Collective Worm and Robot “Blobs” Protect Individuals, Swarm Together - Georgia Tech News Center

Posted: 10 Feb 2021 12:14 PM PST

Earth and Environment Science and Technology

Collective Worm and Robot "Blobs" Protect Individuals, Swarm Together

February 10, 2021 • Atlanta, GA

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Individually, California blackworms live an unremarkable life eating microorganisms in ponds and serving as tropical fish food for aquarium enthusiasts. But together, tens, hundreds, or thousands of the centimeter-long creatures can collaborate to form a "worm blob," a shape-shifting living liquid that collectively protects its members from drying out and helps them escape threats such as excessive heat. (Credit: Christopher Moore and Brice Zimmerman, Georgia Tech)

While other organisms form collective flocks, schools, or swarms for such purposes as mating, predation, and protection, the Lumbriculus variegatus worms are unusual in their ability to braid themselves together to accomplish tasks that unconnected individuals cannot. A new study reported by researchers at the Georgia Institute of Technology describes how the worms self-organize to act as entangled "active matter," creating surprising collective behaviors whose principles have been applied to help blobs of simple robots evolve their own locomotion.

The research, supported by the National Science Foundation and the Army Research Office, was reported Feb. 5 in the journal Proceedings of the National Academy of Sciences. Findings from the work could help developers of swarm robots understand how emergent behavior of entangled active matter can produce unexpected, complex, and potentially useful mechanically driven behaviors.

Collective Behavior in Worms

The spark for the research came several years ago in California, where Saad Bhamla was intrigued by blobs of the worms he saw in a backyard pond.

"We were curious about why these worms would form these living blobs," said Bhamla, an assistant professor in Georgia Tech's School of Chemical and Biomolecular Engineering. "We have now shown through mathematical models and biological experiments that forming the blobs confers a kind of collective decision-making that enables worms in a larger blob to survive longer against desiccation. We also showed that they can move together, a collective behavior that's not done by any other organisms we know of at the macro scale."

Such collective behavior in living systems is of interest to researchers exploring ways to apply the principles of living systems to human-designed systems such as swarm robots, in which individuals must also work together to create complex behaviors.

"The worm blob collective turns out to have capabilities that are more than what the individuals have, a wonderful example of biological emergence," said Daniel Goldman, a Dunn Family Professor in Georgia Tech's School of Physics, who studies the physics of living systems.

Why the Worms Form Blobs

The worm blob system was studied extensively by Yasemin Ozkan-Aydin, a research associate in Goldman's lab. Using bundles of worms she originally ordered from a California aquarium supply company – and now raises in Georgia Tech labs – Ozkan-Aydin put the worms through several experiments. Those included development of a "worm gymnasium" that allowed her to measure the strength of individual worms, knowledge important to understanding how small numbers of the creatures can move an entire blob.

She started by taking the aquatic worms out of the water and watching their behavior. First, they individually began searching for water. When that search failed, they formed a ball-shaped blob in which individuals took turns on the outer surface exposed to the air where evaporation was taking place – behavior she theorized would reduce the effect of evaporation on the collective. By studying the blobs, she learned that worms in a blob could survive out of water 10 times longer than individual worms could.

"They would certainly want to reduce desiccation, but the way in which they would do this is not obvious and points to a kind of collective intelligence in the system," said Goldman. "They are not just surface-minimizing machines. They are looking to exploit good conditions and resources."

Using Blobs to Escape Threats

Ozkan-Aydin also studied how worm blobs responded to both temperature gradients and intense light. The worms need a specific range of temperatures to survive and dislike intense light. When a blob was placed on a heated plate, it slowly moved away from the hotter portion of the plate to the cooler portion and under intense light formed tightly entangled blobs. The worms appeared to divide responsibilities for the movement, with some individuals pulling the blob while others helped lift the aggregation to reduce friction.

As with evaporation, the collective activity improves the chances of survival for the entire group, which can range from 10 worms up to as many as 50,000.

"For an individual worm going from hot to cold, survival depends on chance," said Bhamla. "When they move as a blob, they move more slowly because they have to coordinate the mechanics. But if they move as a blob, 95% of them get to the cold side, so being part of the blob confers many survival advantages."

A Worm Gymnasium

The researchers noted that only two or three "puller" worms were needed to drag a 15-worm blob. That led them to wonder just how strong the creatures were, so Ozkan-Aydin created a series of poles and cantilevers in which she could measure the forces exerted by individual worms. This "worm gymnasium" allowed her to appreciate how the pullers managed to do their jobs.

"When the worms are happy and cool, they stretch out and grab onto one of the poles with their heads and they pull onto it," Bhamla said. "When they are pulling, you can see the deflection of the cantilever to which their tails were attached. Yasemin was able to use known weights to calibrate the forces the worms create. The force measurement shows the individual worms are packing a lot of power."

