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The Turtle with Human Eyes

Redneck
Redneck, my favorite red-eared slider (Trachemys scripta elegans) turtle is a difficult "pet."  He is often gone on walkabout for weeks or months at a time, and there have been entire seasons that I cannot find him.  I often spend hours trudging through the wetlands that surround our home looking for Redneck, worrying that something has happened to him.  He usually turns up, eventually.  When he is around I love talking to him and taking photos of him basking and doing whatever turtles do around our three large ponds (15,000 gallons each; 57,000 liters).

People often ask how I can identify Redneck from the many other turtles in our ponds.  Redneck is the most expressive.  What can I say?  I know him.  Also he has a large white area on the right front of his shell that is unmistakable.  
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One Question Answered
Another Question Still Baffles
I've done a lot of research into red-eared sliders trying to figure out what it is about their eyes that make them so human-like, and why red-eared sliders have a stripe across their eye.  What evolutionary event led to selection of the striped eye?  Why was some past relative of Redneck's more successful because of the stripped eye, so much so that they passed on that genetic mutation eventually making it permanent.  Was it a fluke that passed on with other traits or is it something significant that suggests striped-eye red-eared sliders are more successful (survive longer) than those without a stripe.

While I'm still trying to figure the answer to the stripe question, there is ongoing scientific research into the bigger question of why red-eared sliders evolved human-like eyes, and some answers have been found through scientific research.
At first glance, most eyes look the same. There’s a small opening through which light passes. That light goes through the transparent liquid behind the lens and strikes the retina, a thin film of light-sensitive nerve cells that line the back of the eye. But there's actually a great deal more to vision than that.
Some animals, like humans, cats, and owls, have their eyes facing forward, while in some species the eyes face sideways, like cows and zebras. That distinction, while superficially simple, betrays complex underlying musculature.
VOR
That's because most animals have what's called a vestibulo-ocular reflexor VOR. That's the reflex that allows you to maintain your focus on a part of your visual field even while your head moves. If you rotate your head to the right, your eyes rotate left to compensate. (Not all animals have a VOR. Some birds, like chickens and pigeons, lack the reflex, which is why they bob their heads while they walk. It's a different solution to the same problem.) Without the ability to stabilize the world, we'd all get seasick very quickly.
While animals with forward-facing and sideways-facing eyes both have VORs, it works slightly differently. That is, the different muscles that control the eye do their work different ways. In forward-facing mammals, for example, the superior oblique muscle rotates the eye to the side, away from the nose. In mammals with eyes on the sides of their head, the same muscle instead does the opposite: it rotates the eyes inwards, towards the nose. These processes, called abduction and adduction, respectively, are two of the mechanisms that comprise the VOR.
Scientific Research
In 2006, Saint Louis University School of Medicine researchers Michael Jones and Michael Ariel discovered that red-eared sliders (Trachemys scripta elegans),  like my "Redneck," have eye muscles that work as if they were front-facing mammals despite having lateral eyes. That is, when the researchers stimulated the the superior oblique muscle, the eyes rotated outwards, rather than inwards. That surprise led Jones and Ariel to explore this puzzling finding by looking into the physiology, anatomy, and behavior of this peculiar turtle's eyes. That study, led by J. R. Dearworth Jr. of Lafayette College, Parasympathetic control of the pupillary light responses in the red-eared slider turtle.  Veterinary Ophthalmology Vol 10, issue 2, pp 106-110, March 2007, and others by Dearworth,  led to the conclusion that these turtles eyes are uniquely evolved.
One thing that sets these turtles apart from other types of turtles is that their visual fields change when they retract their heads into their carapaces. The turtles' shells restrict their peripheral vision and limit their head mobility. As a result, when their heads are retracted, their eyes are more like those of forward-facing mammals, and when extended, their eyes are more like those of side-eyed mammals. That's a unique challenge for the VOR, because it has to allow the turtles to maintain a stable field of vision both when their heads are extended and when they are retracted into their protective armor.
Did these evolutionary quirks have something to do with predation?  Raccoons will prey on slider turtles if they can catch them.  Red-eared sliders are the only turtle that can completely retract their head into the carapace.
In 2006, Jones and Ariel discovered that the red-eared sliders' eyes behaved as if they were forward facing. In another study, they also looked at the anatomy and physiology of the eyes. It turned out that their ocular anatomy and physiology were also unique for turtles. 

Say I gave you the eye of a red-eared slider, but you had guess what animal it came from. Based on its anatomy, physiology, and behavior alone, you'd assume that the eye was from an animal with forward-facing eyes, like a human. And you'd only be half right, since the turtles spend a lot of time with sideways-facing eyes.
Redneck and Evolution
Evolution was faced with a unique problem: an animal whose eyes usually face sideways, but sometimes face forwards. Each type of animal - forward-facing or sideways facing - evolved it's own method for achieving the VOR; here's a critter that is both types at once. In order to maintain the VOR, the red-eared slider evolved eyes that work differently from every other species with sideways facing eyes.
What that suggests is that the muscles that control the red-eared slider's eye evolved according to the constraints imposed by their unique ability to completely retract their heads into their shells, something no other turtle can do. The result was a peculiar turtle with human-like eyes.

Reference

Dearworth J.R., Ashworth A.L., Kaye J.M., Bednarz D.T., Blaum J.F., Vacca J.M., McNeish J.E., Higgins K.A., Michael C.L. & Skrobola M.G. & (2013). Role of the trochlear nerve in eye abduction and frontal vision of the red-eared slider turtle, Journal of Comparative Neurology, 521 (15) 3464-3477. DOI:10.1002/cne.23361
Abstract
Horizontal head rotation evokes significant responses from trochlear motoneurons of turtle that suggests they have a functional role in abduction of the eyes like that in frontal-eyed mammals. The finding is unexpected given that the turtle is generally considered lateral-eyed and assumed to have eye movements instead like that of lateral-eyed mammals, in which innervation of the superior oblique muscle by the trochlear nerve (nIV) produces intorsion, elevation, and adduction (not abduction). Using an isolated turtle head preparation with the brain removed, glass suction electrodes were used to stimulate nIV with trains of current pulses. Eyes were monitored via an infrared camera with the head placed in a gimble to quantify eye rotations and their directions. Stimulations of nIV evoked intorsion, elevation, and abduction. Dissection of the superior oblique muscle identified lines of action and a location of insertion on the eye, which supported kinematics evoked by nIV stimulation. Eye positions in alert behaving turtles with their head extended were compared with that when their heads were retracted in the carapace. When the head was retracted, there was a reduction in interpupillary distance and an increase in binocular overlap. Occlusion of peripheral fields by the carapace forces the turtle to a more frontal-eyed state, perhaps the reason for the action of abduction by the superior oblique muscle. These findings support why trochlear motoneurons in turtle respond in the same way as abducens motoneurons to horizontal rotations, an unusual characteristic of vestibulo-ocular physiology in comparison with other mammalian lateral-eyed species. J. Comp. Neurol. 521:3464-3477, 2013.


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