Peer reviewed
Experimental study
Animals
How heat and drought threaten fruit fly dehydration defences
Researchers at the Francis Crick Institute have identified a specialised lipid barrier in the fruit fly pupa that protects against dehydration in dry and hot environments. Their findings also expose the lipid barrier's limit, suggesting that insects in some regions of the world may struggle to adapt to climate change.
The fruit fly, or Drosophila, is widely used in research and can provide insights into how insects protect themselves from environmental stresses. Drosophila spends its early days as a larva in a humid environment, feeding and burrowing in decomposing fruit. It then crawls to a drier place and becomes an immobile pupa. The pupa develops into an adult fly through a complex transformation called metamorphosis.
The pupal and adult stages of insects like Drosophila occupy dry land environments and are therefore particularly vulnerable to dehydration. To help prevent this, the adult fruit fly is covered with a barrier of lipid (fat): a hydrophobic coating made of long hydrocarbon molecules that blocks water loss. Until now, researchers didn't know how the pupa protects itself from dehydration or what kind of hydrocarbon barrier it might have.
As many of the known hydrocarbons in Drosophila are similar to those found in crude oil, the team at the Crick analysed them by adapting methods from the petroleum industry and by using state-of-the-art molecular imaging. Published today in Science Advances, these findings revealed a surprise: the pupa doesn't have any hydrocarbons on the surface of its outer body casing (cuticle), whereas the adult has them in abundance. Instead, the pupa's lipid barrier is internal, coating the underside of the cuticle, and it is made of hyper-long hydrocarbons, much longer than those of the adult.
Next, the team traced the origin of the hyper-long hydrocarbons, finding that they are premade by specialised cells in the larva and then stored until needed in the larva's fat reserve. The researchers think that this anticipatory strategy may allow hyper-long hydrocarbons to be deployed very quickly to the underside of the cuticle during the rapid transition from larva to pupa.
Feeling the heat
By looking at the expression of genes involved in producing hydrocarbons, the team identified a specific elongase enzyme that makes hyper-long hydrocarbons. However, removing this enzyme in standard laboratory conditions didn't have a huge impact, suggesting that other elongase enzymes also contribute to the production of hyper-long hydrocarbons.
The researchers then recreated high temperature and low humidity conditions, similar to those of some subtropical and mediterranean climates. Exposure of the pupa to this environment significantly decreased its water content but, without the hyper-long elongase enzyme, dehydration almost doubled to a level incompatible with survival.
An evolutionary tug-of-war
The hydrocarbons of the lipid barrier also function as sex pheromones, air-borne chemical signals that flies use as mating cues. Long hydrocarbons best protect against dehydration but short ones evaporate into the air more easily and are better suited as sex pheromones. So pupae, which have yet to sexually mature, make hyper-long hydrocarbons to prevent water loss, whereas adult flies have settled on a medium length compromise to satisfy both the barrier and pheromone functions.
However, the team found that a desert species of fruit fly called Drosophila mojavensis retains hyper-long hydrocarbons as an adult, instead of switching to shorter ones like other Drosophila species. In a desert environment, an optimal barrier to dehydration may be more important for survival than air-borne sex pheromones. It is likely that D. mojavensis uses other mating signals such as contact or visual cues.
Lena Lampe, postdoctoral researcher in the Physiology and Metabolism Laboratory at the Crick, and co-first author, said: "We've identified a key enzyme that ensures the development of a specific lipid barrier in the pupa that protects it from water loss in hot and arid conditions. However, Drosophila has its survivable environmental limits and our studies of this enzyme have helped to define these."
Clare Newell, Principal Laboratory Research Scientist in the Physiology and Metabolism Laboratory at the Crick, Visiting Scientist at the National Physical Laboratory (NPL), and co-first author, said: "The immobile pupa is a particularly vulnerable stage in development, as it can't simply move to another environment if it's too hot or dry. It's fascinating that the larva prepares for this challenge before metamorphosis, building a resource of hyper-long hydrocarbons. Embracing techniques normally used outside biology helped us to reveal one of the many hidden secrets of metamorphosis."
Alex Gould, Group Leader of the Physiology and Metabolism Laboratory, and senior author, said: "Insects are vital to life on Earth, pollinating three-quarters of global food crop species. With the backdrop of human-induced climate change, it's important to understand the resilience of insects to increases in aridity and temperature. We hope that this work in Drosophila will inspire similar research in other insect species, including those that play an important role in our food chains."
The research involved collaboration with the Metabolomics team and the Fly Facility at the Crick, Ian Gilmore at the National Centre of Excellence in Mass Spectrometry Imaging at the National Physical Laboratory and Li Zhao at the Laboratory of Evolutionary Genetics and Genomics at The Rockefeller University.
