Desiccation resistance differences in Drosophila species can be largely explained by variations in cuticular hydrocarbons
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Evaluation Summary:
This paper is an extensive analysis of the underlying basis of desiccation resistance in 50 Drosophila species from diverse habitats. The work suggests that the longer methyl-branched alkanes (mbCHC) of the cuticular hydrocarbons are critical for this resistance. The study, which informs on the evolution of desiccation resistance in flies, is well done, although the main hypothesis is currently only partially supported by coating experiments, which presently lack controls and would be greatly strengthened by "replacement" experiments to add mbCHCs to flies without CHCs. The work is of relevance to evolutionary biologists in general.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Abstract
Maintaining water balance is a universal challenge for organisms living in terrestrial environments, especially for insects, which have essential roles in our ecosystem. Although the high surface area to volume ratio in insects makes them vulnerable to water loss, insects have evolved different levels of desiccation resistance to adapt to diverse environments. To withstand desiccation, insects use a lipid layer called cuticular hydrocarbons (CHCs) to reduce water evaporation from the body surface. It has long been hypothesized that the water-proofing capability of this CHC layer, which can confer different levels of desiccation resistance, depends on its chemical composition. However, it is unknown which CHC components are important contributors to desiccation resistance and how these components can determine differences in desiccation resistance. In this study, we used machine-learning algorithms, correlation analyses, and synthetic CHCs to investigate how different CHC components affect desiccation resistance in 50 Drosophila and related species. We showed that desiccation resistance differences across these species can be largely explained by variation in CHC composition. In particular, length variation in a subset of CHCs, the methyl-branched CHCs (mbCHCs), is a key determinant of desiccation resistance. There is also a significant correlation between the evolution of longer mbCHCs and higher desiccation resistance in these species. Given that CHCs are almost ubiquitous in insects, we suggest that evolutionary changes in insect CHC components can be a general mechanism for the evolution of desiccation resistance and adaptation to diverse and changing environments.
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Evaluation Summary:
This paper is an extensive analysis of the underlying basis of desiccation resistance in 50 Drosophila species from diverse habitats. The work suggests that the longer methyl-branched alkanes (mbCHC) of the cuticular hydrocarbons are critical for this resistance. The study, which informs on the evolution of desiccation resistance in flies, is well done, although the main hypothesis is currently only partially supported by coating experiments, which presently lack controls and would be greatly strengthened by "replacement" experiments to add mbCHCs to flies without CHCs. The work is of relevance to evolutionary biologists in general.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The …
Evaluation Summary:
This paper is an extensive analysis of the underlying basis of desiccation resistance in 50 Drosophila species from diverse habitats. The work suggests that the longer methyl-branched alkanes (mbCHC) of the cuticular hydrocarbons are critical for this resistance. The study, which informs on the evolution of desiccation resistance in flies, is well done, although the main hypothesis is currently only partially supported by coating experiments, which presently lack controls and would be greatly strengthened by "replacement" experiments to add mbCHCs to flies without CHCs. The work is of relevance to evolutionary biologists in general.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Reviewer #1 (Public Review):
In their manuscript, the authors compared the CHC quality in around 50 different, including distantly related fruit fly species that occupy diverse habitats. Based on correlative data (produced by appropriate statistical analyses), they hypothesise that methyl-branched alkanes (mbCHC) might be decisive in resistance against desiccation in these species. They confirm previously published results that rather than the amount of CHC their quality plays an important role in desiccation resistance. Moreover, their results indicate that desiccation resistance increases with longer mbCHCs. In mbCHC coating experiments, the authors tentatively support their hypothesis.
Overall, the data are impressive, and their statistical analyses (Pearson's method, etc) are performed accurately yielding convincing results. These …
Reviewer #1 (Public Review):
In their manuscript, the authors compared the CHC quality in around 50 different, including distantly related fruit fly species that occupy diverse habitats. Based on correlative data (produced by appropriate statistical analyses), they hypothesise that methyl-branched alkanes (mbCHC) might be decisive in resistance against desiccation in these species. They confirm previously published results that rather than the amount of CHC their quality plays an important role in desiccation resistance. Moreover, their results indicate that desiccation resistance increases with longer mbCHCs. In mbCHC coating experiments, the authors tentatively support their hypothesis.
Overall, the data are impressive, and their statistical analyses (Pearson's method, etc) are performed accurately yielding convincing results. These results, however, are not as strong as the statement in the abstract that longer mbCHCs are a "key determinant" of desiccation resistance. Admittedly, the authors' wording is very and appropriately careful about this issue.
