Adaptation of the Week – the Insect Dorsal Ocelli
Dog Day Cicada (wikipedia commons)
There's one particular event of every summer in the South that I always await with great anticipation: the emergence of the millions of annual Dog Day cicadas (Tibicen canicularis).
It's not just the event itself that I love. The cicadas are certainly wonders in themselves; but for me, they are more than just insects of the order Homoptera - they are the standard-bearers of my favorite time of year: the "dog days" of summer. It's the time of year when the sun shines the brightest, heat covers the land as lazy dogs curl in cool digs in the shade, and Sirius - the Dog Star and the brightest in the sky - makes its appearance above the Southern horizon.
Spring is nice. Fall is fairly beautiful. Winter could be thrown to the dogs and I wouldn't bat an eye. But Summer? Ahh, summer is the incubator of my soul. When I'm in it, the warmth makes my happiness grow as ideas sprout from the imaginal discs of my imagination.
It is in no small part the fact that cicadas choose late summer to burst newly reformed into the world, leaving their former larval stages behind, that they receive my respect. I like their style.
But they deserve my awe for many other reasons beyond our shared love of summer. Many of us are well aware of the cicadas' prolonged existence as grubs feeding amongst the roots of trees for years, the exact time dependent on the particular species. Many species have synchronized both their development and life-cycles to such a degree that they burst forth from the ground all at once after 13 or 17 years of sucking sap as larvae. They enjoy an incredibly short adulthood, frantically mating for a few weeks, followed by death en masse (much like the death orgies of the market squid).
The advanced life-cycle adaptations of the cicadas and the timing thereof are deserving of their own tribute. However, the focus of this article lies elsewhere in our cicadan wonders. For the cicada contains an organ prevalent among many orders of insects that many of you have likely never even heard of: the "dorsal ocelli".
"There are no more other worlds to conquer!" - Alexander the Cicada
"Did I play my role well? If so, then applause, because the comedy is finished!" - Cicadan Emperor Augustus
Dorsal Ocelli
I took the images above last summer after the poor (or perhaps ecstatically happy) little cicada had already performed its life duties. Shortly after emerging and mating, cicadas slowly become lethargic, then immobile, and finally they simply die. This individual had reached the immobile stage. It was still alive when these pictures were taken, but days later it had died - remaining in the exact same location and position you see it in now.
Now, look more closely. You may notice its head is bejeweled with three orange organs. These are its dorsal ocelli (singular: ocellus).
"It is during our darkest moments that we must focus to see the light." - Cicada Benson
The ocellus is a strange and still quite mysterious organ. It is present throughout the insect world, but only erratically. Despite their ongoing mystery, the organs have been studied fairly extensively since the 1920s and 30s. The following distribution of ocelli among the insects (for you entomologists) is from The Function of the Insect Ocellus1, by D. A. Parry in 1947:
ORTHOPTERA : always present in Acriidae and Gryllidae; sometimes present in Blattidae, Mantidae, Tettigoniidae; not present in Grylloblattidae. DERMAPTERA : absent. PLECOPTERA : two or three present. ISOPTERA: present. EMBIOPTERA: absent. PSOCOPTERA: sometimes present. ANOPLURA: absent. EPHEMEROPTERA: present. ODONATA: usually present. THYSANOPTERA: present. HEMIPTERA: great variation. Some families separated on the presence or absence of ocelli. Several families in which some genera possess ocelli and some do not. NEUROPTERA: conspicuous in some families, absent in others. MECOPTERA: some genera with ocelli, others without. TRICHOPTERA: some families with ocelli, others without. One family including six genera with ocelli and two without. LEPIDOPTERA: sometimes present. COLEOPTERA : absent except in a few species not all in the same family. STREPSIPTERA : absent. HYMENOPTERA: usually present, but sometimes absent in the Vespoidea. DIPTERA: sometimes present. APHANIPTERA: uncertain.
Many species it seems have found great use in the ocellus, as evidenced by its retention throughout much of the Insecta class, while others have completely disposed of it.
But what is it?
“If the sight of the blue skies fills you with joy, if a blade of grass springing up in the fields has power to move you, if the simple things in nature have a message you understand, Rejoice, for your soul is alive.” - Eleanora Cicada
Essentially, the dorsal ocellus is an eye. But dorsal ocelli are not like the large compound eyes always present nearby. Nor are they like our own.
Early studies measuring the focal depth of various ocelli lenses all came to the conclusion that ocelli cannot focus forms on their simple retinas. It has since been shown that this is mostly true, except with some dragonflies which apparently may be able to form images with their ocelli.
