Why is the "black box" so complicated??

I received an e-mail question about a recent article I wrote with a graduate student. The question shows a common misunderstanding of evolution, and I thought it would be interesting, or at least potentially useful to more that one person, to post my response here.

Hi Dr. Oakley,

I am writing a research paper and came across your paper entitled, Opening the “Black Box”: The Genetic and Biochemical Basis of Eye Evolution. I was hoping you could give me your perspective on a question that is part of my research interest.

Since a simpler mechanisms for phototransduction would theoretically work, why would evolution favor a more complicated phototransduction cascade with intermediates such as transducin and PDE? I would greatly appreciate any insight you could provide me.

The implication in the e-mail is that evolution is a force that produces sleek perfection. Expensive solutions to problems should not arise by evolution (or at least they should not be maintained), especially if the complexity is unnecessary. This is a modernist view of biology, a view that can be found in 20th Century biological research, and a view that is also common today among students, and the general public outside the field of evolutionary biology. It is a view that results from an often unstated assumption natural selection is a supremely powerful force that leads to perfection.

From this Modernist, Bauhaus perspective, it is indeed perplexing to learn that opsin initiates a complex, baroque, Rube Golddberg-like cascade to turn light energy into a nervous impulse. This cascade includes reactions from opsin->transducin->PDE->CNG; each protein signaling in one way or another to another protein down the line - and this description is even VERY simplified compared to the actual complexity!

So the question is, why would evolution "favor this complicated phototransduction cascade", when all that seems to matter is that opsin signal directly to the CNG ion channel protein to cause the nervous impulse.

The most direct answer is that evolution is not an Intelligent Designer, rather it is a bricoleur, a tinkerer. Evolution acts upon what is available, and things that are useful are kept. In the case of the phototransduction cascade, evolution co-opted existing components: an existing GPCR cascade gained light sensitivity. We know this because the components of phototransduction pre-date opsin (e.g. here). Phototransduction was not invented from scratch, in the most efficient way possible. Instead, it was cobbled together using available parts.

This can be conceived as an example of a phylogenetic or historical constraint. In other words, history matters. All living things and all components of living things share a common history. Because of this, and because of the interdependence of components of living things, it is usually not easy to completely re-invent something. The number of shared genes in all animals (for example) clearly illustrates that history matters. Components are used and re-used, not invented anew.

This answers the proximate question, of why phototransduction is so complex. But doesn't address the question of why all GPCR cascades are so complex. I don't know the answer to this, but perhaps the complexity allows for flexibility. In fact, GPCR cascades are supremely flexible, and underlie signaling from outside to inside cells for many processes in animals, including vision and other senses, hormone signaling, metabolism, development, reproduction, etc, etc.


Interestingly, this question showed me yet another new perspective on the flawed argument for Intelligent Design. ID proponents suggest that when we see something outlandishly complex, then it must have been designed by an intelligent agent. However, as this question points out, extravagant complexity is not a sign of intelligence. Why use 50 components when 2 will suffice? Elegant simplicity is far more intelligent than excessive complexity. Again, evolutionary biology provides a logical and plausible explanation for the biological processes that we are coming to understand.

Eyes abound

Unraveling and disentangling homology and convergence is one of the most fascinating endeavors in biology. Homology indicates common origin and maintenance, and is often taken as evidence for importance: ancient features are thought to be maintained because they are too useful to dispose of during evolution. In contrast, convergence, is the separate invention of similar features or functions during evolution. Convergence is taken as evidence for an element of predictability in evolution. For a simple example, fish and dolphins are highly convergent, and we can use this knowledge to predict that when vertebrates evolve to live in the ocean, that evolution will produce particular features like flippers/fins.

I recently came across a fascinating paper, arguing that structures that interact with light - either by altering or receiving it - are highly convergent, and may even be homologous at some level. Namely, bird feathers that reflect UV light have some striking similarities with eyes! Furthermore, a paper I am a co-author on just came out in PNAS that further supports this general claim. We found that the light producing structure of a bioluminescent squid shares many features with eyes, including the ability to detect ('see') the light it produces!

