Evolution in Real Time: Scientists predict and witness evolution in a 30-year marine snail experiment

In 1988, the Koster archipelago, a group of islands off the Swedish west coast near the border to Norway, was hit by a particularly dense bloom of toxic algae, wiping out marine snail populations. It turns out that this event would open up the opportunity to predict and see evolution unfolding before our eyes.

Before this event, the islands and their small intertidal skerries—rocky islets—were home to dense and diverse populations of marine snails of the species Littorina saxatilis. While the snail populations of the larger islands were restored within two to four years, several skerries could not seem to recover from this harsh blow. Amid these events, marine ecologist Kerstin Johannesson from the University of Gothenburg, Sweden, saw a unique opportunity. In 1992, she re-introduced L. saxatilis snails to their lost skerry habitat—starting an experiment that would have far-reaching implications more than 30 years later. 

This 30-year experiment now allowed an international collaboration led by researchers from the Institute of Science and Technology Austria (ISTA), Nord University, Norway, the University of Gothenburg, Sweden, and The University of Sheffield, UK, together with researchers from the University of Sussex, UK, and from BIOPOLIS-CIBIO/InBIO in Portugal, to predict and witness evolution in the making.

Littorina saxatilis is a commonly known species of marine snails found throughout the North Atlantic shores, where different populations evolved traits adapted to their environments. These traits include size, shell shape, shell color, and behavior. The differences among these traits are particularly striking between the so-called Crab- and Wave-ecotype. These snails have evolved repeatedly in different locations, either in environments exposed to crab predation or on wave-exposed rocks away from crabs. Wave snails are typically small, and have a thin shell with specific colors and patterns, a large and rounded aperture, and bold behavior. Crab snails, on the other hand, are strikingly larger, have thicker shells without patterns, and a relatively smaller and more elongated aperture. Crab snails also behave more warily in their predator-dominated environment.

The Swedish Koster archipelago is home to these two different L. saxatilis snail types, often found on the same island or only separated by a few hundred meters across the sea. Before the toxic algal bloom, Wave snails inhabited the skerries, while nearby shores were home to both Crab and Wave snails. This close spatial proximity would prove crucial.

Seeing that the Wave snail population of the skerries was entirely wiped out due to the toxic algae, Johannesson decided in 1992 to reintroduce snails to one of these skerries, but of the Crab-ecotype. Because the new habitat was previously home to Wave snails, she rightfully expected the transplanted Crab snails to adapt to their new environment by evolving Wave-specific traits. With 1 to 2 generations each year, the snails’ evolution would likely happen right before scientists’ eyes. 

"We saw evidence of the snails’ adaptation already within the first decade of the experiment,” says Diego Garcia Castillo, a graduate student at ISTA, one of the authors leading the study. "Over the experiment’s 30 years, we were able to predict robustly what the snails will look like and which genetic regions will be implicated. And the transformation was both rapid and dramatic” he adds.

However, the snails did not evolve these traits entirely from scratch. Co-corresponding author Anja Marie Westram, currently a researcher at Nord University, explains, "Some of the genetic diversity was already available in the starting Crab population but at low prevalence. This is because the species had experienced similar conditions in the recent past. The snails’ access to a large gene pool drove this rapid evolution.”

The team examined three aspects over the years of the experiment: the snails’ phenotype, individual gene variabilities called "single nucleotide polymorphisms” or "SNPs”, and larger genetic changes affecting entire regions of the chromosomes, called "chromosomal inversions”, a segment of chromosome that flips 180º, which happens to be the main topic of the BIOPOLIS-CIBIO/InBIO co-author of this study, Rui Faria.

In the first few generations, the researchers witnessed an interesting phenomenon called "phenotypic plasticity”. Very soon after their transplantation, the snails modified their shape to adjust to their new environment while their genetic material remained unchanged. But the population also quickly started to change genetically. The researchers could predict the extent and direction of the genetic changes, especially for the chromosomal inversions. "Chromosomal inversions were first discovered roughly 100 years ago but only now we start to fully understand their relevance in adaptation and speciation”, says Rui Faria.

The authors showed that the snails’ rapid and dramatic transformation was possibly due to two complementary processes: A fast selection of traits already present at a low frequency in the transplanted Crab snail population and likely gene flow from neighboring Wave snails that could have simply rafted over 160 meters to reach the skerry.

In theory, scientists know that a species with high enough genetic variation can adapt more rapidly to change. However, few studies aimed to experiment with evolution over time in the wild. "This work allows us to have a closer look at repeated evolution and predict how a population could develop traits that have evolved separately in the past under similar conditions,” says Garcia Castillo.

The team this work will drive further research on maintaining species with large and diverse genetic makeups to learn how species to modern environmental challenges such as pollution and climate change. "Perhaps this research helps convince people to protect a range of natural habitats so that species do not lose their genetic variation,” Westram concludes. "This is a very important point” adds Rui Faria. "In terms of conservation, the community often focus on avoiding species extinction but our efforts should be anticipated to maintain the adaptive potential of populations by conserving different habitats and let the evolutionary processes naturally follow their path”.

Rui Faria, who just started a research group at CIBIO (SEAGEN- Seascape Genomics and Speciation) that combines population genomics and molecular ecology to understand adaptation and speciation in marine environments, conludes: "Importantly, this study also shows that we need more such long-term research projects to fully understand evolutionary processes in natural populations and how they shape biodiversity, in order to be able to predict more realistically the impacts of global warming. This is often not possible due to funding restrictions and the need for short-term quick scientific returns that scientists face nowadays, particularly in Portugal. As an international team, we are trying to overcome these challenges and will try to continue implementing longer-term evolutionary experimental studies in this fantastic model system (Littorina marine snails).”

Diego Garcia Castillo, Nick Barton, Rui Faria, Jenny Larsson, Sean Stankowski, Roger Butlin, Kerstin Johannesson, and Anja M. Westram. 2024. Predicting rapid adaptation in time from adaptation in space: A 30-year field experiment in marine snails. Science Advances.
DOI: 10.1126/sciadv.adp2102

Image 1: Two ecotypes of Littorina saxatilis marine snails, adapted to different environments. The Crab ecotype (left) is larger and wary of predators. The Wave ecotype (right) is smaller and has bold behavior. © David Carmelet

Image 2: From the shore to the little black dot in the sea. The donor shore of the transplanted snail population (foreground) and the experimental skerry (little dot in the sea to the right). © Kerstin Johannesson

Image 3: The experimental skerry in the Koster archipelago off the Swedish west coast. Crab-ecotype L. saxatilis snails were brought here in 1992 after toxic algae wiped out the original Wave-ecotype population. © Kerstin Johannesson