In The Eyes of the Aye-ayes

18 September 2007

Or, “Officer. Of course my pupils are dilated. I’m nocturnal…hey, check out all those colors….”

Aye-Aye trip

Painting by Joseph Wolf (c. 1863), crudely distorted by me.
Original at Wikimedia Commons.

According to Malagasy lore, when an Aye-aye (Daubentonia madagascariensis) fingers you with his hyper-elongate middle digit your number’s up. You know, kind of a reverse E.T. effect. This is but one of several compelling reasons not to take hallucinogens in Madagascar1

No doubt about it, Aye-ayes are trippy critters even without any entheogenic assistance. Early naturalists originally thought this strange arboreal animal was some kind of effed up nocturnal squirrel, given its rodent-like incisors and long bushy tail. Today, it’s regarded as an exceptionally primitive primate primate (zing), one that diverged from our own lineage some fifty-odd million years ago. In fact despite it’s otherworldly appearance, the lifestyle of Daubentonia may not be far removed from that of our early primate ancestors2.

Aye-ayes do most of their foraging at night, employing a unique acoustic strategy to find prey. Like Larry Craig in a airport bathroom, they use an elaborate repertoire of finger taps to search for insect larva tunneling through rotten wood (sound clip here). When a tasty, wriggly morsel is detected, the primate then uses it sharp incisors to peel away the bark and then fishes out the grub with its hypertrophied middle finger.

In spite of this specialized tool kit, Aye-ayes also dine on a wide range of other invertebrate prey and fruit, even raiding human food crops. This latter habit, along with the whole harbinger of death thing, has lead to a rocky relationship between Aye-ayes and the human inhabitants of Madagascar. The Aye-aye is now critically endangered due to direct persecution and even more so due to habitat loss and degradation. It’s not at all certain that Daubentonia madagascariensis won’t go the suffer the same fate as it’s larger cousin Daubentonia robusta, the Giant Aye-aye which went extinct in the early 20th century.

Aye-ayes have been in the news lately, thanks to a new study from Perry et al. appearing in the Journal of Molecular Biology and Evolution. This study looks at the genes involved in the production of opsins, the proteins used to by vertebrates to absorb light in the retina. Opsins come in two varieties. Rhodopsin (shown below) is used by the rods as a general light detector and is important in night vision. Photopsins (or iodopsins) are used by the cones for color vision.

 

Computer model of Rhodopsin, an important vision protein.

The new study found no evidence of degradation in the color sensitive opsin genes in the Aye-aye. This is somewhat surprising because night light levels are so low that color vision shouldn’t be possible. The genes that control color vision should be of little value to a nocturnal primate and would be expected to accumulate mutations overtime without selective correction.

Even more surprising, these genes appear to have undergone “purifying selection.” In other words, they aren’t just strangely conserved anachronisms, but are in fact actively evolving under some selective pressure. This suggests the opsins play some important functional role in the Aye-aye.

As per usual, the press release (and hence most news reports) herald this as a totally unexpected and shocking discovery. And, as per usual, this isn’t strictly the case. In fact, in a way, the new study confirms predictions made 10 years ago by Nei et al. in the, wait for it…Journal of Molecular Biology and Evolution.

In a fascinating paper entitled “Color Vision of Ancestral Organisms of Higher Primates” (pdf) Nei et al. looked at the opsin genes in a wide range of primates as well as in four ‘outgroup’ vertebrates very distantly related to primates (goat, chicken, anole and gecko). Toward the end the paper, the authors note that,

Recent studies of opsin genes indicate that the blue and red/green genes of primates have coexisted in the genome for more than 500 Myr and, thus, the red/green gene did not become extinct during the long nocturnal stage of mammalian evolution. (Nei et al. 1997)

Hm. Then things get even weirder. The authors then discuss a study of blind cave fish that found their color vision genes to be highly conserved and even undergoing purifying selection (e.g. actively evolving). They go on to postulate that opsins may play an important role in controlling biological clocks (Bora? nudge nudge) and therefore could be vital even in organisms without color vision or even eyes3.

Multifunction in biology, especially in complex organs, is truly interesting as it hints at exaptive shortcuts up “mount improbable.” Mammals probably evolved from organisms with decent color vision, but most living mammals apparently don’t see color well. The most notable exception is primates and it was always supposed that primates had to ‘reinvent’ color vision as they transitioned from nocturnal insectivores or generalist feeders to diurnal fruit and leaf eaters.

Nei et al. hint at a possible backdoor route, with early primates retaining much of the genetic “instructions” for color vision because they were serving an additional important function in setting biorhythms. When the lifestyle changes that favored color vision rolled around, primates would have ‘simply’ had to deploy the opsin genes back into their color detecting role. All of this is entirely speculative of course, but damn fun!

In their new study on Aye-aye opsins, Perry et al. take a different tack interpreting the apparently functional genes as an indication of something like night-time color vision!

We speculate that dichromatic nocturnal primates may be able to perceive color while foraging under moonlight conditions, and suggest that behavioral and ecological comparisons among dichromatic and monochromatic nocturnal primates will help to elucidate the specific activities for which color vision perception is advantageous. (Perry et al. 2007)

Of course, the two hypothesis aren’t necessarily contradictory, opsins may provide some night-time visual function and a biorhythmical one. We clearly have much, much more work to do in working out the patterns of visual evolution in our primate brothers and sisters and mammals at large. Of course, if we lose the Aye-aye first we’ll be losing an important witness to this history, and more importantly we’ll lose a fascinating creature that deserves to be preserved.

