). The weaker behavioral response to glucose in D. suzukii could also arise from differences in central processing of glucose signals. It will be interesting to determine if there are differences in the connectivity of taste circuits in the two species. Alternatively, taste projection neurons in D. suzukii could have a reduced dynamic range, saturate at lower levels of receptor neuron firing, and be less able to distinguish among higher sugar concentrations."
Additionally, although Gr64d transcript is almost completely absent in D. suzukii leg RNA seq data in Figure 4B, there are no differences in the electrophysiological responses in leg sensilla in Figure 3.
This seems to imply that, although there are differences gene expression of some Grs that this does not necessarily lead to a functional difference.
We have added to the Discussion a statement to clarify that although similar, the sugar responses of leg sensilla are in fact not the same in the two species: "Leg sensilla of D. suzukii responded to sucrose, but dose-response analysis of the f5s sensillum of the leg showed that the response was lower than in its D. melanogaster counterpart to higher concentrations of sucrose (Figure 3—figure supplement 1E) ."
The authors identify mechanosensory genes that are upregulated in D. suzukii compared to D. melanogaster and suggest that these changes underlie the difference in substrate stiffness. However, it is not immediately clear that high levels of these mechanosensors would impart a new oviposition preference. Although the authors acknowledge that there are likely circuit-level differences between the two species, they do not directly test the role of any of these mechanosensors in oviposition preference in either species.
See response below to the point about nompC.
In Figure 3 there are clear differences in some of labellar responses but the leg responses look similar overall. This suggests that the labellum is playing a special role in oviposition evaluation. The paper would be strengthened by providing more insight into which tissues (labellum, legs, wings, ovipositor, etc...) are likely used to sample potential egg laying substrates.
We agree and have added to the Discussion the following: "Multiple taste organs, including the pharynx as well as the labellum and legs, contribute to oviposition behavior; sensory neurons of the ovipositor appear to play an important role as well (Yang Science 2008; Joseph Genetics 2012; Chen PNAS 2022)."
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eLife assessment
Wang, Carlson, and colleagues investigate sensory adaptations in the fruit pest Drosophila suzukii, which prefers ripe over overripe fruit. This study focuses on changes in sensory pathways for sugars and food texture, which may contribute to ecological shifts. Several interesting physiological and molecular adaptations are observed in D. suzukii, but it remains unclear whether these observed changes account for behavioral changes.
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Reviewer #1 (Public Review):
This study characterizes interesting behavioral differences between the pest Drosophila Suzuki, and the well-studied fruit fly Drosophila melanogaster. D. Suzuki display a weaker preference for sugar-rich foods, and also prefer harder food substrates. The manuscript then investigates changes in electrophysiological responses to sugars, finding that some but not all sweet-sensing sensilla are lost. The authors also show reduced expression of several sweet-sensing gustatory receptors and increased expression of several mechanoreceptors in D. Suzuki. Additional studies are needed to determine whether physiological and molecular changes account for observed behavioral changes.
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Reviewer #2 (Public Review):
Drosophila suzukii prefers to lay eggs on ripe, intact fruit, which contrasts with Drosophila melanogaster, which lays eggs primarily on overripe fruit. The goal of the work by Wang et al. is to decipher the basis for this difference. Part of the explanation is that D. suzukii have a lower preference for sugars, compared to D. melanogaster. Based on electrophysiological recordings, the lower sugar preference in D. suzukii could be due in part to reduced sugar responsiveness of their gustatory receptor neurons in the labella.
The authors then performed transcriptome analyses to analyze the differential expression genes in the tarsi and labella of D. melanogaster and D. suzukii. They found that multiple sugar Grs were reduced in expression in D. suzukii, potentially accounting for the lower sugar …
Reviewer #2 (Public Review):
Drosophila suzukii prefers to lay eggs on ripe, intact fruit, which contrasts with Drosophila melanogaster, which lays eggs primarily on overripe fruit. The goal of the work by Wang et al. is to decipher the basis for this difference. Part of the explanation is that D. suzukii have a lower preference for sugars, compared to D. melanogaster. Based on electrophysiological recordings, the lower sugar preference in D. suzukii could be due in part to reduced sugar responsiveness of their gustatory receptor neurons in the labella.
The authors then performed transcriptome analyses to analyze the differential expression genes in the tarsi and labella of D. melanogaster and D. suzukii. They found that multiple sugar Grs were reduced in expression in D. suzukii, potentially accounting for the lower sugar responsiveness of D. suzukii.
