Water-land transition in the early tetrapods

The transition from water to land is one of the most important and stimulating major transitions in vertebrate evolution. And the question of how and when tetrapods moved from water to land has long been a source of wonder and scientific debate.

Early ideas speculated that drained pools of water had stranded the fish on land and that being out of the water provided the selective pressure to evolve more limb-like appendages back to the water. In the 1990s, recently discovered specimens suggested that early tetrapods retained many aquatic features, such as gills and a tail fin, and that limbs may have evolved in water before tetrapods adapted to life on land. However, there is still uncertainty about when the transition from water to land took place and what the first terrestrial tetrapods really were like.

A paper published on November 25 in Nature answers these questions using high-resolution fossil data and shows that although these early tetrapods were still water-related and had aquatic characteristics, they also had adaptations indicating some ability to move on land. However, they may not have been very good at it, at least by today’s standards.

Lead author Blake Dickson, Ph.D. ’20 in Harvard University’s Department of Organismic and Evolutionary Biology, and Senior Author Stephanie Pierce, Thomas D. Cabot Associate Professor in the Department of Organismic and Evolutionary Biology and Curator of vertebrate paleontology at Harvard University’s Museum of Comparative Zoology, examined 40 three-dimensional models of fossil humeri (upper arm bone) of extinct animals bridging the water-land transition.

“Because the fossil record of the land transition in tetrapods is so sparse, we went to a fossil source that could better represent the entirety of the transition from being a fully aquatic fish to a fully terrestrial tetrapod,” Dickson said.

Two-thirds of the fossils came from the historical collections housed at Harvard’s Museum of Comparative Zoology, which come from all over the world. To fill in the missing gaps, Pierce reached out to colleagues with key champions from Canada, Scotland and Australia. Of importance to the study were the new fossils recently discovered by co-authors Dr. Tim Smithson and Professor Jennifer Clack, University of Cambridge, UK, as part of the TW: eed project, an initiative designed to understand the early evolution of the land -going tetrapods.

The researchers chose humerus bone because not only is it abundant and well preserved in the fossil record, it is also present in all sarcopterygians, a group of animals that includes coelacanth fish, lungfish and all tetrapods, including all their fossil representatives. “We expected that the humerus would carry a strong functional signal as the animals went from being a fully functional fish to being completely terrestrial tetrapods, and that we could use it to predict when the tetrapods started moving on land,” he said. said Pierce. “We found that the Earth ability seems to coincide with the origin of the limbs, which is really exciting.”

The humerus fixes the front leg to the body, hosts many muscles, and must withstand many stresses during limb-based movement. For this reason, it contains a large amount of critical functional information related to the movement and ecology of an animal. The researchers suggested that evolutionary changes in the shape of the humerus bone, from short and stocky in fish to more elongated and present in tetrapods, had important functional implications related to the transition to terrestrial locomotion. This idea has rarely been studied from a quantitative perspective, at least until now.

When Dickson was a sophomore graduate student, he was fascinated by applying quantitative trait modeling theory to understand functional evolution, a technique introduced in a 2016 study led by a team of paleontologists and co-author of Pierce. At the heart of the quantitative modeling of traits is paleontologist George Gaylord Simpson’s 1944 concept of the adaptive landscape, a rugged three-dimensional surface with peaks and valleys, like a mountain range. In this landscape, increasing height represents better functional performance and adaptive fitness, and over time natural selection is expected to push populations to rise to an adaptive peak.

Dickson and Pierce thought they could use this approach to model the transition of tetrapods from water to land. They speculated that if the humerus changed shape, the adaptive landscape would also change. For example, fish would have an adaptive peak where functional performance was maximized for swimming and terrestrial tetrapods would have an adaptive peak where functional performance was maximized for walking on land. “We could then use these landscapes to see if the humerus shape of the earlier tetrapods was more suitable for performing in water or on land,” Pierce said.

“We started thinking about which functional traits it would be important to collect from the humerus,” Dickson said. “Which wasn’t an easy task as the fins of the fish are very different from the limbs of the tetrapods.” Eventually, they focused their attention on six traits that could be reliably measured across all fossils, including simple measurements like relative bone length as a proxy for stride length and more sophisticated analyzes that simulated mechanical stress in different loading scenarios. to estimate the strength of the humerus.

“If you have an equal representation of all functional traits, you can map how performance changes as you move from one adaptive peak to another,” explained Dickson. Using computational optimization, the team was able to reveal the exact combination of functional traits that maximized performance for aquatic fish, terrestrial tetrapods and early tetrapods. Their results showed that early tetrapods had a unique combination of functional traits, but did not conform to their own adaptive peak.

“What we found is that the humerus of the first tetrapods clustered at the base of the Earth’s landscape,” Pierce said. “indicating an increase in performance for moving on land. But these animals had developed only a limited set of functional traits for effective land walking.”

The researchers suggest that the ability to move on land may have been limited due to the selection of other traits, such as feeding in water, which linked the early tetrapods to their ancestral aquatic habitat. Once the tetrapods freed themselves from this constraint, the humerus was free to evolve morphologies and functions that improved limb-based locomotion and eventual invasion of terrestrial ecosystems

“Our study provides the first high-resolution quantitative information on the evolution of terrestrial locomotion through the water-land transition,” Dickson said. “It also provides a forecast of when and how [the transition] success and what functions were important in the transition, at least in the humerus. “

“Moving forward, we are interested in extending our research to other parts of the tetrapod skeleton,” said Pierce. “For example, it has been suggested that the forelimbs became terrestrial capable earlier than the hind limbs and our new methodology can be used to test this hypothesis.”

Dickson recently started as a postdoctoral researcher in Duke University’s Animal Locomotion lab, but continues to collaborate with Pierce and his lab members on further studies involving the use of these methods on other parts of the skeleton and fossils.