How did the function of the forelimbs change as vertebrates acquired limbs and moved to land?

From fins to limbs

Life reconstruction of the early Pederpes tetrapods showing the bones of the forelimbs under the skin. Credit: Image copyright 2021 Julia Molnar.

When tetrapods (four-limbed vertebrates) started moving from water to land around 390 million years ago, this triggered the rise of lizards, birds, mammals, and all land animals. that exist today, including humans and some aquatic vertebrates such as whales. and dolphins.

The earliest tetrapods originate from their fish ancestors in the Devonian period and are more than twice as old as the oldest dinosaur fossils. They looked like a cross between a giant salamander and a crocodile and were around 1 to 2 meters long, had gills, webbed legs, and caudal fins, and were still strongly water-bound. Their short arms and legs had up to eight digits on each hand and foot, and they were probably ambush predators, hiding in shallow water waiting for prey to approach.

Scientists know how the fins of fish developed into members of tetrapods, but controversies remain over where and how the first tetrapods used their members. And, although many hypotheses have been proposed, very few studies have rigorously tested them using the fossil record.

In an article published on January 22 in Scientific advances an international team of researchers examined three-dimensional digital models of the bones, joints and muscles of the fins and limbs of two extinct early tetrapods and a closely related fossil fish to reveal how the function of the forelimbs changed as the fins evolved in members. Research by Julia Molnar, assistant professor at the New York Institute of Technology College of Osteopathic Medicine and Stephanie Pierce, Thomas D. Cabot Associate Professor of Organismic and Evolutionary Biology at Harvard University, discovered three distinct functional stages in the transition from fins to members. , and that these early tetrapods had a very distinct pattern of muscle lever that did not resemble a fish fin or modern tetrapod limbs.

To reconstruct the functioning of limbs from the first known tetrapods, Molnar, Pierce and co-authors John Hutchinson (Royal Veterinary College), Rui Diogo (Howard University) and Jennifer Clack (University of Cambridge) first had to determine which muscles were present. . in fossil animals. A difficult task because the muscles are not preserved in fossils and the muscles of modern fish fins are completely different from those of tetrapod limbs. The team spent several years trying to answer the question, how exactly did the few simple muscles in a fin become dozens of muscles that perform all kinds of functions in a tetrapod limb?

“Figuring out what muscles were present in a 360 million year old fossil took many years of work just to get to the point where we could start building some very complicated musculoskeletal models,” Pierce said. “We needed to know how many muscles were present in fossil animals and where they attached to the bones so that we could test their function.”

They constructed three-dimensional musculoskeletal models of the pectoral fin in Eusthenopteron (a fish closely related to the tetrapods that lived in the late Devonian around 385 million years ago) and the forelimbs of two early tetrapods, Acanthostega (365 million years living near the end of the Upper Devonian) and Pederpes (348-347 million years living at the beginning of the Carboniferous period). For comparison, they also built similar models of pectoral fins of live fish (coelacanth, lung) and forelimbs of live tetrapods (salamander, lizard).

To determine how the fins and limbs function, the researchers used computational software originally developed to study human locomotion. This technique had been used recently to study locomotion in the ancestors of humans and also dinosaurs like T. rex, but never in something as old as an early tetrapod.

Virtual skeleton of the early Pederpes tetrapod from the fossil and musculoskeletal reconstruction scanned by micro-computed tomography of its forelimb. Credit: Copyright 2021, Julia Molnar.

By manipulating the models in the software, the team was able to measure two functional traits: the maximum range of motion of the joint and the ability of the muscles to move the fin or limb joints. Both measurements would reveal trade-offs in the locomotor system and allow researchers to test hypotheses of functioning in extinct animals.

The team found that the forelimbs of all terrestrial tetrapods went through three distinct functional stages: a ‘benthic fish’ stage that looked like a modern red lung, an ‘early tetrapod’ stage unlike any extinct animal, and a “Crowned tetrapod” stage exhibiting the characteristics of two lizards. and salamanders.

“The fin of Eusthenopteron had a pattern reminiscent of the lungfish, which is one of the closest living relatives of tetrapods, ”Pierce said. But the early members of the tetrapods had more similarities than modern fish or tetrapods. “

“It was perhaps the most surprising,” Molnar said. “I thought Pederpes, and eventually Acanthostega, would fit fairly well into the range of modern tetrapods. But they formed their own distinct group that did not resemble a modern tetrapod member or fish fin. They weren’t in the middle but had their own collection of characteristics that likely reflected their unique surroundings and behaviors. “

The results showed that the early tetrapod limbs were more suited to propelling than weight bearing. In the water, animals use their limbs to propel themselves to move forward or backward, allowing the water to support their body weight. Moving on land, however, requires the animal to act against gravity and push downward with its limbs to support its body mass.

This does not mean that the first tetrapods were unable to move on earth, but rather that they did not move like a modern living tetrapod. Their means of locomotion were probably unique to those animals which were still very much water-related, but who also ventured onto land, where there were many opportunities for vertebrate animals but little competition or fear of the animals. predators.

“These results are exciting because they independently support a study I published last year using completely different fossils and methods,” Pierce said. “This study, which focused on the arm bone, indicated that the early tetrapods had some ability for land movement but may not be very good at it.”

Researchers are closer to reconstructing the evolution of terrestrial locomotion, but more work is needed. They plan to then model the hind limb to study how the four limbs worked together. It has been suggested that the earliest tetrapods used their forelimbs for propulsion, but modern tetrapods derive most of their propulsive power from the hind limbs.

“We plan to look for any evidence of a change in forelimb-driven locomotion to hindlimb motor locomotion, such as modern tetrapods,” Molnar said. Looking at the forelimbs and hind limbs together, one could tell more about the transition from water to land and how the tetrapods came to dominate the land realm.

Water-land transition in the first tetrapods

More information:
“Evolution of the musculoskeletal function of the forelimbs during the fish-tetrapod transition” Scientific advances, DOI: 10.1126 / sciadv.abd7457

Provided by Harvard University

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