Barnacles offer genetic clues on how organisms adapt to changing environments

By Phoebe Hall, Assistant Director of Communications, Division of Biology and Medicine

Long-term work by a Brown research team on how barnacles thrive in intertidal zones has increasingly wide implications for understanding how other organisms may adapt in the face of climate change.

PROVIDENCE, R.I. [Brown University] – What genes help organisms survive in changing environments? As climate change impacts species across the planet, it’s a big question in basic biology. New research on barnacles may provide some answers.

Barnacles are crustaceans, related to shrimps and crabs. After a brief period when they float freely around the ocean, barnacle larvae attach to a hard surface – a rock, a boat, a whale – and develop into adults. They build hard plates surrounding their bodies, which they can open to feed and to reproduce, and close protectively during low tide and other harsh conditions.

How barnacles not only survive these radically changing habitats, but choose mates and evolve, has fascinated biologists since the days of Charles Darwin, who wrote multiple volumes on the subject.

David Rand
Chair of Ecology and Evolutionary Biology David Rand collects barnacles near the Tjärnö marine station in Bohuslän, Sweden.

“They make a commitment to an environment,” said David Rand, chair of the Department of Ecology and Evolutionary Biology at Brown University. “If they make the wrong decision, they’re dead. If they make the right decision, they reproduce.”

When Rand came to Brown in 1991, he wanted to use barnacles to identify the gene or genes that seem to allow individuals to adapt to high-stress areas – typically the high intertidal zone, which remains dry for hours between high tides. Conversely, he hypothesized, barnacles settled in the low intertidal zone, which is usually underwater, would have different forms of ecologically important genes.

“How do we find a needle in a haystack?” asked Rand, also a professor of natural history and of biology. “Of tens of thousands of genes in a genome, how do we find those genes that are meaningful to climate change, environmental heterogeneity, the Darwinian problem?”

In the 1990s, Rand and graduate student Paul Schmidt – who earned his Ph.D. from Brown in 1999 and is now a professor at University of Pennsylvania – used a technique called classic protein gel electrophoresis to identify a central metabolic protein, mannose-6 phosphate isomerase (Mpi), that allows the barnacle Semibalanus balanoides to survive in its variable habitat. Subsequent researchers in his lab built on that work to identify the structure of the gene encoding the Mpi protein.

They make a commitment to an environment. If they make the wrong decision, they’re dead. If they make the right decision, they reproduce.

David Rand Chair of the Department of Ecology and Evolutionary Biology

Fast-forward a couple of decades, and genome sequencing technology has now caught up with Rand’s original hypothesis – and it’s validated the earlier work. Last month, the newest study from Rand’s research team was published in the Proceedings of the National Academy of Sciences. Led by Brown graduate student Joaquin Nunez, the team reported molecular evidence of natural selection on the Mpi gene in Semibalanus balanoides, confirming the hypothesis that the gene helps the barnacle to survive the extreme changes of the intertidal zone.

Nunez, who joined Rand’s lab nearly five years ago, analyzed the genomic data to tie it together.

“You always build upon the knowledge that’s before you,” Nunez said.

The team showed, at the nucleotide level, that different versions of the Mpi gene are present at different frequencies depending where the barnacles are found in the intertidal zone. The enzyme plays an important role in glycolysis, which converts sugars to energy; one form performs well under high stress, like a hot day at low tide; the other form does better under low stress.

barnacles
Northern acorn barnacles, or semibalanus balanoides, attach to the rocky shore.

The study shows how natural selection enables the barnacles’ survival in this ever-changing environment by maintaining multiple versions of the gene that codes for that enzyme.

The paper also uncovered more information about the structural impact of the gene variant. Nunez found new positions in the protein that the gene encodes, where mutations altered the sequence of the protein and, presumably, its function. Colleagues from Sweden modeled the two versions of the protein, suggesting how they would conform to different environmental stressors. These predicted structures are consistent with the differing Mpi enzyme response to its environment.

Future research, Rand said, could use structural biology to “help us elucidate the structures of those alternative forms and get more of the mechanistic details of how this enzyme works.”

Nunez said they also found hints that Mpi may interact with other proteins, producing new characteristics in stressful events – another potential area of study. Though this paper focuses on the adaptations of this barnacle species, the bigger picture is the biological system in which the barnacle operates, he said.

“A very complex set of things needs to work together for these populations to be healthy and thrive for millennia,” Nunez said. “One of the big predictions of climate change is that many natural populations are going to find themselves in environments that aren’t just hotter or more humid or more stressful, but those environments are going to experience very strong fluctuations.”

fort wetherill
Densely settled barnacles are pictured in the intertidal near Fort Wetherill in Jamestown, Rhode Island.

The intertidal is a “natural laboratory” to understand how species survive and prosper in fluctuating extremes, Nunez said. The same methods that he and Rand used to show how barnacle genes adapt to those extremes could be used by entomologists who want to know how honeybees are adapting to climate change, or crop scientists concerned about productivity in a more stressful environment.

“There are labs all around the world looking for evolutionary approaches to solve this adaptation to climate change,” Rand said.

In addition to Rand and Nunez, other authors from Brown were Patrick Flight, Kimberly Neil, Stephen Rong and David Ferranti. Leif Eriksson, Magnus Alm Rosenblad and Anders Blomberg from the University of Gothenburg also co-authored the paper.

The National Science Foundation (IGERT: DGE-0966060), the National Institutes of Health (2R01GM067862), the Carl Trygger Foundation (CTS 11:14), and the Swedish Research Council (2017-04559, 2014-03914) supported the research. Nunez, Neil and Rong are all NSF Graduate Research Fellows and IGERT Fellows, and Ferranti was supported by a Brown University UTRA Fellowship.

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