Here’s a picture of some animal pupils from National Public Radio. The website showed them because they’re the subject of a new paper by M. S. Banks et al. in Sciences Advances (reference below; free download). The paper asks an interesting question: why do the pupils of vertebrate species vary so widely in shape? (Supplementary material, including database and movies, can be found here.)
Now the paper is long and complicated, with lots of simulations and math, but the upshot is pretty simple: animals tend to have vertical pupils if they are nocturnal “ambush” predators and aren’t too tall, while animals that have horizontal pupils tend to be prey that need to detect predators approaching them and also to scan the surrounding terrain to find a good escape route.
These conclusions come from surveying 214 terrestrial species and gathering information about their pupal shape, when they were active, and their mode of foraging. This was combined with optical and mathematical analysis to determine the optimal shape to see under different conditions.
The plot below shows three modes of foraging (herbivores, active predators who search around for their prey, and ambush predators who remain stationary before attacking)—all plotted against pupil shape. You can see that there’s a strong relationship between pupil shape and foraging mode: herbivores tend to have horizontal pupils, active predators circular and subcircular pupils, and ambush predators vertical pupils. (Each species is a separate data point.)
The bulk of the paper is taken up with a complicated analysis of why different foraging modes should select (evolutionarily) for pupils of different shape. I’ll summarize the results very briefly; readers who seek further analysis should consult the original paper.
Vertical slit pupils. It turns out that having a vertical slit in low light gives ambush predators an advantage in calculating the distance to a prey item. (Remember, these predators must accurately gauge the distance to a prey item before they strike.) The calculations suggest that a vertical slit is better at maximizing the blur of objects that aren’t in focus. That is, it helps the predator gauge the distance to a prey by seeing which aspects of the landscape are blurred and which are not. The vertical pupil also aids in stereopsis: the comparison of images from different eyes that is also used to judge distance to prey. In general, then, distance-judging, which is vital if an ambush predator is to eat, is maximized in low light by having a vertical slit. For such a predator, those that can best judge distance to prey are those that get more noms, and thus leave more offspring. And that, O Best Beloved, is why your small, ambush-predator cat has eyes with vertically slit pupils.
That said, the advantage of having a vertical slit, for complicated optical reasons, diminishes as the eye gets higher off the ground. So the authors made and tested a prediction made from theoretical considerations:
We predict, therefore, that shorter frontal-eyed, ambush predators will be more likely to have a vertical-slit pupil than taller animals in that niche.
We evaluated this prediction by examining the relationship between eye height in these animals and the probability that they have a vertically elongated pupil. There is indeed a striking correlation among frontal-eyed, ambush predators between eye height and the probability of having such a pupil. Among the 65 frontal-eyed, ambush predators in our database, 44 have vertical pupils and 19 have circular. Of those with vertical pupils, 82% have shoulder heights less than 42 cm. Of those with circular pupils, only 17% are shorter than 42 cm.
Nearly all birds have circular pupils. The relationship between height and pupil shape offers a potential explanation. A near and foreshortened ground plane is not a prominent part of birds’ visual environment. The only birds known to have a slit pupil (and it is vertically elongated) are skimmers [Rynchopidae]. . .
Foxes, for example, have vertically slit pupils, but the taller wolves have round ones.
Horizontal slit pupils. Based on a similar analysis, the authors found that, in theory, terrestrial animals that are prey should have horizontally slit eyes. For that shape of pupil enables them not only to get a wide look at the horizon around them, thus detecting the presence of predators, but also scope out escape routes by surveying at the landscape. As they say:
Most terrestrial lateral-eyed animals are prey, so their adaptive strategy is to detect predators approaching along the ground and to flee quickly to avoid capture. The visual requirements for this strategy are striking. On the one hand, these animals must see panoramically to detect predators that could approach from various directions. On the other hand, they must see sufficiently clearly in the forward direction to guide rapid locomotion over potentially rough terrain. In both cases, the regions of greatest importance are centered on or near the ground.
Their analysis shows that horizontally elongated pupil gives a better panoramic view of the ground. This led to another prediction. If this is the reason for such a pupil, then if the animal changes its head alignment, as when grazing, it should still keep its eyes horizontal so the pupils align with the horizon. And this is what they observed when looking at grazers, which show this “cyclovergence.”
Conclusion: The authors have made a good hypothesis that seems to explain well the diversity of pupil shapes among animals based on both their foraging mode and time of activity.
I see one potential problem: the correlations are based on many species that are closely related (there are many snakes, for example), so each data point does not necessarily represent an independent act of natural selection molding pupal shape, which is what their correlation in effect assumes. In reality, animals could have inherited their pupil shape from a common ancestor and not evolved it independently, so using, say, ten related snakes is not the same as documenting ten independent events of evolution. This problem, one of “phylogenetic inertia,” reduces the authors’ statistical power. (As an example, we can’t claim that all cat species independently evolved sharp canine teeth to kill their prey and rip apart its flesh. So you can’t use every cat species as an independent test of whether sharp canines are associated with ambush predation.)
They recognize this problem and try to overcome it by giving instances in which animals have diverged from the pupil shape of their ancestors in the predicted direction based on changes in lifestyle. The ancestral canid, for instance, is thought to have been an ambush predator active at several times of day, and having subcircular pupils. The authors note that vertical slit and truly circular pupils evolved independently twice each within the canids, and in the direction expected from their activity periods and hunting patterns.
This does show that “phylogenetic inertia” can be overcome, and that the data points are to some extent independent. But we don’t know how independent, for showing some independent evolution doesn’t tell us how often phylogenetic inertia has rendered other points non-independent. As far as I can see, the authors have recognized the problem of non-independence and dealt with it the best way they can, but haven’t fully overcome the problem.
What they need is an analysis that uses only those data points known to represent independent cases of evolution (Allen Orr and I did this in our work on speciation in Drosophila). I’m not sure it’s possible in this dataset, but until it’s done, the statistical strength of their data remains in question. I think the authors are probably right in their conclusions, and I really like the paper, but I’d also like to see a statistical analysis that is based on “phylogenetically corrected” data.
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Banks, M.S. et al. 2015. Why do animal eyes have pupils of different shapes? Science Advances, Aug. 7, 2015, online.
