Tiny, cold-blooded animals like flies depend on their environment to regulate body temperature, making them ideal "canaries in the mine" for gauging the impact of climate change on the behavior and distribution of animal species. Yet, scientists know relatively little about how insect sense and respond to temperature.
Using two species of flies from different climates - one from the cool, high-altitude forests of Northern California, the other hailing from the hot, dry deserts of the Southwest (both cousins of the common laboratory fly, drosophila melanogaster) - Northwestern University scientists discovered remarkable differences in the way each processes external temperature.
Forest flies showed increased avoidance of heat, potentially explained by higher sensitivity in their antennae's molecular heat receptors, while desert flies were instead actively attracted to heat, a response that could be tracked to differences in brain wiring in a region of the fly brain that helps compute the valence (inherent attractiveness or aversiveness) of sensory cues.
The scientists believe these two mechanisms may have accompanied the evolution of each species as it adapted to its distinctive thermal environment, starting from a common ancestor dating back 40 million years (not long after dinosaurs went extinct).
These findings, published today (March 5) in the journal Nature, help understand how animals evolve the preferences for specific temperature environments and may help predict the impact of a rapidly changing climate on animal behavior and distribution.
'Not enough people care about insects'
"Insects are especially threatened by climate change," said Northwestern neurobiologist Marco Gallio. "Behavior is the first interface between an animal and its environment. Even before the struggle to survive or perish, animals can respond to climate change by migration and by changing their distribution. We are already seeing insect populations declining in many regions, and even insect vectors of disease like the Zika virus and malaria spreading into new areas."
Gallio, a self-appointed "insect advocate," is a professor in the neurobiology department and the Soretta and Henry Shapiro Research Professor in Molecular Biology at the Weinberg College of Arts and Sciences. His lab examines fruit flies and their sensing systems. Gallio acknowledged there is limited data because "not enough people care about the insects," but that available figures record a dramatic decline in insects in the past 20 to 50 years. Though bug haters may rejoice, Gallio said the population decline in the animal group with the most species on Earth is nothing to celebrate.
In addition to their position at the foundation of most terrestrial food chains, insects pollinate 70% of our crops. Gallio said losing insect communities could cause catastrophic damage to ecosystems across the globe and have a direct impact on human wellbeing.
Understanding heat circuits in the brain
Previous work from the Gallio Lab focused on how small insects like laboratory flies respond to sensory cues like harmless and painful temperature changes.
"The common fruit fly is an especially powerful animal to study how the external world is represented and processed within the brain," Gallio said. "Many years of work on fly genetics and neuroscience have given us a map of the fly brain more detailed than that of any other animal."
In the present study, Gallio and colleagues wondered how the brain circuits and resulting behaviors compared in fly species that were very similar aside from their choices of thermal habitat.
Using genetic tools, including CRISPR, to knock out certain genes and gene swaps between species, the team studied both the molecular and brain mechanisms that may explain species-specific differences in temperature preference.
Ph.D. student and lead author Matthew Capek explained that they first found differences in the molecules that detect heat, causing them to activate at different temperatures. And while Capek said the difference in activation could explain the forest flies' preference for cooler environments, a shift in receptor activation was not enough to explain the behavior of the desert fly.
"The desert fly seemed actively attracted to warmer temperatures - around 90 degrees Fahrenheit compared to the forest fly's sweet spot just below 70 degrees," said Capek, who works in the Gallio lab. "In fact, the activation threshold of the antenna heat sensors corresponded to their favorite temperature range, which they will seek, rather than to a temperature they should avoid."
"In other words, the fly doesn't behave any longer as though the antennae are telling it to run away from dangerous heat; they seem to be telling it higher temperatures are good, and to approach them."
High cost, high reward
Gallio was initially puzzled - deserts are hot, so it did not make sense that flies sought out heat - but a lab trip to the Anza Borrego desert of Southern California provided key inspiration.
"Deserts in this region are very hot during the day, but temperatures can drop extremely rapidly when the sun goes down, and night can be downright freezing," said Alessia Para, also a key author of the study and a research associate professor of neurobiology. "Flies in this climate may need to constantly attend to the rapidly changing temperature and always seek the ideal range, finding shady spots during the day and hiding in cacti for warmth at night."
Flies from more forgiving environments may instead ignore temperature except when it changes rapidly. Constantly detecting the right temperature is costly from an energy perspective, but for desert flies, it's life or death.
"This comparative work is useful in a couple of different ways," Gallio said. "When an animal is born, the brain is already programmed to know if many of the things it will encounter are bad or good for it, and we do not understand how that programming works.
These fly species represent a natural experiment because a stimulus that is good for one species is bad for the other, and we can study the differences that make it so. We also want to learn more about how animals have been able to adapt to different temperatures during evolution, so that we may be able to better understand and even predict how they react to ongoing climate change. Of course we care about the insects, and we hope that what we learn may help us appreciate and protect them better."
The paper, titled "Evolution of temperature preference behavior in flies of the genus drosophila," was funded by the National Institutes of Health (grants R21NS130554 and 1F31NS129270) and by the PEW Scholars Program. Gallio is a member of the National Science Foundation's Simons National Institute for Theory and Mathematics in Biology in Chicago.