First, the feathers. Bleiweiss studied the uv/blue feathers of Tanagers and Bluebirds. In nature, short wavelength colors are often produced by structures, as opposed to pigments which produce longer wave colors like orange and red. Structural colors work by differentially interfering/reflecting different wavelengths of light. A familiar example of structural color is a CD/DVD. These disks contain grooves that are spaced very closely together. Because the spacing is similar to the wavelengths of visible light, interference of certain wavelengths occurs, leaving other specific wavelengths that we see as color. These spaced grooves are called diffraction gratings, and they are known in nature, for example on the antennae of some ostracod crustaceans which reflect blue light. Bluebird and tanager feathers do not use diffraction gratings, but instead a different structural mechanism. In the course of studying these feathers, Bleiweiss found some striking similarities with eyes. Perhaps similar to fins/flippers that push water for locomotion, the physical similarities of feathers and eyes may reflect convergence due to shared physical necessities of interactions with light.

An attractive tanager.  Image from britannica.com

What are these similarities between eyes and structurally colored feathers? First is a wide, domed surface to receive the light. Second is tissue that is transparent to some light but reflective of other wavelengths. In eyes, this is the cornea and lens, which are transparent to much light, but often reflect UV (human retinas are actually sensitive to UV, except the light never gets there because the cornea and lens reflect it.). Tanager feathers have physically similar tissues with similar properties to reflect UV/blue light and allow other light to pass through. Third, there is a large central space in both eyes and ocular feathers: eyes contain humors and feathers a space filled with gas (air). Finally, at the bottom is a reflective layer. In eyes, this is the tapetum lucidum, which produces eye shine in cats, coons and other night-active animals. Again, optical feathers share a similar pigmented structure also designed to reflect light.

These similarities seem to be a perfect case of convergent evolution: two structures that perform physically similar functions (light gathering, or light reflecting) have converged on similar solutions. However, Bleiweiss also raises the intriguing possibility that eyes and feathers actually share some (partial) homology. Complex traits like eyes and feathers are made of many components, each with a potentially different evolutionary history. Amazingly, some of the genetic components, developmental features, and signal transduction cascades of eyes and feathers are also shared, in addition to their functional similarities. These similarities might be evidence of a deep shared ancestry between multiple organs, including eyes, feathers, and even teeth.

I was particularly struck by Bleiweiss' paper because I've been thinking about similar things in the context of a collaboration studying the light-producing organ of a squid that yielded a PNAS paper this week. Not unlike tanager feathers and eyes, the convergence of squid light-producing organs and eyes has long been noted. Many squid, including Euprymna scolopes, the object of our study, are bioluminescent. Euprymna seems to use its bioluminescence for camouflage. In the ocean, most light comes from straight above, so animals would cast a distinct and conspicuous shadow below them. Instead of eliciting the shadow response of a predator or prey, Euprynma matches downwelling light to make itself more cryptic. The light is produced in a light organ that houses symbiotic bacteria. It is the bacteria that actually generate the light. Consistent with Bleiweiss' general hypotheis, this light organ has many similarities with eyes.

Light organs and eyes both have lenses. Eyes focus incoming light for better visual acuity, and light organs focus outgoing light, similar to a flashlight. Eyes and light organ have an open space below the lens, and a pigmented layer opposite to the lens. In addition to these similarities, we found that the light organ responds physiologically to light using the same genes (opsin and its signaling components) that are used in eyes. Just as with optical feathers, squid light organs are functionally convergent, yet also share structural components in common, indicating some elements of homology.

Euprymna scolopes Hawaiian Bobtail Squid.  Picture by Chris Frazee, image from pnas.org

These findings indicate an interesting new research program using the tools of phylogenetics. By reconstructing the evolutionary history of multiple components of convergent/partially homologous traits, we can see how and when these components came together, illustrating the pathways by which evolution has produced new features. This will allow a richer, more fundamental understanding of the origins of biodiversity and complexity, topics that intrigue everyone.

References
Bleiweiss, R. (2009). Feathers with Ocular Architecture: Implications for Functional and Evolutionary Similarities of Visual Signals and Receptors Evolutionary Biology, 36 (2), 171-189 DOI: 10.1007/s11692-009-9059-6

Tong, D., Rozas, N., Oakley, T., Mitchell, J., Colley, N., & McFall-Ngai, M. (2009). From the Cover: Evidence for light perception in a bioluminescent organ Proceedings of the National Academy of Sciences, 106 (24), 9836-9841 DOI: 10.1073/pnas.0904571106

Let There Be Light!

