Bernstein member involved: Carlotta Martelli

The rate of development of poikilothermic animals, such as insects, fish, and reptiles, is determined by environmental temperature. A research team at Johannes Gutenberg University Mainz (JGU) has recently demonstrated how temperature can affect brain development in fruit flies. “In the area of the brain we examined, neurons formed more synapses and connected to more synaptic partners at lower temperatures,” stated Dr. Carlotta Martelli, head of the team at the Institute of Developmental Biology and Neurobiology of JGU. In their study, the scientists focused on the olfactory circuit of Drosophila melanogaster, because the sense of smell determines important behavioral patterns in these flies and is essential for their survival. They found that the temperature to which the insects are exposed to during the pupal stage has an effect not only on brain development but also on odor-driven behavior.

Metabolic theory for brain wiring at different temperatures

Temperature is the environmental factor with the most extensive impact on the biology of living organisms, as it determines the rates of all biophysical reactions. On the one hand, development is more rapid at higher temperatures while, at the same time, temperature can also have effects on animal behavior. In bees, for example, even small variations in environmental temperature can affect key areas of the brain responsible for learning. A deeper knowledge of the correlations between temperature and development is important to be able to predict the consequences of changes in temperature on the behavior of wild animals, but also to better understand the processes underlying the development of poikilothermic animals, i.e., those with variable body temperatures.

In the case of Drosophila, it was discovered some years ago that the number of synapses between neurons in the visual system increased when the temperature during their development was lower. Dr. Carlotta Martelli’s team now decided to study the insects’ olfactory circuit and determine the effect of different temperatures. For this purpose, flies were developed at either 18 degrees Celsius or 25 degrees Celsius during the pupal stage, i.e., between larval stage and emerged adult insect, which is when brain wiring happens. Martelli and her team used genetic techniques to detect the synaptic partners of a specific type of neuron in the adult fly brain. A count showed that the animals that had developed at 18 degrees Celsius had more than twice as many postsynaptic neurons as those flies that had developed at 25 degrees Celsius. Greater numbers of connections were apparent at all levels of the olfactory circuit in the insects’ brains.

“In order to explain this outcome, we devised a theory based on the assumption that there are slightly divergent metabolic conditions for the growth of the insect body as a whole and the development of the brain,” added Martelli, whose research combines theoretical physics and neurobiology. In other words, the metabolic processes are somewhat different in neurons than in other body cells. Martelli and her team assumed that metabolism is more rapid in the brain at lower temperatures than in the other parts of the body. “We have been able to confirm our theoretical conjectures in other experiments,” Martelli said. However, direct evidence to support this hypothesis regarding the role of metabolism is still lacking. The researchers are currently analyzing the expression of relevant genes during development to find an answer.

Developmental temperature also influences behavior

Furthermore, the researchers reported that if temperature is lowered during the pupal stage, this affects the odor-driven behavior of the adult flies. For the purpose of the experiment, flies aged ten days were exposed to a tiny quantity of butanone, a liquid with a pungent odor that attracts the insects. Flies that developed at 18 degrees Celsius during the pupal phase exhibited greater attraction to this odor than those pupal fruit flies kept at 25 degrees Celsius.

“Although the flies that developed at lower temperature had greater brain connectivity, they did not appear to have better or stronger odor perception,” pointed out Martelli. “Measurements of neuronal activity show that odor representation in that part of the brain that is equivalent to the human olfactory bulb was unchanged. We have thus concluded that behavioral changes could well be attributable to connectivity in downstream areas of the brain that control innate behavior,” concluded Martelli.

The research was financed by the German Research Foundation (DFG) through the FOR5289 and the Institute for Quantitative and Computational Biosciences (IQCB), which was established in early 2024 at Johannes Gutenberg Mainz University. The corresponding article has been published in Science Advances.