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How seeing snakes in the grass helped primates to evolve

<p><em>Copperhead Snake on Dead Leaves, </em>study for book<em> Concealing Coloration in the Animal Kingdom</em>, <em>c</em>1910-1915, by Abbot Handerson Thayer. <em>Courtesy the Smithsonian American Art Museum</em></p>

Copperhead Snake on Dead Leaves, study for book Concealing Coloration in the Animal Kingdom, c1910-1915, by Abbot Handerson Thayer. Courtesy the Smithsonian American Art Museum

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by Lynne A Isbell + BIO

Dry brown leaves on the forest floor, creating a textured, autumnal scene with varied shades of brown and orange.

Copperhead Snake on Dead Leaves, study for book Concealing Coloration in the Animal Kingdom, c1910-1915, by Abbot Handerson Thayer. Courtesy the Smithsonian American Art Museum

Evolution has favoured the modification and expansion of primate vision. Compared with other mammals, primates have, for example, greater depth perception from having forward-facing eyes with extensively overlapping visual fields, sharper visual acuity, more areas in the brain that are involved with vision, and, in some primates, trichromatic colour vision, which enables them to distinguish red from green hues. In fact, what separates primates from other mammals most is their much greater reliance on vision as the main sensory interface with the environment.

Vision is a window onto the world, its qualities determined by natural selection and the constraints of both animals’ bodies and the environments in which they live. Despite their long, shared evolutionary history, mammals don’t all see the world in the same way because they inhabit a variety of niches with different selective pressures. What were those selective pressures for primates, our lineage, that led to their having visual systems more expansive and more complex than those of other mammals?

In 2006, I published a new idea that could answer that question and more: the ‘snake detection theory’. I hypothesised that when large-gaped constricting snakes appeared about 100 million years ago and began eating mammals, their predatory behaviour favoured the evolution of changes in the vision of one kind of prey, the lineage that was to become primates. In other words, the ability to see immobile predatory snakes before getting too close became a highly beneficial trait for them to have and pass on to their descendants. Then, about 60 million years ago, venomous snakes appeared in Africa or Asia, adding more pressure on primates to detect and avoid them. This has also had repercussions on their visual systems.

There is a consistency between the degree of complexity in primate visual systems and the length of evolutionary time that primates have spent with venomous snakes. At one extreme, the lineage that comprises Old World monkeys, apes and humans has the best vision of all primates, including excellent visual acuity and fully trichromatic colour vision. Having evolved roughly at the same time and in the same place as venomous snakes, these primates have had continuous coexistence with them. They are also uniformly wary of snakes.

At the opposite end of the spectrum, Malagasy primates have the simplest visual systems. Among other things, they have low visual acuity because the fovea, a depression in the retina that is responsible for our visual acuity wherever we focus our eyes, is poorly developed (when it’s present at all). Although Madagascar has constricting snakes, it has no venomous snakes, so primates on that island never had to face that particular selective pressure. Behavioural evidence also reveals that they don’t all react fearfully toward snakes. Some can even walk on snakes or snake models, treating them as if they’re just another branch.

The visual systems of New World monkeys are in the middle. They have better visual acuity than Malagasy primates but more variability in their visual systems than Old World monkeys. For example, New World howler monkeys are all trichromatic, but in other New World primate species, only some individuals are able to distinguish red from green hues. New World primates were originally part of the anthropoid primate lineage in Africa that also includes Old World monkeys and apes, and so had to deal with venomous snakes for about 20-25 million years, but then, some 36 million years ago, they left Africa and arrived in South America where venomous snakes were not present until roughly 15 million years later. By then, New World monkeys had begun to diversify into different genera, and so each genus evolved separate solutions to the renewed problem caused by the arrival again of venomous snakes. As far as I know, no other explanation for the variation in their visual systems exists.

Since I proposed the snake detection theory, several studies have shown that nonhuman and human primates, including young children and snake-naive infants, have a visual bias toward snakes compared with other animate objects, such as lizards, spiders, worms, birds and flowers. Psychologists have discovered that we pick out images of snakes faster or more accurately than other objects, especially under cluttered or obscuring conditions that resemble the sorts of environments in which snakes are typically found. Snakes also distract us from finding other objects as quickly. Our ability to detect snakes faster is also more pronounced when we have less time to detect them and when they are in our periphery. Moreover, our ‘primary visual area’ in the back of the brain shows stronger electrophysiological responses to images of snakes than of lizards 150-300 milliseconds after people see the images, providing a measurable physical correlate of our greater visual bias toward them.

Since vision is mostly in the brain, we need to turn to neuroscience to understand the mechanisms for our visual bias toward snakes. All vertebrates have a visual system that allows them to distinguish potential predators from potential prey. This is a nonconscious visual system that involves only subcortical structures, including those that in mammals are called the superior colliculus and the pulvinar, and it allows for very fast visual detection and response. When an animal sees a predator, this nonconscious visual system also taps directly into motor responses such as freezing and darting.

As vertebrates, mammals have this nonconscious visual system, but they have also incorporated vision into the neocortex. No other animals have a neocortex. This somewhat slower, conscious visual system allows mammals to become cognizant of objects for what they really are. The first neocortical stop is the primary visual area, which is particularly sensitive to edges and lines of different orientations.

In a breakthrough study, a team of neuroscientists probed the responses of individual neurons in the pulvinar of Japanese macaques as they were shown images of snakes, faces of monkeys, hands of monkeys, and simple geometric shapes. Sure enough, many pulvinar neurons responded more strongly and more quickly to snakes than to the other images. The snake-sensitive neurons were found in a subsection of the pulvinar that is connected to a part of the superior colliculus involved in defensive motor behaviour such as freezing and darting, and to the amygdala, a subcortical structure involved in mediating fear responses. Among all mammals, the lineage with the greatest evolutionary exposure to venomous snakes, the anthropoid monkeys, apes and humans, also have the largest pulvinar. This makes perfect sense in the context of the snake detection theory.

What is it about snakes that makes them so attention-grabbing to us? Naturally, we use all the cues available (such as body shape and leglessness) but it’s their scales that should be the most reliable, because a little patch of snake might be all we have to go on. Indeed, wild vervet monkeys in Africa, for instance, are able with their superb visual acuity to detect just an inch of snake skin within a minute of coming near it. In people, electrophysiological responses in the primary visual area reveal greater early visual attention to snake scales compared with lizard skins and bird feathers. Again, the primary visual area is highly sensitive to edges and lines of different orientations, and snake skins with their scales offer these visual cues in spades.

The snake detection theory takes our seemingly contradictory attitudes about snakes and makes sense of them as a cohesive whole. Our long evolutionary exposure to snakes explains why ophiophobia is humanity’s most-reported phobia but also why our attraction and attention to snakes is so strong that we have even included them prominently in our religions and folklore. Most importantly, by recognising that our vision and our behaviour have been shaped by millions of years of interactions with another type of animal, we admit our close relationship with nature. We have not been above or outside nature as we might like to think, but have always been fully a part of it.

5 February 2019
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