I'm looking forward to attending a Darwin Day event next week in Iowa City.  I will be delivering a lecture entitled,  

Let There Be Light!

Evolution and the Genesis of Light Sensitivity in Animals

I'll discuss our lab's work to try to learn about how light sensitivity, which today allows vision, first originated in animals.  Some of our work is published, and I've discussed some of it before on the blog here.  

Namely, we have been studying the genetic basis of photosensitivity in the cnidarian Hydra magnipapillata.  Cnidarians are the most distant relatives of humans that possess (type-II) opsin-based photosensitivity.  As such, components of the mechanisms of light sensitivity shared in humans and cnidarians may have been present at the very origin of this type of photosensitivity, and can inform us about how this amazing sense originated during evolution.

To test whether particular genes are used in sensing light in hydra, we are taking advantage of a behavioral response to light.  Hydra have no eyes - they do not have pigmented spots.  But they do respond to light.  I've today been working on a video to illustrate a contraction response that hydra undergoes when light is shined on them.  We can knock out candidate photo genes, and if the animal doesn't contract, this supports the hypothesis that the knocked out gene could be used in sensing light.

The video is time-lapse, shot through a dissecting microscope.  The animal is small, less than half an inch long.  Its base, to the right, is attached to a petri dish, and its tentacles are out to the left.  The hydra does a little stretch, and then the contraction.  This happens over about a minute or two, but is condensed to a few seconds here.

This type of behavior was noted in a different species way back in 1744 by Abraham Trembly.  At that time, people thought polyps were plants.  Trembly saw a hydra polyp move, and decided it was probably an animal.  To test this hypothesis, he cut one in half: animals should die, and plants could regenerate.  But hydra can regenerate even though they are animals.  So Trembly discovered animal regeneration, and (sort of) stem cells.

Exaptation! PT flare up #2

Continuing on with my thoughts about the flare up at Panda's Thumb (part 1 here):

Basically, I think "Green" the anonymous undergrad from a University in the UK, raised a few valid issues that are worth thinking about. A lot of the evolutionists, while I agree with their points on general terms, are not addressing the concern of "Green" directly.

Her main point is (from the comments at Panda's Thumb):

“Co-option may not be the de novo formation of genes, but it still requires mutations (such as, for example, the gain of a cis regulatory region). My whole point was that simultaneous mutations are required for the evolution of the phototransduction cascade. Correct me if I’m wrong, …”

This is in part true, and raises the point that we should be discussing EXAPTATION and not co-option, to most clearly convey the point.

Green is stating that even if all the components of phototransduction are present an ancestral genome that lacks phototransduction, multiple mutations would be required to assemble all those components into a phototransduction cascade. So, multiple co-option events would be required, and this is what she is having a problem with.

HOWEVER, what is false is the requirement for all these mutations to occur simultaneously. Instead, the components could be assembled one by one in a graduated, step-wise (Darwinian) fashion.

Instead of focusing on co-option, Green should focus on "exaptation". Exaptation is the idea (roughly) that features can arise for one function, and then change function later on. In the case of phototransduction, much of the phototransduction cascade originated for another purpose - sensing some signal from outside the cell to elicit changes inside the cell. (And just because a yeast pheromone cascade isn't THE phototransduction precursor, doesn't mean there wasn't one). One response to a signal evolves, changing the signal that is detected (to light) seems pretty surmountable. In fact, this has happened independently in the lineage leading to C. elegans (see my post here).

For another example of exaptation, we've found that many components used in synapses predate synapses themselves. See these posts in pharyngula, Newsweek. The open access paper and other news sites (including radio interview) are here.

PT eye evolution flare up

I was notified that there was a little flare up at Panda's Thumb about our recent article on eye evolution, entitled:

Opening the "Black Box": The Genetic and Biochemical Basis of Eye Evolution by Todd H. Oakley and M. Sabrina Pankey (PDF) published in Evolution: Education and Outreach.

Warning: Long Post. If you only read one thing, read this:

One might argue that we are just pushing back the origins, changing the question of "phototransduction" origin to the question of "transduction" origins. In a way this is true, but it is also a fundamental insight about how evolution works. New features are not breathed into organisms by some unknown force, they evolve by duplication/divergence or recombination of existing features. Trace a feature like phototransduction back far enough in evolutionary time, component by component, and it grades into something else altogether.

