Desiccation resistance differences in Drosophila species can be largely explained by variations in cuticular hydrocarbons

Wang, Zinan; Receveur, Joseph P.; Pu, Jun; Cong, Haosu; Richards, Cole; Liang, Muxuan; Chung, Henry

doi:10.7554/elife.80859

Cited by 27 publications

(43 citation statements)

References 85 publications

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“…Our experiments showed that transgenic D. melanogaster flies with Dmoj/mElo overexpression were significantly more desiccation resistant (Mean ± SE, Females: 13.0 ± 0.3 h, Males: 7.8 ± 0.2 h) compared to control flies (Females: 8.4 ± 0.2 h, Males: 5.9 ± 0.1 h) and flies with Dmel/mElo overexpression (Females: 10.3 ± 0.2 h, Males: 6.0 ± 0.2 h) ( Figure 2C ). This result demonstrated that the production of longer mbCHCs can significantly increase desiccation resistance, consistent with our previous findings using synthetic mbCHCs (Wang et al ., 2022).…”

Section: Resultssupporting

confidence: 93%

“…We had previously shown that the length of mbCHCs can largely explain desiccation resistance across Drosophila species (Wang et al, 2022). Drosophila species produces combinations of mbCHCs of different carbon backbone lengths ranging from 24 carbons (2MeC24) to 32 carbons (2MeC32) (Jallon and David, 1987; Khallaf et al, 2021; Wang et al ., 2022). D. melanogaster mainly produces 2MeC24, 2MeC26, and 2MeC28, while D. mojavensis produces longer mbCHCs, 2MeC28, 2MeC30, and 2MeC32 ( Figure 1A ).…”

Section: Resultsmentioning

confidence: 99%

“…The oenocyte driven overexpression of Dmel/mElo and Dmoj/mElo in the D. melanogaster produces mbCHCs of different chain lengths ( Figure 2 ), suggesting that there are differences in protein coding sequences of this gene between the two Drosophila species, and that these differences contribute to the different mbCHCs produced by these two species. Our previous study using ancestral trait reconstruction showed that the last common ancestor of D. melanogaster and D. mojavensis has an mbCHC phenotype that is intermediate between the mbCHCs phenotypes of the two species (Wang et al ., 2022). As mElo controls the length of the longest mbCHCs produced in each of these two species, this suggests that evolutionary changes in this gene may have occurred in both species from the common ancestor, i.e., evolution in this gene led to D. melanogaster to produce shorter mbCHCs and D. mojavensis to produce longer mbCHCs as both species adapt to their environments ( Figure 5B ).…”

Section: Discussionmentioning

confidence: 99%

“…CHC extraction, GC/MS analysis, CHC identification, and quantification were performed as described previously (Wang et al ., 2022). The GC thermal program was set as follows: start from 100 °C, 5 °C/min to 200 °C, and 3 °C/min to 325 °C.…”

Section: Methodsmentioning

confidence: 99%

“…Desiccation assays were performed as described previously (Wang et al ., 2022). Silica gel (S7500-1KG) was ordered from Sigma-Aldrich.…”

Section: Methodsmentioning

confidence: 99%

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Evolution of a fatty acyl-CoA elongase underlies desert adaptation inDrosophila

Wang

Richards

et al. 2023

Preprint

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To survive in extreme environments such as hot-arid deserts, desert-dwelling species have evolved physiological traits to withstand the high temperatures and low aridity beyond the physiologically tolerable ranges of most species. Such traits which include reducing water loss have independently evolved in multiple taxa. However, the genetic and evolutionary mechanisms underlying these traits have thus far not been elucidated. Here we show that Drosophila mojavensis, a fruitfly species endemic to the Sonoran and Mojave deserts, had evolved extremely high desiccation resistance, by producing very long chained methyl-branched cuticular hydrocarbons (mbCHCs) that contributes to a cuticular waterproofing lipid layer reducing water loss. We show that the ability to synthesize these longer mbCHCs is due to evolutionary changes in a fatty acyl-CoA elongase (mElo). CRISPR/Cas9 knockout of mElo in D. mojavensis led to loss of longer mbCHC production and significant reduction of desiccation resistance at high temperatures but did not affect mortality at high temperatures or desiccating conditions individually, indicating that this gene is crucial for desert adaptation. Phylogenetic analysis showed that mElo is a Drosophila specific gene with no clear ortholog outside Diptera. This suggests that while the physiological mechanisms underlying desert adaptation are general, the genetic mechanisms may be lineage-specific.

