Sloths and Armadillos See The World In Black-and-White

Armadillos have terrible vision. In 1913, American zoologists Horatio H. Newman and J. Thomas Patterson wrote, “The eyes [of the nine-banded armadillo] are rudimentary and practically useless. If disturbed an armadillo will charge off in a straight line and is as apt to run into a tree trunk as to avoid it.”

The three-toed sloth isn’t much better. “If an infant sloth is placed five feet away from its mother on a horizontal branch at the same level, at once the young sloth begins to cry, the mother shows that she heard it calling and turns her head in all directions. Many times she looks straight in the direction of her offspring but neither sight, hearing nor smell apparently avail anything,” wrote Michel Goffart in 1971. And more comically: “Infuriated male [sloths] try to hit each other when they are still distant by more than a metre and a half.”

Now, decades after these descriptions were written, Christopher Emerling and Mark Springer from the University of California Riverside think they know why armadillos and sloths are so poor of sight. These animals have broken copies of the genes that build colour-detecting cone cells in their eyes. That leaves them with only rod cells, which have poorer resolution and work best in dim light. They see the world in coarse black-and-white, and they struggle to cope with bright light.

This discovery supports the idea the armadillos, sloths, and anteaters—a group collectively known as the xenarthrans—evolved from a burrowing ancestor that spent much (if not all) of its time underground. With light in short supply, these ancestral animals may have prioritised the sensitive rod cells over the sharp and colour-tuned cones.

They eventually re-surfaced and, in the case of sloths, even took to the trees. But they still retain traces of their burrowing past, including sturdy front legs, curved claws, and skeletal features that gave them a powerful digging stroke (the word “xenarthran” means “strange joints”). Anteaters use these traits to rip through ant nests, while sloths use them to hang from branches.

But they also carried their ancestors’ cone-less retinas. These, according to Emerling and Springer, might have constrained their evolution in important ways. With poor vision, they couldn’t take up many of the lifestyles that other mammals developed, like fast-running, active-hunting, or gliding. And armadillos “have minimal ability to see approaching cars when crossing roads, a fact all too familiar to residents of Texas,” says Emerling.

This discovery is part of a much larger narrative for mammals—one that highlights evolution’s fickle nature. A wide range of animals, including many birds, fish, reptiles, and amphibians, have eyes with four types of cones, allowing them to discriminate between a huge range of colours. Mammals, however, evolved from a nocturnal ancestor that had already lost two of its cones, and many have stuck with this impoverished set-up. Dogs, for example, still only have two cones: one tuned to violet-ish colours and another tuned to greenish-blue. (Contrary to popular belief, a dog’s world isn’t black-and-white; they see colours, albeit a limited palette.)

Humans and other primates partly reversed the ancient loss by reinventing a third red-sensitive cone, which may have helped us to discern unripe green fruits from ripe red/orange ones. Ocean-going mammals, meanwhile, took the loss of cones even further and disposed of their blue/violet-sensitive ones. And the great whales have lost all their cones entirely. They only have rods. The ocean is blue, but a blue whale would never know.

Springer’s team discovered the rod-only whale retinas a few years ago. It seemed to make sense, since these are deep-diving animals that spend a lot of time at depths where little light penetrates. The same team also showed that golden moles also lack cones—they are ‘rod monochromats’. Again, this made sense: these animals spend most of their time underground.

But the nine-banded armadillo was more puzzling. Emerling looked at its genome and saw that several of its cone-building genes had picked up debilitating mutations, which should saddle it with a rod-only retina. “I was convinced this was a sequencing error,” he says,” since armadillos are often active in the daytime. They don’t dive deep in the ocean and don’t live underground.”

Emerling checked the results more carefully and showed that the armadillo still has working copies of all its rod-specific genes, but has broken versions of seven cone-specific ones. He found similar examples of broken cone genes in the genomes of other xenarthrans, including five other armadillo species, three anteaters, a living sloth, and even an extinct ground sloth.

By comparing these genes, he concluded that the group’s last common ancestor had already lost one of its cones thanks to a disabling mutation. Two different branches—the armadillos, and the sloths/anteaters—then independently disabled different genes involved in building the last remaining cone.

“It was even more of a shock to discover the same thing for sloths,” says Emerling. “Sloths live in trees! Of all the things to get rid of as an arboreal mammal, daylight vision does not seem like it should be one of them!”

But Tom Cronin from the University of Maryland, Baltimore County cautions that “all-rod vision is not incompatible with daylight activity”. The great whales spend a lot of time at the ocean’s surface in full daylight, he says. And there are even people who have rod-only vision—they do well in all but brilliant sunlight, and have sharp enough vision to read in normal light. (Then again, Emerling says that this condition is sometimes called “day blindness”, and that “it’s frequently painful for these individuals to keep their eyes open during the day.”)

Cronin also notes that it’s hard to draw firm conclusions about an animal’s vision through genetics alone. Xenarthrans could have compensated for their broken cone genes, so to prove that they really have rod-only sight, you’d have to examine their retinas and actually test their vision.

Emerling acknowledges this, but points to other lines of evidence. For example, xenarthran eyes lack a muscle that helps other mammals to focus their lenses, which is suggestive of poor eyesight. There are also many anecdotal accounts of sloths, armadillos, and anteaters having terrible daytime vision. And in one experiment, sloths behaved no differently when wearing eye masks. Put all of this together, and “it seems extremely probable that armadillos and sloths lack cones entirely,” he says.

But if that’s the case, it raises another mystery: why have so many burrowing mammals, including African mole-rats, European moles, and many species of rodents, kept their cones? Despite spending their lives underground, they all have retinas that are far closer to those of day-living mammals than nocturnal ones. Subterranean living doesn’t necessarily equate to cone loss.

“There is no obvious reason why either xenarthrans or [whales] should have given up their cones,” says Cronin. So why did they?

Reference: Emerling & Springer. 2014. Genomic evidence for rod monochromacy in sloths and armadillos suggests early subterranean history for Xenarthra. Proc Roy Soc B http://dx.doi.org/10.1098/rspb.2014.2192

Correction: This post originally stated that marine mammals lost their green-sensitive cones. They actually lost their blue/violet-sensitive ones.