Here is the story:
A week or two ago, I was contacted by an undergraduate from a university in the UK (I see no reason to reveal her name). She had questions about the article, writing:

I've just been reading your 2008 paper 'Opening the Black Box: the genetic and biochemical basis of eye evolution' and found it really interesting! I'm just writing an essay on eye evolution atm and am trying to get to the crux of the issue, and find out how the phototransduction cascade itself evolved. After explaining that opsin probably arose by a mutation in a serpentine gene/protein, you mention in your paper that:

"In yeast...these receptors [GPCR's - the serpentine proteins] are sensitive to pheremones, and they even direct a signal through proteins homologous to non-opsin phototransduction proteins."

What I'm wondering is, is it this whole yeast pathway that has been modified for the metazoan phototransduction cascade? Or is it only the opsin which has been derived from it? (With the subsequent molecules involved in the phototransduction cascade being co-opted from other proteins not involved in the yeast signalling pathway).

Based on this email, it seemed the student had a pretty good grasp of the issues, and I replied:

Thanks for you questions.  I found out after writing the paper that the yeast pheromone proteins are not the "rhodopsin type" GPCR, so they are distantly related at best to opsins.  So they should not be considered anything like direct ancestors of opsin.

As for other components of the yeast pheromone cascade, these are different than phototransduction.  Yeast pheromones activate a MAP kinase cascade. So, I think all that is similar is the GPCR and G-protein.

So, it really is an open question as to what the ancestral function was of some of the genes of phototransduction, although some of these genes do function in other sensory transduction pathways...

Unfortunately, she misinterpreted this email, understanding it to mean (written over at PT, using the pseudonym "Green"):

"Yeah I knew that co-option thing would be coming. Turns out there was a mistake in that Oakley and Pankey paper.

The yeast intracellular signalling cascade turns out not to be homologous in any way to the metazoan signalling cascade. It just got published before the authors realised."

First of all, this is an incorrect interpretation of what I wrote. In fact, I wrote "So, I think all that is similar is the GPCR and G-protein." This is far from "not homologous in any way", as claimed by the student. The G-protein is undeniably homologous, and the yeast pheromone receptor is a 7-transmembrane protein, at least conformationally like opsin (whether or not the opsin and pheromone receptor sequences are homologous is a trickier issue).

But the larger issue is I think an issue of "linear thinking", which I address quite often on this blog. The student seems to think that if we cannot identify in yeast (taken as a linear ancestor of animals) a cascade identical to phototransduction except for opsin, then the origin of phototransduction requires numerous simultaneous mutations. This is not the case. First of all, yeast is a more distant relative of animals with phototransduction than is sponges. I just mentioned the yeast pheromone photoreceptor in the paper as a well studied example of a pathway outside of animals with partial homology (some components homologous, some not) to photoreception. There are closer "relatives" of phototransduction in sponges (poorly studied functionally, but the genes are known) and in other animals (better studied).

Another issue is a difficulty that people have with thinking about partial homology - that some components can be homologous and some not, depending on the time scale of the comparison (see my post The Red Herring of Eye Evolution).

Partial homology is a pattern that indicates a mechanism of co-option in the evolution of features. Co-option is the combination of existing things in a new way (analogy: dijonaisse = dijon mustard plus mayonaisse). All of the components of phototransduction pre-date animals, except opsin. And if we consider opsin to be a GPCR, which it is, then all of the components of phototransduction pre-date animals. This may be considered a pattern of co-option, or exaptation. Signaling pathways were already present before phototransduction. Some of the phototransduction components function together as far back as the yeast + human common ancestor (GPCR + G-protein). Other components of phototransdcution function together in non-phototransduction cascades of other animals. This indicates that phototransduction did not assemble all at once, but built incrementally upon an existing scaffold.

One might argue that we are just pushing back the origins, changing the question of "phototransduction" origin to the question "transduction" origins. In a way this is true, but it is also a fundamental insight about how evolution works. New features are not breathed into organisms by some unknown force, they evolve by duplication/divergence or recombination of existing features. Trace a feature like phototransduction back far enough in evolutionary time, and it grades into something else, component by component.




There were other comments, too. Again at PT, she also commented:

Yeah I read Oakley and Gregory’s articles on eye evolution a couple of weeks ago. Unfortuantely neither address the crux of the issue: namely the origin of the biochemical phototransduction cascade.

