I owe the following example of evolutionary adaptation to the always amazing evolutionary and developmental biologist Dr. Sean B. Carroll, from his lecture "Making of the Fittest" for the Darwin College - Darwin Lecture Series, available at iTunes U (I highly recommend everyone give it a listen).
Imagine that you are a fish - exothermic and thus unable to regulate your own body temperature - and the contingent foibles of natural history have all conspired to leave you and your kind in the frigid oceans of the Antarctic just as they are beginning to reach the freezing point (10-14 million years ago).
You like the cold and are well adapted for it, but these temperatures are beginning to give even you - a master of the cold - the icthy chills.
Now imagine that the hands of mother nature have given you the tools to change your own genetic code, and thus your nature, allowing you to make yourself even more suited for waters that are 2 degrees celsius below the freezing point of pure water.
What would you do? Would you inject your DNA with a molecular antifreeze? That seems like a reasonable addition - one we will get to momentarily.
But if you were a genius of bioengineering would you reach out a molecular scalpel and hack away the genes that allow the production of red blood cells, hemoglobin, and myoglobin, leaving only molecular fossils behind?
It doesn't seem like a particularly well thought out plan. But then again, neither you, the fish, nor mother nature are genius bioengineers. Fortunately for life, the forces of evolution still manage to get the job done, however sloppy the end results (yes, technically the job is never done - forgive my metaphor wearing thin).
In fact, natural selection performed just such a feat somewhere around 8.5 million years ago in the ancestors of a flock of related species in the Antarctic: the Channichthyidae icefishes (also known as crocodile icefishes or white-blooded fishes).
As we all know, liquids tend to become more viscous in the cold. Just compare maple syrup before and after refrigeration. Blood viscosity would have no doubt been an issue in the ancient ice fish ancestors, or at least one that could be improved upon. Normal vertebrate blood is filled with big, round, and red blood cells coursing through the blood vessels. Now imagine lowering the temperature of the blood below the normal freezing point of water - that's bound to create some significant resistance.
But aren't erythrocytes critical for carrying oxygen? How could an organism just dispense with them completely? As many scientists know, one of the great things about really cold water is that it can be packed with oxygen. Such is the case with the waters of the Southern Ocean, which are saturated with oxygen.
Thus, it seems that at some point, the icefish ancestors developed mutations in the pathways that result in red blood cell production. Furthermore, the species eventually acquired a deletion in the key genes of red blood cells: the alpha and beta hemoglobin genes. No longer could this fish produce hemoglobin.
As is often the case with evolution through loss of gene function, the deletion wasn't perfect. Almost all vertebrates have both hemoglobin genes lying next to each other within the genome. In most Channichthyidae icefishes, the beta hemoglobin gene has been completely deleted, along with all but the truncated end of the alpha hemoglobin gene (interestingly, these fish have lost their myoglobin gene as well)1. To quote the original paper by Near et al.:
"Despite the costs associated with loss of hemoglobin and myoglobin in icefishes, the chronically cold and oxygen-saturated waters of the Southern Ocean provided an environment in which vertebrate species could flourish without oxygen-binding proteins."
The upshot of all this is that the icefish has completely clear blood lacking in any erythrocytes - and they are the only species of vertebrates to have such a trait.
Of course, a few other supporting traits evolved as well. Their hearts are significantly larger than other fish hearts, and they pump 4 to 5 times larger volume of blood per stroke2. Their capillary beds have become much more dense as well to make sure all their tissues get adequate oxygenation. Of course, like amphibians that breathe through their skin, with the loss of red blood cells, those that were better able to absorb oxygen tended to outperform their cohorts. Thus they became scaleless as well.
As if these adaptive feats weren't cool enough (pun intended), the antarctic icefishes have evolved their own antifreeze as well3,4. What's amazing about this antifreeze (an Antifreeze Glycoprotein - or "AFGP") is that it represents one clear cut case in which a gene with a specific function has evolved into a separate gene used for a completely different function in a novel way. In the case of the icefish, the ancestral gene was a trypsinogen (a pancreatic digestive enzyme), which has been mutated and co-opted to be secreted and distributed throughout the body to act as an antifreeze. Specifically (for you biologists out there), the 5' secretory signal and 3' UTR sequences of trypsinogen were tacked onto an amplified nine nucleotide sequence from within the trypsinogen precursor to create the novel antifreeze peptide.
