Fish Changed in a Surprising Way Before Invading Land

Even before they grew strong legs, their eyes surged in size.

Tiktaalik peers out of the water
Tiktaalik peers out of the water (Malcolm MacIver)

Around 385 million years ago, fish started hauling themselves onto land. Over time, their flattened fins gradually transformed into sturdy legs, ending in feet and digits. Rather than paddling through water, they started striding over solid ground. Eventually, these pioneers gave rise to the tetrapods—the lineage of four-legged animals that includes reptiles, amphibians, and mammals like us. This transition from water to land is an evocative one, and for obvious reasons, people tend to focus on the legs. They are the organs that changed most obviously, that gave the tetrapods their name, and that carried them into their evolutionary future.

But Malcolm MacIver from Northwestern University was more interested in eyes.

The earliest tetrapods had much bigger eyes than their fishy forebears. MacIver always assumed that this enlargement happened after they marched onto land, allowing them to see further and to plan their paths. “That was an expectation fueled by ignorance,” he says. Actually, after studying the fossils of many fishapods—extinct species that were intermediate between fish and tetrapods—MacIver found that bigger eyes evolved before walking legs.

As the eyes swelled in size, they also moved to the tops of their owners’ heads, allowing them to peer out of the water surface like crocodiles do today. These traits enabled them to see further than their aquatic ancestors and to look over a much greater range of space, allowing them to snatch up prey from the shoreline. And that ability could have given them the impetus to leave the water entirely, driving the evolution of their vaunted legs. Perhaps eyes, not legs, led the invasion of the land. Perhaps, as MacIver puts it, “the gateway drug to terrestriality was being like a crocodile.”

“This study helps explain how fishes built for life in the water could be lured to shore without losing their competitive edge along the way,” says Lauren Sallan from the University of Pennsylvania, who was not involved in the work.

Eyes don’t fossilize, but you can estimate how big they would have been by measuring the eye sockets of a fossilized skull. MacIver and his colleagues, including fossil eye expert Lars Schmitz, did this for the skulls of 59 species—from finned fish to intermediate fishapods to legged tetrapods. They showed that over 12 million years, the group’s eyes nearly tripled in size. Why?

Eyes are expensive organs: it takes a lot of energy to maintain them, and even more so if they’re big. If a fish is paying those costs, the eyes must provide some kind of benefit. It seems intuitive that bigger eyes let you see better or further, but MacIver’s team found otherwise. By simulating the kinds of shallow freshwater environments where their fossil species lived—day to night, clear to murky—they showed that bigger eyes make precious little difference underwater. But once those animals started peeking out above the waterline, everything changed. In the air, a bigger eye can see 10 times further than it could underwater, and scan an area that’s 5 million times bigger.

In the air, it’s also easier for a big eye to pay for itself. A predator with short-range vision has to constantly move about to search the zone immediately in front of its face. But bigger-eyes species could spot prey at a distance, and recoup the energy they would otherwise have spent on foraging. “Long-range vision gives you a free lunch,” says MacIver. “You can just look around, instead of moving to inspect somewhere else.”

Those early hunters would have seen plenty of appetizing prey. Centipedes and millipedes had colonized the land millions of years before, and had never encountered fishapod predators. “I imagine guys like Tiktaalik lurking there like a crocodile, waiting for a giant millipede to walk by, and chomping on it,” says MacIver. “No invertebrate on land would have been a match for it.”

So here’s what MacIver thinks may have happened. In shallow, freshwater rivers and lakes, some fish gradually moved their eyes to the top of their skulls, to better exploit the down-welling sunlight. This happened during the Devonian period, when the Earth’s oxygen levels were declining. Struggling to get enough oxygen in the water, creatures like Tiktaalik evolved breathing holes at the tops of their heads, just behind their eyes. They started surfacing more regularly, allowing them to tackle prey that wandered near the water. At first, they would only have seen the blurry outlines of their targets, but even small changes to their eyes would have produced enormous benefits. Over time, their eyes became bigger. And eventually, their limbs changed too, allowing them to make longer forays into this new world—a world of not only solid ground, but also large distances.

Some of this is speculative, but it fits with the patterns that MacIver’s team see in their fossils and their data. Jenny Clack from the University of Cambridge, who is an expert on the evolution of tetrapods, is pleased that the team have measured the increase in socket size—something that others have noted, but never in this much detail. But “socket size doesn’t always correlate with eyeball size,” she says. It’s better to look at the sclerotic ring—a disc of bone that’s found around the eyes of many animals. MacIver counters that in the fossils that he and Schmitz studied, the correlation between eyeball and socket is “very good,” and that “the presence of the ring doesn’t seem change our predictions.”

“They took a very creative and new approach to an old problem,” says Neil Shubin from the University of Chicago, who discovered Tiktaalik. Most people who study the evolution of tetrapods have focused on their limbs and jaws. Instead, MacIver’s group focused on sense organs—the eyes. And they suspect that the eyes are linked to the evolution of another critical organ—the brain.

MacIver’s idea is that long-range vision changes the type of mental abilities that an animal benefits from. Underwater, a fish is like a driver zooming along a foggy road. It can only react to what’s directly in front of it—life, as they say, comes at you fast. But a tetrapod, walking on land, can scan a much greater area. In a way, bigger eyes let you see further into time as well as space. Now, there are more benefits to abilities like planning, strategic thinking, and complex decision-making. Animals become less reactive, and more proactive.

He calls this the Buena Vista Sensing Club hypothesis. “Maybe having this expanded sensing volume allowed us to break the knee-jerk connection between sensing and moving, and decouple thoughts from action,” he speculates. “Now you’re choosing the best thought for your environment, which looks like a kind of proto-consciousness.”