REFERENCES

Nei, M., J. Zhang and S. Yokoyama; 1997. Color Vision of Ancestral Organisms of Higher Primates. Mol. Biol. Evol. 14(6):611-618

Perry, G. H., R. D. Martin and B. C. Verelli; 2007. Signatures of Functional Constraint at Aye-aye Opsin Genes: The Potential of Adaptive Color Vision in a Nocturnal Primate. Mol. Biol. Evol. 24(9):1963-1970

 

1Fine, since you asked here are some others:

  • experiencing an overwhelming urge to hug an Alluaudia.
  • trying to swim to Mozambique to prove a biogeographical point.
  • freaky-ass midnight lemur calls.

2For those keeping score at home, there are a number of interesting purported Aye-aye analogs in the fossil record. One of these was the plesiadapid and close primate relative Chiromyoides. Even more Aye-aye like were the Apatamyidae who had sharp incisors and elongate digits and almost assuredly pursued a lifestyle quite similar to Daubentonia. I’m fortunate enough to have done my own small part to add to the record of the apatamyids by finding a few probable apatamyid teeth when I worked as an intern at Fossil Butte National Monument.

Perhaps most amazingly there were even Aye-ayeish dinosaurs! Scansoriopteryx from late Jurassic china was an arboreal feathered-dinosaur with elongate fingers. It’s tempting to imagine the precursors (or should I say prevolancers?) of bats and pterosaurs using their elongate fingers to fish out grubs before exapting them it the frames for flying membranes, but I’m not aware of any fossil evidence to support this.

3Another organ that plays a major role in biorhythms and circadian cycles also had an optical origin. The pineal gland, which produces melatonin and regulates our internal clocks as well as some aspects of puberty is found deep within the human brain. It probably began however as a photoreceptor near the top of the skulls of ancient ancestors. In fact, in some modern organisms the pineal ‘eye’ remains near the roof of the skull and may actually be light sensitive.

The pineal gland is also supposed to play a role in transcendental meditation, according to various new agers and was regarded by Descartes as the seat of the soul. It’s also been (controversially) tied to LSD function in the brain and some have even suggested that it produces our brain’s own DMT analog. Oh, yeah…full circle baby…

7 Responses to “In The Eyes of the Aye-ayes”

  1. laelaps Says:

    This is perhaps one of the most excellent posts I have ever read; you should definitely submit it to the Open Lab aggregation that Bora is heading up again. I had just learned the other day that tarsiers, too, seem to conserve diurnal traits in their eyes (i.e. a pit in the back of the eye filled with cones), and they have not developed a tapetum lucidum like the strepsirhines (i.e. lemurs, bush babies, the aye-aye, etc.). Given that a strpsirhine seems to show a similar conservation of traits that would probably be suggestive of a diurnal ancestry, I’d be interested to see what those opsins and selected traits are doing for it.


  2. […] Neil has one of the most singularly excellent posts I have ever seen up over at microecos about the eyes of the Aye-Aye, a very rare and bizarre endangered strepsirhine primate that is truly unusual (and, as W.E. le […]

  3. DDeden Says:

    That a nocturnal mammal could lose it’s color vision isn’t unexpected, but should? Why? Even the faintest moonlight is still reflectable.

    Light in the eyes causes melanin production, according to the book Survival of the Sickest, a recent popular medical book. Melanin is antibiotic in addition to being a pigment, so nocturnal mammals may get a health bonus by being more sensitive to moonlight. Somehow.

  4. Neil Says:

    Brian: Thanks again for the kind words and the link, I will certainly consider submitting to the Open Lab. I’d really like to hear Bora’s thoughts on this stuff given his biorhythmic persuasions.

    DDenden: Thanks for the comments. Conventional wisdom has generally said that vertebrate cones don’t work well by moonlight, nocturnal animals instead usually rely on non-color sensitive cones to see at night.

    Recently however, researchers in Sweden demonstrated that some geckos are able to distinguish hues by moonlight, apparently the first proof of color night vision in a vertebrate (moths have been shown to have good night color vision as well): Roth and Kelber 2004 (full text available).

    The new Perry et al. study hints that they think the retained opsin genes in the aye-ayes may allow them to see color in the dark, but to my knowledge this hasn’t been demonstrated.

    Of course, even nocturnal creatures may get some benefit to being able to see color in the daytime, being able to see diurnal predators for instance. Some have proposed that color vision in primates evolved as a defense mechanism against predators, something I’m a little skeptical about but it is certainly a possibility.

    Your melanin suggestion is interesting. Are opsins/cones/polychromacy specifically involved in the melanin production? If so, this might be another good hypothesis for why an animal might retain these traits even if it wasn’t using them for foraging or defense.


  5. I have been delving into the world of color and have posted a few articles myself.

    This is interesting blog.


  6. […] you’ve surely guessed by the sycophancy, a microecos post, In the Eyes of the Aye-Ayes, has been selected to appear in the science blogging anthology.  For once, I’m […]


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