What dorsal ocelli can do quite well is sense light. In fact they are much more sensitive to light intensity than the main compound eyes.
Studies in the 40s showed that ocelli nerve impulses were inhibited by light. When the ocellus was occluded, signals would then propogate down the large nerves to ganglia. Essentially, if a shadow passed over the ocellus, signals fired. And because the nerves are very large in diameter (often the largest nerve fibers), they are very fast.
It was additionally shown that light perception in the ocelli alone could not lead to reflexive movement. Thus it was suggested, and some still hold, that light perception (or shadow perception) acts to set the excitatory potential of the nervous system. Thus, if a shadow passes overhead, the nervous system would be primed to react to visual stimuli from the compound eyes.
Advances in Insect Physiology
More recent studies have shown that ocelli are intricately involved in orientiation to light (including UV), particularly to the horizon, and so are integral parts of the flight stabilization machinery, which makes sense when considering that most flying insects have ocelli.
Again, research in dragonflies indicate that the ocelli can form images with very wide fields, and can sense motion. There are other indications that ocelli may play a role in circadian entraining.
To my knowledge, no physiological research has been conducted on the cicada ocelli. Regardless, it appears that whatever the function of the ocellus, it is intricately and physically intertwined with the circuitry of vision from the compound eyes.
The ocellus represents just one more example - among myriads - of a sense that we as humans can hardly fathom. It is hard enough to imagine perceiving the world through thousands of individual ommatidia (the many eyes within a single insect compound eye). Add to that a complex system of light perception wired to the eye circuitry to aid in orientation, flight stability, or to prime the brain for visual stimuli. Such perception is impossible to even imagine.
It's clear from my limited research that science has yet to fully explain the purpose of these beautiful adaptations, despite the prevalence of their existence. It just goes to show that we have not come close to deciphering all the mysteries of life - even mysteries that have stared us in the face for a century.
So this summer, as the cicadas raise their eyes and dorsal ocelli to the summer sun for the first and last time, take a second to give them a closer look. You may just find yourself in awe of these photosensitive jewels.
References
- Parry D.A. (1947) The Function of the Insect Ocellus. Journal of Experimental Biology. Vol. 24. Nos. 3 & 4. pp. 211-219 (pdf)
- Beament J.W. L. (1966) Treherne J.E. Advances in Insect Physiology. Academic Press. (book)
- Berry R.P., Stange G., Warrant E.J. Form vision in the insect dorsal ocelli: An anatomical and optical analysis of the dragonfly median ocellus. Vision Research. Volume 47, Issue 10, May 2007, pp. 1394-1409.
- Simple eyes in Arthropods. Wikipedia.org
Previous Adaptations of the Week:
Flatfish Eye Development – Video Update
If you haven't read my piece on Flatfish Eyes & Recapitulation Theory, you should check it out. For those of you who have read it, I updated it with the following AMAZING morph animations of flatfish development that I somehow missed before (much thanks to Adrian Thysse, FCD of Evolving Complexity for pointing these out to me).
WANDERING EYES from Science News on Vimeo.
FROM FRY TO FISH from Science News on Vimeo.
Adaptation of the Week – Flatfish Eyes & Recapitulation Theory
Most biologists at one time or another in their training have learned of the 19th century theory expounded upon by Ernst Haeckel called "Recapitulation Theory".
The theory's thesis: "Ontogeny recapitulates phylogeny." Don't worry - it's not as complicated as the biological jargon might imply.
Ernst Haeckel's Drawings (1892 Romane copy). Note: Haeckel oversimplified these drawings. I use them here as a simple illustration of the concept of developmental similarity.
The idea boils down to a simple one - one that seemed to make sense in light of the fact that the science of developmental biology had only just begun from a systematic standpoint. The idea: if you watch an organism develop from an embryo to an adult, you can watch it slowly move through the evolutionary steps that had created it. That is: development repeats evolution.
So a human embryo would first look like a fish, then a reptile, then a mammal, and finally a human. Of course, we now know that in a literal sense, the theory is completely and utterly wrong. No stage of human development, or of any other organism, correlates with a discrete step in evolution.
We are never fish. (Though we do have embryonic tails).
However, that doesn't mean that there aren't kernels of truth to the idea, if applied loosely. Take the most famous and classic example: embryonic human gills. You may have heard yourself that humans have gills as embryos. Unfortunately this claim arises from misconception and incomplete understanding of developmental biology. Humans do not - ever - have gills. But as embryos we do have "pharyngeal arches." These are little bumps around what you might consider the neck area of a developing embryo (see Haeckel's drawings above). And these little mounds of tissue do in fact remarkably resemble similar mounds found in fish - mounds that in fish develop into gills (Note: Haeckel vastly oversimplified these drawings. I use them here as a simple illustration of the concept of developmental similarity. See: http://zygote.swarthmore.edu/evo5.html. Thanks Bjørn!).