One major weakness of this work is the coating experiments. The authors simply incubate Drosophila melanogaster flies with mbCHC and observe that they become more resistant to drought. Along with this "adding" experiment, "replacement" experiments should be carried out, ie add the mbCHC to flies without CHCs. Moreover, control experiments with CHCs with the same chain lengths but without branched methyl groups should be added. This point is crucial as the authors tempt with it to render their correlative data causative.
A second point that needs more attention regarding the discrepancies between males and females (e.g Fig. 3 & 5). These data are not discussed.
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Reviewer #2 (Public Review):
Wang et al. used 50 Drosophila species and close relatives to assess how differences in CHCs affect desiccation resistance. They first demonstrate that simply having greater abundance of CHCs is not enough to confer desiccation resistance. They then use multivariate analysis to show that CHC composition did affect desiccation resistance. Random forest modeling was used to identify methylbranched CHCs (mbCHCs) and mbCHC length as major contributors to desiccation resistance. An experimental test of this idea was performed by treating D.melanogaster with mbCHCs of different lengths, with longer lengths having a greater effect on desiccation resistance. Finally, the authors ask whether the evolution of CHCs in Drosophila is consistent with these findings. Using a phylogenetically controlled approach, they show …
Reviewer #2 (Public Review):
Wang et al. used 50 Drosophila species and close relatives to assess how differences in CHCs affect desiccation resistance. They first demonstrate that simply having greater abundance of CHCs is not enough to confer desiccation resistance. They then use multivariate analysis to show that CHC composition did affect desiccation resistance. Random forest modeling was used to identify methylbranched CHCs (mbCHCs) and mbCHC length as major contributors to desiccation resistance. An experimental test of this idea was performed by treating D.melanogaster with mbCHCs of different lengths, with longer lengths having a greater effect on desiccation resistance. Finally, the authors ask whether the evolution of CHCs in Drosophila is consistent with these findings. Using a phylogenetically controlled approach, they show that the evolution of longer mbCHCs is correlated with greater desiccation resistance in at least 4 clades within Drosophila.
Overall, I found this a very interesting body of work. There is longstanding literature discussing how a change in CHC amounts and composition should affect that n-alkanes seem to be driving differences in desiccation resistance. The presence of methyl branches should lower melting points, but perhaps this is offset by their greater chain lengths. However, the 'perfuming' experiments provide good experimental support for the statistical correlations. It should be noted that mbCHCs can also act as cuticular pheromone components, so this work may have implications for insect chemical ecology.
It remains to be seen whether the conclusions of this work extend beyond Drosophila. Many insects have internally branched CHCs, whereas Drosophila do not. Drosophila is also unusual in having few or no n-alkanes.
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Reviewer #3 (Public Review):
This study utilizes 46 species of Drosophila and 4 closely related species to try and determine the relative role of specific hydrocarbons on desiccation resistance. The use of many species of Drosophila that have variations in hydrocarbon profiles and variations in natural desiccation resistances allowed the researchers to draw conclusions about the relative role of specific hydrocarbons contributing to preventing water loss through the cuticle. By using a statistical package they were able to conclude that methyl-branched hydrocarbons are the most important in those species that were more desiccation resistant. This is not surprising since a previous study has shown that 2 methyl-branched hydrocarbons have the highest melting temperatures. In addition, it seems that desiccation resistance also involves …
Reviewer #3 (Public Review):
This study utilizes 46 species of Drosophila and 4 closely related species to try and determine the relative role of specific hydrocarbons on desiccation resistance. The use of many species of Drosophila that have variations in hydrocarbon profiles and variations in natural desiccation resistances allowed the researchers to draw conclusions about the relative role of specific hydrocarbons contributing to preventing water loss through the cuticle. By using a statistical package they were able to conclude that methyl-branched hydrocarbons are the most important in those species that were more desiccation resistant. This is not surprising since a previous study has shown that 2 methyl-branched hydrocarbons have the highest melting temperatures. In addition, it seems that desiccation resistance also involves other factors since some species that had lower desiccation rates had similar amounts of methyl branched hydrocarbons. It is also difficult to extrapolate to other insects that have a variety of lipids on their cuticular surface. Probably most insects will have hydrocarbons but some have a variety of other lipids on the cuticular surface that will contribute to preventing desiccation. The use of Drosophila species in this study is fortuitous because apparently only hydrocarbons are found on the cuticular surface.
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