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Section: Resultssupporting

confidence: 93%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

“…Desiccation assays were performed as described previously (Wang et al ., 2022). Silica gel (S7500-1KG) was ordered from Sigma-Aldrich.…”

Section: Methodsmentioning

confidence: 99%

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Evolution of a fatty acyl-CoA elongase underlies desert adaptation inDrosophila

Wang

Richards

et al. 2023

Preprint

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Colorimetric surface lipid quantification in Drosophila

Yang,

Flaven‐Pouchon,

Cortot

et al. 2024

Arch Insect Biochem Physiol

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Insects are covered with free neutral cuticular hydrocarbons (CHC) that may be linear, branched, and unsaturated and vary in their chain length. The CHC composition is species‐specific and contributes to the adaptation of the animal to its ecological niche. Commonly, CHCs contribute substantially to the inward and outward barrier function of the cuticle and serve pheromonal communication. They are generally determined by gas‐chromatography, a time‐consuming method requiring detailed expertize, but it is not available in many laboratories. Here, we report on the establishment of a colorimetric method allowing semi‐quantitative determination of unsaturated CHCs in Drosophila flies. This method is based on the in vitro reaction of vanillin with double bounds in lipid molecules in an acidic solution to generate a reddish color. We found a robust correlation between gas chromatographic and vanillin‐colorimetric data on unsaturated CHCs amounts in single flies. As the role of unsaturated CHCs in the performance of insects in their environment is only partly understood, we think that this novel method would allow fast and broad analyses of this type of CHCs in insects both in the field and in laboratories and thereby contribute to a substantial improvement in the investigation of this matter.

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Highly diverse cuticular hydrocarbon profiles but no evidence for aggression towards non‐kin in the ambrosia beetle Xyleborinus saxesenii

Melet,

Leibold,

Schmitt

et al. 2024

Ecology and Evolution

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Animal societies use nestmate recognition to protect against social cheaters and parasites. In most social insect societies, individuals recognize and exclude any non‐nestmates and the roles of cuticular hydrocarbons as recognition cues are well documented. Some ambrosia beetles live in cooperatively breeding societies with farmed fungus cultures that are challenging to establish, but of very high value once established. Hence, social cheaters that sneak into a nest without paying the costs of nest foundation may be selected. Therefore, nestmate recognition is also expected to exist in ambrosia beetles, but so far nobody has investigated this behavior and its underlying mechanisms. Here we studied the ability for nestmate recognition in the cooperatively breeding ambrosia beetle Xyleborinus saxesenii, combining behavioural observations and cuticular hydrocarbon analyses. Laboratory nests of X. saxesenii were exposed to foreign adult females from the same population, another population and another species. Survival as well as the behaviours of the foreign female were observed. The behaviours of the receiving individuals were also observed. We expected that increasing genetic distance would cause increasing distance in chemical profiles and increasing levels of behavioural exclusion and possibly mortality. Chemical profiles differed between populations and appeared as variable as in other highly social insects. However, we found only very little evidence for the behavioural exclusion of foreign individuals. Interpopulation donors left nests at a higher rate than control donors, but neither their behaviours nor the behaviours of receiver individuals within the nest showed any response to the foreign individual in either of the treatments. These results suggest that cuticular hydrocarbon profiles might be used for communication and nestmate recognition, but that behavioural exclusion of non‐nestmates is either absent in X. saxesenii or that agonistic encounters are so rare or subtle that they could not be detected by our method. Additional studies are needed to investigate this further.

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Desiccation resistance differences in Drosophila species can be largely explained by variations in cuticular hydrocarbons

Cited by 27 publications

References 85 publications

Evolution of a fatty acyl-CoA elongase underlies desert adaptation inDrosophila

Evolution of a fatty acyl-CoA elongase underlies desert adaptation inDrosophila

Colorimetric surface lipid quantification in Drosophila

Highly diverse cuticular hydrocarbon profiles but no evidence for aggression towards non‐kin in the ambrosia beetle Xyleborinus saxesenii

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