One of the amazing aspects of developmental biology that much of the public does not generally understand is that evolution does not occur by adding new organs, appendages, or tissues to adult animals (whether through gradual steps or not). Evolution works by slowly sculpting the early embryonic clay of an organism.
Fish evolved these gill pouches as embryos - pouches that could then be sculpted into gills. As evolution waltzed and hopped along at its geological pace, genetic mutations began to change how these little mounds were sculpted, such that now in humans, these arches are sculpted into various parts of the face and head. A genetic program was already in place to control the shaping of the pouch. All that natural selection did was slightly tweak that program. For example, instead of a group of cells moving one direction, they moved another. Instead of becoming blood vessel cells, they became cartilage or bone cells.
Thus, while we now understand that we are not witnessing evolution in miniature during development, we are seeing pieces of our evolutionary history - little remnants that remind us of our relationships to our ancestors and also help inform us on what morphogenetic processes underlie evolution.
Which brings us to our adaptation of the week: the freaky asymmetric eyes of the flatfish.
Flatfish (www.seawater.no)
Most people have probably seen a flounder - one member of the flatfishes. They have adapted to lie amongst the silty ocean bottom, hidden from predators and prey, flat on their sides. For a normal fish this might be maladaptive - they would constantly have one eye buried in the sand. Of course the negative of being one-eyed might be offset by being much more camouflaged and undetectable.
Luckily for the flounder, the eye that should be buried in the sand has moved around its forehead so that both eyes are on one side.
The flatfish eye served as one line of attack against natural selection back in the day - and Darwin himself didn't quite know how to answer the charges. Evolutionary gradualism would predict that through successive steps, the eye slowly moved upward toward the forehead and eventually to the other side of the face. But what advantage could a slightly moved eye give, if it still was on the wrong side? Alternatively, as Richard Goldschmidt postulated in the 1930s and 40s, perhaps a single monstrous freakfish was born with both eyes on one side, and this allowed it to lie flat without losing half its vision. It could have then survived and had lots of little freak fish babies of its own.
So how did the flatfish become the strange creature it is now? Let's first look at the developmental biology of the flatfish eye.
WANDERING EYES from Science News on Vimeo.
FROM FRY TO FISH from Science News on Vimeo.
Flatfish Metamorphosis (Schreiber 2006)
It's been know for quite some time that flatfish larvae look like perfectly normal, symmetrical, and upright fish. The picture to the right is from a study by Alexander Schreiber in the Journal of Experimental Biology from 2006. As you can see, at early stages the larvae are normal, but progressively tilt and become horizontal as one eye moves across the face. He also showed in this study that eye movement and flattening behavior occur independently during development - but that's a much longer story.
Alright, so one eye gradually moves across the skull during development. What about during evolution? Do we have any clues as to the steps involved? Well, as many biologists know, the fossil record has now answered the question for us.
In a well-known study that was published last summer in Nature and received much media attention, Matt Friedman showed findings from a series of fossils delineating a clear gradual evolution from symmetrical to asymmetrical flaltfishes. (For excellent in-depth coverage looking at this study and the debate over flatfish evolution, see one of my favorite science bloggers, Ed Yong at Not Exactly Rocket Science, and also see the popular science writer Carl Zimmer at The Loom, and GrrlScientist at Living the Scientific Life).
Flatfish Evolution (Friedman 2008)
The evolution of the flatfish eye seems to mirror what we see during development. Thus, here we have a case of ontogeny appearing to recapitulate phylogeny quite wonderfully. There are many excellent examples of this throughout the biological world, though few that show such incredible similarity between the two processes of development and evolution. Nonetheless, this isn't really evolution we're watching during flatfish development - we're merely seeing how slight changes of the developmental programs are themselves responsible for the changes we see over time through evolution. Generally speaking, earlier developmental processes appear much more similar across varied species than later processes.
Development is in fact one of the primary constraints against evolution.
So while you were never a fish, you still showed remnants of fishy development during your own development. For it was these fishy developmental process that allowed the evolution of your own.
Scientific References:
- Schreiber AM. Asymmetric craniofacial remodeling and lateralized behavior in larval flatfish. J Exp Biol. 2006 Feb;209(Pt 4):610-21.
- Friedman M. The evolutionary origin of flatfish asymmetry. Nature. 2008 Jul 10;454(7201):209-12.