Some worms were stronger than others, and as the temperature increased, their willingness to work out at the gym declined.

Applying Worm Principles to Robots

Ozkan-Aydin also applied the principles observed in the worms to small robotic blobs composed of "smart active particles," six 3D-printed robots with two arms and two sensors allowing them to sense light. She added a mesh enclosure and pins to arms that allowed these "smarticles" to be entangled like the worms and tested a variety of gaits and movements that could be programmed into them.

"Depending on the intensity, the robots try to move away from the light," Ozkan-Aydin said. "They generate emergent behavior that is similar to what we saw in the worms."

She noted that there was no communication among the robots. "Each robot is doing its own thing in a decentralized way," she said. "Using just the mechanical interaction and the attraction each robot had for light intensity, we could control the robot blob."

By measuring the energy consumption of an individual robot when it performed different gaits (wiggle and crawl), she determined that the wiggle gait uses less power than the crawl gait. The researchers anticipate that by exploiting gait differentiation, future entangled robotic swarms could improve their energy efficiency.

Expanding What Robot Swarms Can Do

The researchers hope to continue their study of the collective dynamics of the worm blobs and apply what they learn to swarm robots, which must work together with little communication to accomplish tasks that they could not do alone. But those systems must be able to work in the real world.

"Often people want to make robot swarms do specific things, but they tend to be operating in pristine environments with simple situations," said Goldman. "With these blobs, the whole point is that they work only because of physical interaction among the individuals. That's an interesting factor to bring into robotics."

Among the challenges ahead are recruiting graduate students willing to work with the worm blobs, which have the consistency of bread dough.

"The worms are very nice to work with," said Ozkan-Aydin. "We can play with them and they are very friendly. But it takes a person who is very comfortable working with living systems."

The project shows how the biological world can provide insights beneficial to the field of robotics, said Kathryn Dickson, program director of the Physiological Mechanisms and Biomechanics Program at the National Science Foundation.

"This discovery shows that observations of animal behavior in natural settings, along with biological experiments and modeling, can offer new insights, and how new knowledge gained from interdisciplinary research can help humans, for example, in the robotic control applications arising from this work," she said.

This research was supported by the National Science Foundation (NSF) under grants CAREER 1941933 and 1817334 and the Army Research Office under grant W911NF-11-1-0514. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the sponsoring agencies.

CITATION: Yasemin Ozkan-Aydin, Daniel I. Goldman, and M. Saad Bhamla, "Collective dynamics in entangled worm and robot blobs. (Proceedings of the National Academy of Sciences, 2021). https://doi.org/10.1073/pnas.2010542118

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Fish had the genes to adapt to life on land—while they were still swimming the seas - Science Magazine

Posted: 10 Feb 2021 12:30 PM PST

This illustration from a 14th century Dutch encyclopedia of animal life shows scientists have been thinking about the fin to limb transition for centuries.

Der naturen bloeme/Nationale Bibliotheek

By Elizabeth PennisiFeb. 10, 2021 , 3:30 PM

Almost 700 years ago, Jacob van Maerlant, a Dutch poet, envisioned a fish all set for life on land: It had sprouted arms to hoist itself ashore. Now, three genetic studies make his fantasy look remarkably prescient. Together, the studies suggest that in terms of genes, the aquatic precursors of four-limbed land animals, or tetrapods, were as well-prepared as the Dutch fantasy fish. They were pre-equipped with genes that could be turned to making limbs, efficient air-breathing lungs, and nervous systems tuned to the challenges of life on land.

"All these studies tell us that the origin of tetrapods was something waiting to happen," says Borja Esteve-Altava, an evolutionary biologist at Pompeu Fabra University in Barcelona, Spain. Genetically, "Everything necessary was already there" before vertebrates came ashore, nearly 400 million years ago.

Fossils reveal the outlines of the story. Fish with fleshy fins supported at their base by a single bone, known as lobe-finned fish, moved into shallow water about 375 million years ago. About 5 million years later, some of those lobe fins crawled onto terra firma. The first fish to set fin on land must have already had at least some of the physical traits and genetic modifications needed to do so, but researchers hadn't worked out how and when they became equipped for the change. "The big question of how such a large morphological shift actually occurred remains very much in play," says Peter Currie, an evolutionary developmental biologist at Monash University.

In the trio of studies published last week in Cell, genes in living fish took the place of fossils as a way to peer back in time. One set of clues came from studies of mutagenized zebrafish, a favorite model for studying development. M. Brent Hawkins, then a Harvard University graduate student and now a postdoc, was shocked to discover zebrafish mutants with two bones resembling the forelimb bones of land animals in their front fins, complete with muscles, joints, and blood vessels. The finding is "quite spectacular," says Marie-Andrée Akimenko, a developmental biologist at the University of Ottawa.