So here we have in the icefish's adaptation to the cold, at least one case of de novo creation of a novel gene with a new function from an old gene, as well as the loss of two other genes that have left genomic fossils behind to whither in the weathers of time.
It may not be the cleanest or best engineered solution to the problem of living in an Antarctic Hell (or perhaps Heaven from the perspective of the fish), but this messiness of evolution is precisely what makes it so incredibly beautiful.
- Near T.J., Parker S.K., Detrich H.W. A genomic fossil reveals key steps in hemoglobin loss by the Antarctic icefishes. Molecular Biology and Evolution, v.23, 2006, p. 2008 - 2016.
- William C. Aird. Endothelial biomedicine. Edition: illustrated. Published by Cambridge University Press, 2007
- Chen L., DeVries A.L., Cheng C-H. C. Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid?fish. PNAS, April 15, 1997 vol. 94 no. 8 3811-3816
- Chen L., DeVries A.L., Cheng C-H. C. Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic?cod. PNAS, April 15, 1997 vol. 94 no. 8 3817-3822
- Top image © Dr Julian Gutt and Alfred Wegener Institute
- Icefish larval image by Uwe Kils
Previous Adaptations of the Week:
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".
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).
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?
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.
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.
- 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:
Therein, in symbiotic relationship number one, sat a photograph that I found utterly astonishing:
According to the WebEcoist website which published this list of "symbiotic wonders."
"It looks like something out of a storybook - and in fact it can be traced back to accounts told thousands of years ago - a crocodile opens its mouth, invites a bird in before … what? ::Chomp:: it swallows the sap alive? Amazingly, the crocodile remains still while the plover picks meat from its mouth. This cleans the crocodile’s teeth and prevents infection while providing a somewhat scary meal for the hungry bird."
The image stewed in my head for a couple of days, and I mentally bookmarked it as an excellent adaptation to cover in my Adaptation of the Week series. The story began to write itself as I drove to and from work.
It's quite easy to see how such a relationship, once begun, would be reinforced over successive generations, with the daring plovers becoming well-fed and the tolerant crocodiles' pearly whites gleaming like Smilin' Bob's.
But how would such a symbiotic relationship begin, I wondered?
Regardless of the incremental steps that naturally must have occurred, at some point a single dumb, brave, or incredibly hungry bird had to have been the pioneer to first brave the feast-laden crocodilian death-trap. Imagine being the first bird to firmly plant talons on that massive reptilian tongue. No doubt others had come to this place before - but none had survived unscathed.
And what of the first crocodile. Was he just so stuffed that he couldn't bear the thought of shoving one more feathered morsel down his gullet ("it's only wafer thin"). Or perhaps he was the Einstein of the ancient crocodiles, somehow sensing the advantage of letting the little plover do its thing.
In reality, I thought, the relationship probably came in many fits and starts, with the birds initially pecking around the crocs, grabbing whatever leftover bits they could. The crocs tolerated them, much as cattle do with egrets. Perhaps a fair number of plovers did end up as croc snacks. But over time, the crocs most friendly to the plovers gained a slight advantage, with the "friendly alleles" slowly increasing in frequency throughout the population. The birds, of course, now had to compete with one another, becoming bolder and more adventurous.
In the end, this beautiful relationship was forged and stabilized, to the benefit of both parties (though I imagined that crocodiles who break the contract probably continuously cropped up).
I had my article, plainly written right there in my brain. But of course, as with any good article dealing with science..er...well, anything, I first had to do a little bit of research. What species of bird is it? How common is the relationship?
I make my way back to the original "7 Symbiotic Wonders" article and click on the above image to get the image credits.
