Evolution can't keep up with rapidly changing environments

When evolution chases change and never quite catches up, surprising things happen at the level of DNA.

A new theory from researchers at the University of Michigan (UM) suggests that genes constantly try to keep pace with shifting environments, yet many changes that survive still look neutral on the surface.

For decades, many biologists leaned on the neutral theory, the idea that most DNA changes do not affect an organism’s chances to survive or reproduce.

That picture is now being challenged by work showing that useful genetic changes are common, but the world around organisms can change so quickly that these advantages rarely spread through an entire population.

How neutral changes work

In the late 1960s, Motoo Kimura published a paper arguing that most changes in DNA are neutral and spread by random chance rather than selection.

That idea helped explain why sequences in different species often change at a steady pace, a pattern called the molecular clock, a roughly constant rate of genetic change over long stretches of time.

The UM study was led by Jianzhi Zhang, an evolutionary biologist who studies how genomes respond to natural selection in changing environments.

The research revisits this long-standing picture using huge datasets from microbes such as yeast and E. coli.

The team set out to investigate how often a beneficial mutation, a DNA change that boosts an organism’s success in its current conditions, really appears. The team found that more than one percent of tested changes are helpful.

Watching evolution happen

To estimate these effects, the experts relied on deep mutational scanning, an approach where thousands of versions of a gene are built and tested to see how each one changes growth.

Each version carries a different mutation, and scientists track which versions become more or less common over many generations.

Earlier work from the same group used this approach on 21 genes from budding yeast and showed that even so called silent changes in DNA often affect growth, in a large dataset that mapped how thousands of mutations shifted performance.

That project and related efforts made clear that many mutations once labeled harmless can nudge cells up or down in success.

Testing evolution in the lab

To resolve this puzzle, the study turned to evolution experiments where microbes grow for hundreds of generations in controlled conditions.

One set of yeast populations evolved in a single nutrient rich medium for about 800 generations, while another set moved through ten different media, spending around 80 generations in each before conditions changed.

In the constant environment, many helpful mutations spread widely, because conditions stayed favorable long enough for their advantages to matter.

In the shifting environment, helpful changes still appeared, but conditions changed before those mutations could reach everyone, and some advantages flipped into disadvantages as soon as nutrients or stresses switched.

Evolution in a changing environment

The team describes this pattern using antagonistic pleiotropy, a situation where one mutation helps in some conditions but harms in others.

The researchers combined this method with adaptive tracking, ongoing genetic adjustment as environments change over time, to build a model in which populations are always trying to catch up but rarely settle into a perfect fit.

“We’re saying that the outcome was neutral, but the process was not neutral,” said Jianzhi Zhang, U-M professor of ecology and evolutionary biology.

He argues that natural populations are usually chasing moving targets rather than sitting at a perfect match with their surroundings.

Why good changes fail

One key part of the story is time. A beneficial mutation does not sweep through even a fast growing microbial population instantly, because it has to arise, avoid being lost by chance, and then increase generation after generation.

For a typical advantage, theory shows that fixation can take thousands of generations in a population with a realistic effective population size – the number of individuals that actually contribute genes to future generations.

Environmental conditions often shift on similar or even shorter timescales, especially in nature, where changes in temperature, nutrients, or competitors can happen quickly.

Long running experiments with E. coli have shown that adaptation continues even after 50,000 generations in a constant laboratory environment, as seen in one detailed analysis. 

Those results suggest that fully fine tuned adaptation takes a very long time even when conditions barely change, which makes such perfect tuning even less likely in the wild.

In the new model, most of the beneficial mutations that appear are specific to the current conditions and will become harmful if the environment changes in the wrong direction.

Only a very small fraction of changes are helpful across many conditions, and those rare winners may already be fixed, leaving the rest of the genome cycling through successes that never quite last.

Human evolution in modern environments

The idea of adaptive tracking also reshapes how to think about how well species match their present-day environments. 

“Some mutations may be beneficial in our old environments, but are mismatched to today,” said Jianzhi Zhang, U-M professor of ecology and evolutionary biology.

Field work supports this picture in animals that live through strong seasonal swings. In fruit flies, researchers have watched genetic variants rise in frequency in the summer and then fade by late fall, while other variants do the opposite.

In this view, many natural populations are only partly adapted at any given moment. Their genes reflect a tug of war between past conditions that favored certain combinations and new conditions that reward different ones.

Humans add another twist, because culture and technology can change environments far faster than genes can follow.

Modern diets, urban life, and medical care differ sharply from the settings where many of our traits first became common. This may help explain why some genetic variants that once helped with survival now contribute to disease.

Questions for future research

Most of the data behind the new model come from unicellular organisms, which are easier to grow in huge numbers and mutate systematically.

A major next step is to see whether similar patterns of frequent, environment specific benefits and antagonistic pleiotropy hold in multicellular organisms, including plants and animals.

For many researchers, neutral models remain useful tools, but they may be hiding a busy layer of short term advantages and reversals that never show up in long term averages, a view that still underpins much of how genetic data are interpreted.

Understanding that hidden motion could change how evolution is interpreted in areas from conservation to medicine.

The study is published in the journal Nature Ecology and Evolution.

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