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Distant mammal ancestors such as Dimetrodon (right) had three spine regions; a mouse (left) has five.

K. JONES ET AL., SCIENCE, 361, 6408 (2018)

The evolution of the spine fueled the rise of mammals—and human back problems

Run, climb, breathe deep. You might not connect those abilities to your backbone. In fact, mammals owe many of their capabilities to the complex structure of their spine, which has five distinct regions, each free to adopt specialized functions. In this week's issue of Science, Harvard University vertebrate paleontologist Stephanie Pierce and postdoc Katrina Jones report an investigation of fossils from the dawn of mammals that shows how evolution built our versatile spine.

"This is an important analysis," says Richard Blob, a biomechanist at Clemson University in South Carolina. "It's tackling a fundamental problem: the origins of animal construction." And it shows how mammals ended up with a backbone that "can evolve in pieces and respond to different selective pressures at different places along the column," says Emily Buchholtz, a vertebrate paleontologist at Wellesley College in Massachusetts.

Biologists have long recognized distinct regions in the mammalian spine based on their vertebrae. For example, small cervical vertebrae make up the neck, thoracic vertebrae bear the ribs and support the chest, and the ribless, hefty lumbar vertebrae bring up the rear. In contrast, reptiles and amphibians have very uniform backbones. "All their vertebrae are essentially doing the same thing," Pierce says. She and others assumed a regionalized spine was unique to mammals.

But in 2015, a sophisticated statistical analysis of a snake spine and a look at the genetic programs controlling its development indicated this backbone, too, has very subtly defined regions. "The work showed that regions could be distinct even if they weren't as different as in mammals," says Christian Kammerer, a paleontologist at the North Carolina Museum of Natural Sciences in Raleigh. The finding suggested a regionalized vertebral column evolved early in land animal history, even before the divergence of mammals and reptiles.

To probe its origins, Pierce, Jones, and their colleagues scoured museums for fossils with complete backbones. Ultimately, they analyzed spines from 16 synapsids, creatures that lived 200 million to 300 million years ago and include distant and immediate predecessors to mammals. They used computerized tomography scanning to get high-resolution images and worked with paleontologist David Polly from Indiana University in Bloomington to precisely measure the shapes of the vertebrae and assess regionalization within each animal.

The analysis uncovered a stepwise addition of regions. More distant ancestors of mammals, such as Dimetrodon, a large reptilelike synapsid with a giant sail on its back, had three regions, designated cervical, anterior dorsal, and posterior dorsal. The therapsids, creatures that just preceded mammals, had a fourth region, the pectoral. A fifth region, the lumbar, appeared after early, egg-laying mammals arose and is found today in placental and marsupial mammals.

The work also pointed to factors driving the emergence of these distinct regions. The pectoral region, for example, appeared in the therapsids as they evolved longer forelimbs, positioned under the body rather than splayed to the sides. (Think of a dog's legs compared with a lizard's.) The limb changes would have required changes in the shoulder girdle and the vertebrae supporting it, resulting in a distinct region of the spine just behind the neck. The same set of changes also freed some shoulder muscles to evolve into a muscular diaphragm, which improved breathing and enabled mammals to have a higher metabolic rate, Buchholtz says.

Over time, further decoupling led to the modular spine seen in mammals today, in which individual vertebrae can change without jeopardizing the function of the whole spine. As a result, different regions can "take on new forms and functions, so they can adapt to different environments," Pierce says. Perhaps the most variable part of the spine has been the last to emerge: the lumbar region, which interacts with the pelvis and hind limbs.

The cat family illustrates the benefits of the region's evolutionary freedom. All cats look, well, catlike, but lions tend to keep their feet on the ground and hunt large prey, whereas clouded leopards live in trees, leaping on their quarry, and cheetahs chase down antelopes at high speeds. Paleontologists Marcela Randau and Anjali Goswami of the Natural History Museum in London did 3D analyses of 109 cat skeletons representing species with various hunting and living strategies. They compared the vertebrae within each species and between species, as well as the limbs, shoulders, pelvises, and skulls.

In all these cats, most of the spine looks similar. Their lumbar regions have diversified, however, suggesting this region evolved independently of the rest of the spine and skeleton, Randau said last month at the second Joint Congress on Evolutionary Biology in Montpellier, France. The size and shape of the lumbar vertebrae vary depending on what the cat does best.

"It's the lumbar region that really allows mammals to do all sorts of different things," Pierce says. On the downside, the more recently evolved parts of the back—the lumbar region in particular—are also the source of most back pain, Pierce says, so "maybe we also owe our ancestors for having back complications."