The photography website (Warren Photographic) immediately opens to the same image with the following caption:
"WP00955. Nile Crocodile (Crocodylus niloticus) with Egyptian Plover or Crocodile Bird (Pluvianus aegyptius) - digital reconstruction of popular myth attributed to Herodotus, 5th Century BC." [emphasis mine]
That's not a real image, but a photoshopped one? I immediately googled the bird (Pluvianus aegyptius), which pulled up this Wikipedia article:
"It is also sometimes referred to as the Crocodile Bird because it is famous for an unconfirmed symbiotic relationship with crocodiles. According to a story dating to Herodotus, the crocodiles lie on the shore with their mouths open, and the plovers fly into the crocodiles' mouths so as to feed on bits of decaying meat that are lodged between the crocodiles' teeth. The crocodiles do not eat the plovers, as the plovers are providing the crocodiles with greatly-needed dentistry. Two prominent ornithologists have supported this story anecdotally,[who?] but the behaviour has never been authenticated (Richford and Mead 2003)." [emphasis mine]
You mean to tell me that after all of this thought, the whole thing is only an ancient myth?!
Apparently the author over at WebEcoist didn't do his research for the article (sorry Ecoist). I mean, c'mon! The original image they used as the lede explicitly states that it's only a myth.
So much for my Adaptation of the Week...
What a croc!!
In the end, I decided to do some research and find a REAL symbiotic relationship:
(I photoshopped this)
Update: I found a great post on SkepticWiki that discusses this exact supposed phenomenon, and it even talks about how some creationists use the "crocodile bird" (erroneously) as an example of a behavior that could not have evolved naturally. Right...
Previous Adaptations of the Week:
The theory's thesis: "Ontogeny recapitulates phylogeny." Don't worry - it's not as complicated as the biological jargon might imply.
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.
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.
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).
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.
- 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.
Previous Adaptations of the Week:
"In the gloom it came along the branches towards me, its round, hypnotic eyes blazing, its spoon-like ears turning to and fro like radar dishes, its white whiskers twitching and moving like sensors; its black hands, with their thin fingers, the third seeming terribly elongated, tapping delicately on the branches as it moved along."
- Gerald Durrell, The Aye-aye and I
Imagine that you're a nocturnal prosimian primate in Madagascar some odd thousands of years ago. You've made a living eating insects under the bark of trees using powerful teeth to chew your way to your prey. There are no woodpeckers living on this giant island, thus many trees contain pre-packaged boreholes filled with tasty grubs. You can get to the grubs, but it requires some trial and error and alot of wasted gnawing energy.
Luckily some of your offspring are even better at finding the tree grubs, and even more adept at getting the little insects out of the holes. Generations pass, and before you know it, your descendants have become masters of the art of tree grub prospecting.
They have become the magnificent Aye-Aye lemur (Daubentonia madagascariensis)!
I was recently privileged enough to see the Aye-Aye in person at the Duke Lemur Center in Durham, NC (one of a small handful of places in the US where they can be seen).
In fact, I was cursed to death by one.
You see, the Aye-Aye has become so adept at finding insects in trees because of one singularly peculiar adaptation: it's third finger has become a skeletally thin and extraordinarily long hollow-space-detecting, insect-pulling device.
The Aye-Aye uses its long finger first to find the insect larvae - it gently taps the tree, using it's enormous and independently rotating ears to hear the hollow reverberation. Once found, it tears into the hollow area with its teeth. Now the finger shows its prime utility; the Aye-Aye inserts the skinny appendage into the hole, using its sharp claw to pull out the grub. In addition, it's knuckle joint is much like our ball-and-socket joints in our hips, making it all the more dexterous!
And this one from 8thContinent:
Unfortunately, many of the Malagasy people of Madagascar do not quite see the beauty in this unique ability. The Aye-Aye is surrounded by several superstitious myths, including the belief that if an Aye-Aye points at you (which they are wont to do), you are cursed to death. Generally, if you see an Aye-Aye or if it shows up in your village - you and/or your village are cursed to death. As such, the Aye-Aye is often killed on sight.
I, on the other hand, considered it a blessing when we entered the Lemur Center's nocturnal habitat, the red lights turned on, and an Aye-Aye immediately began swiveling its long pointy adaptation at me and my wife. It was actually quite thrilling, considering that the tour guide had just told us about the myth.
However, with the help of the Duke Lemur Center's conservation and education efforts in Madagascar (and many other such efforts), some of the Malagasy people seem to be changing their views. The Aye-Aye is still highly endangered, but hope remains...
Previous Adaptations of the Week: