How mammals grow ears: With a flaw

Hey evolution, thanks for nothing. When a mammal embryo develops, its middle ear appears to form in a pop-and-patch way that seals one end with substandard, infection-prone tissue.

“The way evolution works doesn’t always create the most perfect, engineered structure,” says Abigail Tucker, a developmental biologist at King’s College London. “Definitely, it’s made an ear that’s slightly imperfect.”

The mammalian middle ear catches sound and transfers it, using three tiny bones that jiggle against the eardrum, to the inner ear chamber. Those three bones — the hammer, anvil and stirrup — are a distinctive trait that distinguishes the group from other evolutionary lineages.

Research in mouse embryos finds that the middle ear begins as a pouch of tissue. Then its lining ruptures at one end and the break lets in a different kind of tissue, which forms the tiny bones of the middle ear.

This intruding tissue originates from what’s called the embryo’s neural crest, a population of cells that gives rise to bone and muscle. Neural crest tissue has never been known before to create a barrier in the body. Yet as the mouse middle ear forms, this tissue creates a swath of lining that patches the rupture, Tucker and colleague Hannah Thompson, report in the March 22 Science.  

This neural crest tissue isn’t great at forming barrier linings. Its patch in the middle ear tends to flake off when infected. And it doesn’t form the forest of protective hairlike cilia that sweeps away debris in the rest of the middle ear.

The improvisational patch may explain why infections in this bald zone of the middle ear tend to be more severe and frequent than in cilia-covered stretches.

Before this paper, biologists thought the entire lining of the middle ear came from one kind of tissue, endoderm, which readily forms hairs. Tucker says she wondered how that endoderm layer managed to grow a continuous lining despite the middle ear’s complicated obstacles of developing bones, along with their tendons and blood supplies.

To trace the process in detail, she and Thompson turned to genetically engineered mice that have labels distinguishing neural crest and endoderm tissues. By staining mouse tissue samples, the researchers revealed these labels and pieced together the parts of the middle ear that came from each precursor cell type.

The development process may be general to all mammals, says Donna Fekete of Purdue University in West Lafayette, Ind. The scenario fits with observations of a lining rupture and a no-cilia zone in both human and rat middle ears. “If I were revising a textbook of human embryology,” she says, “I would change the drawings.”

That middle ear does have its strengths, Tucker says. The three little bones provide sensitivity to sounds. Two of them evolved from hinge bones in the jaws of mammals’ deep ancestors.

Whether the crummy patch of lining is the evolutionary price of having three ear bones remains to be seen. Examining marsupial ear development might test the notion, suggests vertebrate paleontologist Anne Weil of Oklahoma State University Center for Health Sciences in Tulsa. The common ancestors of marsupials and the rest of mammals, living more than 100 million years ago, had already developed the bony middle ear. If kangaroos or other marsupials show traces of the rupture-repair process in the middle ear, then an evolutionary link with the three bones would look likely.