In the forests of South America lives the unusual but aptly named owl monkey, or douroucouli. You could probably guess by looking at its large round eyes that it’s nocturnal, and indeed, it is the only monkey to be mostly active at night. But its eyes have many adaptations for such a lifestyle, beyond a large size.

The owl monkey’s retinas are 50% larger than those of a day-living monkey of similar size, like the brown capuchin. The proportions of different cells in their retina are also different. Owl monkeys have relatively few cone cells, which are responsible for colour vision and fewer ganglion cells, which process the signals from the cones. In contrast, they have many more rod cells, which are far more sensitive than cones and function best in low light, and rod bipolar cells, which transmit signals from the rods.

This is an eye that has sacrificed sharpness and colour for sensitivity. Nocturnal mammals the world over have developed a very similar suite of adaptations and according to Michael Dyer and Rodrigo Martins, these may be easier to evolve than you might think.

All of the cells in the retina are produced by a small group of stem cells called retinal progenitor cells (RPCs). As an embryo grows, its RPCs go through cycles of division, still maintaining their “stemness”. At some point, they leave this cycle and commit to becoming one of the various types of retinal cells. The fate they choose depends on when they leave the cycle. Those that are “born” early turn into cells that are important for daylight vision, such as cones and ganglions. Those that exit late become cells that play a greater role in night-vision, including rods and their bipolar cells.

This quirk of organisation means that the retina’s cells are always produced in a very specific order, with those that grant good night-vision cells appearing later. The upshot is that the owl monkey has been able to adapt its retina to see in the dark simply by tweaking the timing of its development. In its retinas, more RPCs commit to a particular fate later on in their cycle, producing fewer of the earlier types of cells and many more of the later ones. The result: an extra-sensitive retina with a complement of cells perfectly suited for nocturnal living, all triggered by a single change during development.  

The eyes of the owl monkey hammer home an increasingly familiar message – you can get big results by very subtly tweaking the way that bodies develop, without any need for large-scale tinkering. Even the eye, an exceptionally complex organ, can be altered in a coordinated way, simply by shifting the timing of its development. It’s why the owl monkey, in a relatively short space of evolutionary time, has converted the daylight-loving eyes of its ancestor into a nocturnal model.

More and more, evolutionary biologists are discovering examples where evolution has squeezed out a tremendous amount of variation by tinkering with the timing of development. Snakes, for example, have hundreds of vertebrae, while mice have just 50 and humans, just 33. Each vertebra is formed from an embryonic structure called a somite and there’s an internal clock that governs how quickly these somites are formed. In snake embryos, this clock ticks into overdrive so that it develops a hefty collection of smaller somites. That leads to more vertebrae. The owl monkey’s super-sensitive retinas are just another example of this phenomenon.

Dyer and Martins, from the St Jude Children’s Research Hospital in Memphis, studied the RPCs of owl monkey and capuchin foetuses, as their retinas developed. They kept an eye on these cells using a mildly radioactive chemical called bromodeoxyuridine, which gets incorporated into the DNA of dividing cells. This marker revealed that an owl monkey’s RPCs start producing the various cells of its retina much later (and over a shorter period of time) than those of a capuchin’s. This delay means that the owl monkey produces fewer of the earliest cells in the sequence and more of the later types, including the rods that are so vital for night-vision.

The shift in timing could well explain another feature of the owl monkey eye that sets it apart from other monkeys and apes. It lacks a fovea, a spot at the centre of human retinas where our vision is sharpest, where cone cells are abundant and where rods are virtually absent. But as the owl monkey’s retina develops, its dearth of cones and its surplus of rods mean that this focal point never forms. Indeed, the owl monkey has little need for a fovea – acuity is a minor issue when one has to worry about sensing any light at all.

The owl monkey evolved from diurnal ancestors around 15 million years ago. During this relatively short time, it has developed most of the adaptations that other nocturnal mammals have. Its eyes have become bigger and it has lost the third cone cell that other monkeys and apes use to detect light at the red end of the spectrum. But all of its other adaptations – more rods, fewer cones, no fovea – could well be the result of a single change to its development.

It’s a wonderfully elegant system because it means that the proportions of all types of cells in the retina can be adjusted in a coordinated way. Dyer and Martin point out that the alternative explanation – that the fate of each type of cell is controlled individually – isn’t ruled out by their work, but is “an unlikely and rather cumbersome possibility”. 

But why should the retina’s development go through such an orderly sequence, where diurnal and nocturnal features are so conveniently grouped? Some will no doubt choose to read too much into this, but Dyer and Martins think that the advantages of such organisation are “not hard to discern”.

All primates, owl monkeys included, come from a long line of animals that have crossed over from diurnal to nocturnal living and back again, many times over.  This ecological flip-flopping would have filtered out programmes of development that make it easier to cross between the two ways of life. Such programme would produce cells that are relevant to each one at different times, and ensure that boosting one group downplays the other – exactly the system found in mammalian retinas.

Reference: Dyer, M., Martins, R., da Silva Filho, M., Muniz, J., Silveira, L., Cepko, C., & Finlay, B. (2009). Developmental sources of conservation and variation in the evolution of the primate eye Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.0901484106

The amazing ways in which animals see the world

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May 21st, 2009 Tags: capuchin, cone, douroucouli, eye, monkey, night, nocturnal, owl monkey, retina, rods, vision
by Ed Yong in Animals, Evolution, Eye evolution, Mammals, Monkeys | 5 comments | RSS feed | Trackback >