Unlocking the secrets of the evolution of whales and dolphins that adapted their spines to aquatic life

If you’ve ever seen a dolphin swimming, you may have wondered why it moves its body up and down when it swims, instead of from side to side like fish do. Although they have fish-like bodies, cetaceans (a group that includes whales, dolphins, and porpoises) are mammals that descend from land-dwelling ancestors, such as cats, dogs, mice, elephants, cows, and humans.

However, unlike their land-dwelling relatives, cetaceans have undergone profound changes in their body and skeletal structure to thrive in aquatic environments, including the reduction of hind limbs and the evolution of flippers and tail fins, resulting in a streamlined body.

Despite these adaptations, cetaceans retain key features of their terrestrial origins, such as lungs and the ability to nurse their young. And, as with these undulatory movements, they have also retained the similar vertical movements that allow land mammals to run very fast. But the mystery remains: how the transition from land to water, about 53 million years ago, impacted the construction and function of their spine, a central element of the skeleton.

However, in a study published in Nature CommunicationsAn international team of researchers has shed light on how the spines of these marine mammals were reorganized when their ancestors adapted to life in the water.

The team found that, contrary to previous assumptions, the cetacean spine is highly regionalized, although its shape is more homogeneous along its length. The way in which the spine is regionalized, however, is radically different from that of terrestrial mammals.

“When their ancestors returned to the water, whales and dolphins lost their hind legs and developed a fish-like body,” said lead author Dr Amandine Gillet, a Marie Curie Fellow in Harvard’s Department of Organismic and Evolutionary Biology and the Department of Earth and Environmental Sciences at the University of Manchester, UK.

“But this morphological change also means that the spine is now the main part of the skeleton that provides locomotion in an aquatic environment.”

The spine of land mammals that move on land must provide support to help the legs support the weight of the body. When cetaceans moved from land to water, the forces of gravity shifted from the air to the floating water, releasing the pressure to support the weight of the body. The new body structure and movements required to move through the water required the spine of these animals to shift in some way to adapt to their new environment.

Previous studies have looked at the spine from a morphological perspective, looking at changes in the morphology of the vertebrae. In a 2018 paper published in ScienceCo-authors Professor Stephanie Pierce and Dr Katrina Jones explored the complex evolutionary history of the mammalian spine using a new statistical method originally developed to study the spine of snakes.

Pierce and Jones revised the model to fit their study, allowing them to demonstrate that the spinal column of land mammals is characterized by many distinct regions compared to amphibians and reptiles.

“It’s a challenge to understand how regions of a land mammal can be found in whales and dolphins, and one reason is that their spines look very different in terms of morphology, even though they evolved from them,” said Pierce, a professor of organismal and evolutionary biology at Harvard and senior author of the study.

“They lost the sacrum, a chain of fused vertebrae supporting the hind legs and a key landmark needed to distinguish the tail from the rest of the body.”

Cetacean vertebrae are even more complex in that they have become more homogeneous in their anatomical features. Thus, the transition from one vertebra to another is gradual compared to the extreme transitions observed in terrestrial mammals, making it more difficult to identify regions.

“Not only do they have very similar vertebrae, but some species, particularly porpoises and dolphins, have many more vertebrae than land mammals, with some species having nearly 100 vertebrae,” said Jones, a presidential fellow in the Department of Earth and Environmental Sciences at the University of Manchester, UK.

“It is therefore very difficult to translate the regions found in land mammals to the spine of whales and dolphins.”

Traditional statistical methods used to identify regionalization patterns require exactly the same number of elements for all specimens. The statistical method implemented by Pierce and Jones (called Regions) allowed them to overcome this problem by analyzing the structure of each specimen individually.

While the method worked well for the small spines of land mammals, it proved difficult to calculate for the large number of vertebrae in cetaceans. Gillet collaborated with the Data Science Services team at the Harvard Institute for Quantitative Social Science to rewrite the code, allowing the program to produce results in minutes on a laptop. The researchers have made the new program, called MorphoRegions, available to the scientific community as an R computing package.

“This is definitely one of the biggest advances in our study,” Pierce said. “Amandine spent months refining the program so that it could analyze a system of highly repeated units without crashing the computer.”

Gillet applied the MorphoRegions method to data she had previously collected during her PhD. She visited six museums in Europe, South Africa and the United States, collecting morphological data on 139 specimens from 62 species of cetaceans, two-thirds of the nearly 90 living species. In total, Gillet measured 7,500 vertebrae and analyzed them.

“Our large dataset allowed us to demonstrate that not only does the organization of the cetacean spine differ from that of terrestrial mammals, but also that the patterns vary within cetaceans, as we identified between six and nine regions depending on the species,” Gillet said.

“We then worked from there to find commonalities between regions and identified a common pattern across cetaceans, which is summarized by our nested regions hypothesis.”

The hypothesis proposed by the team introduces a hierarchical organization of the spine in which a precaudal segment and a caudal segment are first identified. The two segments are then each divided into several modules common to all cetaceans: cervical, anterior thoracic, thoracolumbar, posterior lumbar, caudal, peduncle and caudal fin. Then, depending on the species, each module is itself subdivided into one to four regions, with a minimum of six and a maximum of nine post-cervical regions along the spine.

“Surprisingly, this showed us that, compared to terrestrial mammals, the precaudal segment has fewer regions, while the caudal area has more,” Pierce said. “Terrestrial mammals use their tails for a variety of different functions, but not typically to generate propulsive forces, as cetaceans do. Having more regions in the tail may allow movement in very specific regions of the tail.”

“From previous observational studies, we know that whales, dolphins and porpoises don’t swim in exactly the same way,” Gillet said.

“A species may need to swim slowly but with more maneuverability to catch its prey, or because it lives in a shallow environment with many obstacles. Other species living in the open ocean may need to be able to go fast in a straight line without requiring much bodily flexibility.”

So the team looked at the correlation between spinal regions and habitat and swimming speed. They found that species living offshore, further from the coast, have more vertebrae, more regions, and a higher swimming speed. Species living in rivers and bays, and therefore closer to shore, have fewer vertebrae and fewer regions, but their regions are more different from each other, potentially allowing them greater maneuverability.

“It’s a beautiful study,” Pierce said. “You go from dusty skeletons in a museum to demonstrating how the spinal column of one of the most charismatic groups of mammals was reshaped by its aquatic environment. And we can directly relate that to the habitat and swimming performance of living animals.”

With a better understanding of the organization of the cetacean spine, the researchers plan to next tackle understanding the correlation between these morphological regions and function using experimental data on spinal flexibility collected in the laboratory.

These data collected on modern taxa should allow them to deduce the swimming abilities of fossil whales and help understand how the spine evolved from a load-bearing structure on land to a propulsion-generating organ in water.