How ancient whales lost their legs, got sleek and conquered the oceans

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More than 50 million years ago the ancestors of whales and dolphins were four-footed land animals, not unlike large dogs. They became the sleek swimmers we recognize today during the next 15 million years, losing their hind limbs in a dramatic example of evolutionary change.

"We can see from fossils that whales clearly lived on land-they actually share a common ancestor with hippos, camels and deer," said team member Martin Cohn, Ph.D., a developmental biologist and associate professor with the UF departments of zoology and anatomy and cell biology and a member of the UF Genetics Institute. "Their transition to an aquatic lifestyle occurred long before they eliminated their hind limbs. During the transition, their limbs became smaller, but they kept the same number and arrangement of hind limb bones as their terrestrial ancestors."

In findings to be published this week in the Proceedings of the National Academy of Sciences, scientists say the gradual shrinkage of the whales' hind limbs over 15 million years was the result of slowly accumulated genetic changes that influenced the size of the limbs and that these changes happened sometime late in development, during the fetal period.

However, the actual loss of the hind limb occurred much further along in the evolutionary process, when a drastic change occurred to inactivate a gene essential for limb development. This gene-called Sonic hedgehog-functions during the first quarter of gestation in the embryonic period of the animals' development, before the fetal period.

In all limbed vertebrates, Sonic hedgehog is required for normal limbs to develop beyond the knee and elbow joints. Because ancient whales' hind limbs remained perfectly formed all the way to the toes even as they became smaller suggests that Sonic hedgehog was still functioning to pattern the limb skeleton.

The new research shows that, near the end of 15 million years, with the hind limbs of ancient whales nonfunctional and all but gone, lack of Sonic hedgehog clearly comes into play. While the animals still may have developed embryonic hind limb buds, as happens in today's spotted dolphins, they didn't have the Sonic hedgehog required to grow a complete or even partial limb, although it is active elsewhere in the embryo.

The team also showed why Sonic hedgehog became inactive and all traces of hind limbs vanished at the end of this stage of whale evolution, said Cohn. A gene called Hand2, which normally functions as a switch to turn on Sonic hedgehog, was shown to be inactive in the hind limb buds of dolphins. Without it, limb development grinds to a halt.

"By integrating data from fossils with developmental data from embryonic dolphins, we were able to trace these genetic changes to the point in time when they happened," Thewissen said.

"Studies on swimming in mammals show that a sleek body is necessary for efficient swimming, because projecting organs such as rudimentary hind limbs cause a lot of drag, and slow a swimmer down," said Thewissen, who spends about a month every year in Pakistan and India collecting fossils that document the land-to-water transition of whales.

Researchers say the findings tend to support traditional evolutionary theory, a la Charles Darwin, that says minor changes over vast expanses of time add up to big changes. And while Sonic hedgehog's role in the evolution of hind limbs in ancient whales is becoming apparent, it is still not fully defined.

"It's clear when ancient whales lost all vestiges of the limb it was probably triggered by loss of Sonic hedgehog," said Clifford Tabin, Ph.D., a professor of genetics at Harvard Medical School who was not involved in the research. "But it's hard to say for certain because you're looking at events long after they occurred. As they suggest, there could have been a continual decrease in Sonic as the limbs reduced until the modern version of the animal arrived."

The study itself, combining fossil and developmental data, is notable, Tabin said.

"Whales went through this remarkable transformation to become more like the ancestral fish," Tabin said. "Convergence of evolutionary studies and developmental genetics give us another piece in this growing tapestry of how genetic changes lead to morphological change. It is a remarkable process that was achieved simply and led to profound consequences in how whales were able to survive. Only now in the last five years are we developing this understanding of how the world of evolution is controlled genetically."

University of Florida