Two mutated genes, vav2 and waslb, were responsible for the transformation. Both genes code for proteins that are part of a pathway controlling the activity of Hox11 proteins, regulatory molecules that guide the formation of the two forearm bones in mammals, among other functions. In fish, other proteins normally suppress Hox11 and prevent the formation of those bones. But the mutations, which Hawkins re-created using the gene editor CRISPR, reactivate the pathway. The "landmark" finding is "changing the paradigm on limb development and evolution," says Renata Freitas, a developmental biologist at the University of Porto in Portugal.

Other genetic clues come from living representatives of ancient fish lineages. Only two groups of the lobe-finned fish are alive today: lungfish and coelacanths. About 400 million years ago, they diverged from the line of lobe-finned fish that gave rise to tetrapods 30 million years later. Today's oceans are mostly populated with species from another group that originated about 420 million years ago: the ray-finned fish, so named because their fins are supported by slender spines.

Evolutionary geneticists Guojie Zhang at the University of Copenhagen and Wen Wang of Northwestern Polytechnical University in Xi'an, China, and their colleagues sequenced the genomes of the African lungfish, which branched off early from other lobe-finned fish. The researchers also sequenced the bichir, an elongated, air-breathing, ray-finned fish that lives in the shallows of tropical African rivers, as well as the American paddlefish, the bowfin, and the alligator gar. All are ray-finned fishes that evolved much earlier than teleosts, the group that dominates the world's waters today (see diagram, below). Knowing when each of those lineages branched away from others, the researchers could infer when and where certain genes first appeared on the fish family tree.

The long swim to land

The groundwork for terrestrial traits like limbs and lungs was laid deep in the fish family tree. Genes for such traits found in both lobe-finned and ray-finned fishes must also have been present in their common ancestor.

X. BI ET AL., CELL, 2021, DOI.ORG/10.1016/J.CELL.2021.01.046, ADAPTED BY N. DESAI/SCIENCE

None of the sequenced fish is on the precise branch that led to tetrapods. Yet all have much of the genetic equipment needed for life on land, including most of the genes and regulatory DNA needed to build limbs. For example, all the fish sequenced have a regulatory element that helps form synovial joints, which make fins and limbs flexible and are essential for terrestrial locomotion. The fish also have 11 genes that are needed to build lungs and that work the same way in the bichir's lungs as they do in humans. One is for a pulmonary surfactant, a lubricating secretion that helps lungs expand and contract. Both the ray-finned fishes and the lobe-finned lungfish also apparently have a regulatory element that helps shape the right ventricle of the heart to deliver oxygen more efficiently.

The findings show that "a lot of things we think are just in land animals are also in fish," says Gage Crump, a developmental biologist at the University of Southern California. Finding all those genes in both lobe-finned and ray-finned fish means those genetic pathways must have been present in their common ancestor, some 425 million years ago. "It is surprising that some of these elements are so conserved for such a long evolutionary time," Zhang says. (Teleosts, in contrast, have lost much of the DNA that prepared early fish for life on land, apart from the Hox11 pathway, the team reported.)

The genome of the lungfish offers a glimpse of later adaptations along the path to terrestrial life. It includes additional pulmonary surfactant genes that the ray-finned fishes lack, as well as DNA for specifying five toes, connecting nerves to limb muscles, and for sensitizing the brain to react fast. All those genes were previously thought to be unique to tetrapods.

Putting it all together, Wang and Zhang think the transition to land involved three key steps. The ability to breathe air occasionally appeared in the common ancestor to ray-and lobe-finned fish, about 425 million years ago. Then surfactant genes, new nervous system genes, and other innovations enabled lobe-finned fish to leave the water temporarily. Finally, after the African lungfish split off from the lobe fins, the common ancestor of land vertebrates acquired other respiratory and locomotive refinements needed to live out of water.

Rather than building new structures and genetic pathways just when vertebrates moved onto land, evolution apparently was thrifty, using existing genes to adapt to the opportunities offered by terrestrial habitats. "[The studies] show the extent to which the fish-tetrapod transition was achieved by modifying existing molecular systems, rather than creating new ones," says Per Ahlberg, a paleontologist at Uppsala University.

Gaps still remain in understanding how fish made landfall, but the new studies "bring us closer to the living biology of the fish-tetrapod transition," Ahlberg adds. Van Maerlant would be pleased.

*Update, 10 February, 12:30 p.m.: This story, first published on 4 February, has been updated to include information on two additional papers using genomics to understand how vertebrates adapted to life on land.

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