Ripe fruit is harder than overripe fruit. Therefore, the authors considered whether the differential preferences for D. suzukii and D. melanogaster to lay eggs on ripe and overripe food respectively might be due in part to distinct biases for substrates of different hardness. Indeed, D. suzukii and D. melanogaster preferred harder and softer food, respectively. Moreover, several mechanosensory genes, most notably nompC, were expressed at higher levels in D. suzukii.
The authors also examined combinations of different concentrations of sugars and different levels of food hardness. The results support the conclusion that both food hardness and sugar levels contribute to the distinct preferences for oviposition sites for D. suzukii and D. melanogaster.
This work does an excellent job of employing a diverse combination of approaches (behavioral, electrophysiological and transcriptomics) to interrogate the basis for the differences in oviposition preferences in the two Drosophila species. Moreover, this study raises many new questions concerning the mechanisms contributing to the distinct preferences for ripe and overripe fruit exhibited by D. suzukii and D. melanogaster.
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Reviewer #3 (Public Review):
This paper focuses on characterizing differences between D. suzukii and D. melanogaster preferences for laying eggs on substrates of varying sugar content and stiffness. The authors demonstrate that D. suzukii show a weaker preference for multiple sugars in oviposition choice assays, that D. suzukii show a loss of sugar responsiveness in some labellar sensilla, and that some GR-encoding genes are expressed at much lower levels compared to. D. melanogaster in the legs and labellum. Intriguingly, a number of mechanosensory channel genes are upregulated In D. suzukii legs and labellum. The authors show that D. suzukii females prefer stiffer oviposition substrates compared to D. melanogaster and the balance of sweetness/texture preference differs between the two species. This is consistent with their ecological …
Reviewer #3 (Public Review):
This paper focuses on characterizing differences between D. suzukii and D. melanogaster preferences for laying eggs on substrates of varying sugar content and stiffness. The authors demonstrate that D. suzukii show a weaker preference for multiple sugars in oviposition choice assays, that D. suzukii show a loss of sugar responsiveness in some labellar sensilla, and that some GR-encoding genes are expressed at much lower levels compared to. D. melanogaster in the legs and labellum. Intriguingly, a number of mechanosensory channel genes are upregulated In D. suzukii legs and labellum. The authors show that D. suzukii females prefer stiffer oviposition substrates compared to D. melanogaster and the balance of sweetness/texture preference differs between the two species. This is consistent with their ecological niches, with D. suzukii generally preferring to lay eggs in ripe fruit and D. melanogaster generally preferring overripe fruit.
This paper builds on previous work from this group (Dweck et al., 2021) and others (Karageorgi et al., 2017 and others) that previously demonstrated that D. suzukii prefer to lay eggs on stiffer substrates compared to D. melanogaster, will tolerate more bitter substrates and show reduced expression of several bitter GR genes. This manuscript appropriately acknowledges this work and the findings are consistent with these studies.
The manuscript is well-written, the experiments are well-controlled, the figures clearly convey the experimental findings, the data support the authors conclusions, and the statistical analysis is appropriate.
The weakest point of the paper is the lack of connection drawn between the sequencing, electrophysiological, and behavioral data. For example, the electrophysiological responses to glucose appear to be the same in both species in Figure 3 but the behavioral responses in Figure 2 are different between the two species. The authors do not provide any speculation as to what could account for this seeming discrepancy. Additionally, although Gr64d transcript is almost completely absent in D. suzukii leg RNA seq data in Figure 4B, there are no differences in the electrophysiological responses in leg sensilla in Figure 3. This seems to imply that, although there are differences gene expression of some Grs that this does not necessarily lead to a functional difference.
The authors identify mechanosensory genes that are upregulated in D. suzukii compared to D. melanogaster and suggest that these changes underlie the difference in substrate stiffness. However, it is not immediately clear that high levels of these mechanosensors would impart a new oviposition preference. Although the authors acknowledge that there are likely circuit-level differences between the two species, they do not directly test the role of any of these mechanosensors in oviposition preference in either species.
In Figure 3 there are clear differences in some of labellar responses but the leg responses look similar overall. This suggests that the labellum is playing a special role in oviposition evaluation. The paper would be strengthened by providing more insight into which tissues (labellum, legs, wings, ovipositor, etc...) are likely used to sample potential egg laying substrates.
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