Developmental sleep reallocation enables metabolic adaptation in desert flies

Joint Public review:

Summary

This interesting work by Shuhao Li and colleagues suggests that developmental sleep and feeding behavior in larval flies is genetically programmed to prepare the animal for adult contingencies, such as in the case of flies living in harsh ecological environments, such as deserts. Thus, the work proposes that desert-dwelling flies such as Drosophila mojavensis sleep less and feed more than D. melanogaster as larvae, which allows them to feed less and sleep more as adults in the harsh desert conditions where they live. The authors argue that this is evidence for developmental sleep reallocation, which helps the adult flies survive in the desert. In general, their results support this compelling hypothesis, so this work provides a new perspective on how sleep might be differentially programmed across developmental stages according to the requirements of an ecological niche. This work is particularly innovative for several reasons. First, it extends the Drosophila sleep field beyond D. melanogaster and directly addresses questions about the evolution of sleep that remain largely unexplored. Second, it investigates the possibility that changes in sleep across development may be adaptive, rather than sleep being a static trait. Overall, this work opens new avenues of research, effectively bridges the fields of sleep biology and evolutionary ecology, and should be of broad interest to a general readership. The manuscript is scientifically sound and clearly written for a generalist audience.

There are, however, two important weaknesses that should be addressed. The first is the implicit assumption that all observed behavioral differences are adaptive; this would benefit from a more cautious framing. Second, the manuscript would be strengthened by a more detailed discussion, and potentially additional data, regarding the ecological differences experienced by D. mojavensis and D. melanogaster at distinct life-cycle stages.

Strengths:

(1) The study astutely uses desert Drosophila species as models to understand how sleep is optimized in a challenging environment. The manuscript is rigorous, experiments are well controlled, the work is very clearly presented, and the results support the main conclusions, which are quite exciting.

(2) The manuscript examines previously unexplored sleep differences in a non-melanogaster species.

(3) The study provides evidence that selective pressure can be restricted to specific developmental stages.

(4) This work offers evolutionary insights into the trade-offs between sleep and feeding across development.

Weaknesses

(1) The authors should soften interpretations so that it is not assumed that any observed difference between mojavensis and melanogaster is necessarily adaptive, or evolved due to food availability or temperature stress.

(2) The study relies on comparisons and correlations. While it seems likely that the observed differences in sleep explain the increased food consumption and energy storage in the larvae of desert flies, demonstrating this through sleep manipulation would strengthen the authors' conclusions.

(3) The question arises regarding whether transiently quiescent larvae are always really sleeping, and whether it is appropriate to treat sleep as a stochastic population-level phenomenon rather than as an individual trait.

(4) The manuscript would benefit from comparative analysis beyond mojavensis and melanogaster.

(5) A deeper discussion of the ecological differences between the 2 Drosophila species would place the results in a broader context.

(6) The feeding parameters used in adults and larvae measure different aspects of feeding, confounding comparisons.