Rapid adaptation in fruit flies has evolutionary implications

Photo by Seth Rudman, Washington State University

Think evolution is a slow, gradual process? Tell that to fruit flies.

In a new report in Science, researchers from Washington State University and University of Pennsylvania used a controlled field experiment to show that flies rapidly adapted to shifting environmental conditions with alterations throughout their genome and in a suite of physical characteristics.

Over the four months of the experiment, the researchers documented changes to 60% of the flies’ genome. With this direct observation of swift and continuous adaptation in response to the environment—a phenomenon known as adaptive tracking—the biologists have established a new paradigm for thinking about the timescale of evolution.

“What makes this so exciting is the temporal resolution with which we’re seeing evolutionary processes in real time,” said co-lead author Seth Rudman, an assistant professor at WSU’s School of Biological Sciences in Vancouver.

It’s long been known that evolution can progress quickly in short-lived and fast-reproducing fruit flies. But exactly how fast has remained in question, specifically whether multiple traits could evolve together, continuously, in response to short-term environmental changes.

In earlier studies, the researchers had seen that fruit flies present at the beginning of the growing season were different from those in the late fall in measures of stress tolerance, reproductive fitness, and even pigmentation. But that research couldn’t rule out the possibility that new flies were entering the population.

To more tightly control their studies, the team developed an experimental orchard, where multiple enclosures allowed them to study flies in real-life environmental conditions, while preventing flies from entering or escaping.

The researchers began the current investigation with 1,000 Drosophila melanogasterfruit flies in each of 10 enclosures in July 2014. At the experiment’s peak, each population had grown to roughly 100,000 in number.

Once a month, the team removed individual flies and 2,500 eggs from each enclosure, raised them separately, then analyzed them for six physical characteristics governed by multiple genes, such as reproductive success and cold tolerance.

During these check-ins, the researchers randomly selected 100 flies from each enclosure and sequenced their genomes as a pooled group. This allowed them to get a snapshot of changing allele frequencies—the variations in different points in the genome—over time.

Evidence from the physical and genome data was clear: The flies were evolving, adapting to their environment, and faster than anyone had measured before.

“We see that the populations are able to track differences in the environment,” said senior author Paul Schmidt, a University of Pennsylvania biology professor. “This was not a response to a single, selective event, such as a drought. The populations were constantly evolving and shifting throughout the entire experiment.”

Because flies are short-lived, the weeks between each analysis translated to one to four generations of flies—roughly ten generations over the course of the experiment.

Even so, the magnitude of adaptation was unexpected, with more than 60% of the flies’ genome evolving directly or indirectly during the experiment. Schmidt and Rudman noted that this doesn’t mean evolutionary selection is acting on more than half of the genome—some DNA gets pulled along when other parts change in a process known as “genetic draft.”

The direction of adaptation also changed multiple times, swinging like a pendulum as environmental conditions changed.

“To think that a trait could evolve over a certain number of weeks, and then reverse direction the following month, that was very surprising,” Rudman said. “This paints a picture of adaption and selection being really dynamic. The direction of natural selection is changing, the targets are changing, and they’re changing really quickly.”

Though fruit flies reproduce on a much more compressed time scale than humans, the researchers said their findings have relevance to longer-lived species, like humans.

“I would argue that these processes are taking place in a lot of different organisms, but they’re harder to measure over the appropriate time scales,” said Schmidt. “So, for the fruit flies, the pressures to adapt could come with the seasons, but for humans it could be climate change, agriculture, utilization of milk as a food source. This could be a general phenomenon. The burden is now on us to determine the time scale on which it is occurring."

Publication: SETH M. RUDMAN, et al., Direct observation of adaptive tracking on ecological time scales in Drosophila, Science (2023). DOI: 10.1126/science.abj7484

Original Story Source: Washington State University