To be fair, Oakley’s article (the ‘Black Box’ one) at least tries to give some biochemical details. But it only scratches the surface by suggesting a potential origin of the opsin protein. Unfortunately the origin of a new opsin protein is not equivalent to the origin of an entire phototransduction cascade.

So it seems the Darwinian account still falls quite far short of any satisfactory biochemical explanation. Descriptions of morphological change, comparisons of genes, crystallins, etc. all skirt the issue if it cannot be shown how the phototransduction cascade itself arose

The difficulty with this comment is that the origin of opsin defines the origin of phototransduction. The other components of the cascade were already there, they all predate opsin, as described above.

This is also a "God in the Gaps" argument, or maybe, a "God under the surface" argument, stating that describing the origin of the keystone molecule of phototransduction (opsin) "only scratches the surface".

Also, I don't understand what the difference is between "comparisons of genes" and "biochemical explanation". What would a biochemical explanation be for the evolutionary origins of things that doesn't involve "comparisons of genes". The genes of the phototransduction pathway have biochemical interactions with each other, many mediated by interactions between specific amino acids.

Eye evolution issue printed

The new issue of Evolution education and outreach has been printed, and the issue is all about eye evolution. The links to all the articles are below, they are available free of charge.



Evolution: Education and Outreach
Volume 1 Issue 4

Editorial

351. Editorial by Gregory Eldredge and Niles Eldredge (PDF)

352-354. Introduction by T. Ryan Gregory (PDF)

355-357. Casting an Eye on Complexity by Niles Eldredge (PDF)

Original science / evolution reviews

358-389. The Evolution of Complex Organs by T. Ryan Gregory (PDF)
(Blog: Genomicron)

390-402. Opening the "Black Box": The Genetic and Biochemical Basis of Eye Evolution by Todd H. Oakley and M. Sabrina Pankey (PDF)
(Blog: Evolutionary Novelties)

403-414. A Genetic Perspective on Eye Evolution: Gene Sharing, Convergence and Parallelism by Joram Piatigorsky (PDF)

415-426. The Origin of the Vertebrate Eye by Trevor D. Lamb, Edward N. Pugh, Jr., and Shaun P. Collin (PDF)

427-438. Early Evolution of the Vertebrate Eye--Fossil Evidence by Gavin C. Young (PDF)

439-447. Charting Evolution’s Trajectory: Using Molluscan Eye Diversity to Understand Parallel and Convergent Evolution by Jeanne M. Serb and Douglas J. Eernisse (PDF)

448-462. Evolution of Insect Eyes: Tales of Ancient Heritage, Deconstruction, Reconstruction, Remodeling, and Recycling by Elke Buschbeck and Markus Friedrich (PDF)

463-475. Exceptional Variation on a Common Theme: The Evolution of Crustacean Compound Eyes by Thomas W. Cronin and Megan L. Porter (PDF)

476-486. The Causes and Consequences of Color Vision by Ellen J. Gerl and Molly R. Morris (PDF)

487-492. The Evolution of Extraordinary Eyes: The Cases of Flatfishes and Stalk-eyed Flies by Carl Zimmer (PDF)
(Blog: The Loom)

493-497. Suboptimal Optics: Vision Problems as Scars of Evolutionary History by Steven Novella (PDF)
(Blog: NeuroLogica)

Curriculum articles

498-504. Bringing Homologies Into Focus by Anastasia Thanukos (PDF)
(Website: Understanding Evolution)

505-508. Misconceptions About the Evolution of Complexity by Andrew J. Petto and Louise S. Mead (PDF)
(Website: NCSE)

509-516. Losing Sight of Regressive Evolution by Monika Espinasa and Luis Espinasa (PDF)

Book reviews

548-551. Jay Hosler, An Evolutionary Novelty: Optical Allusions by Todd H. Oakley (PDF)

Probing Darwin's Black Box

The 'God of the Gaps' strategy is to assert that anything we do not yet understand is attributable to a god or gods. Two thousand years ago there were a lot of gaps in our understanding, and plenty of room for inventing ad hoc explanations for things. There were a lot of gaps where gods might reside.

Even recently, the god of the gaps argument is sometimes used. One example is the idea of 'Darwin's black box', the false assertion that the exquisite details of molecular biology cannot be understood in an evolutionary context.

There are two facets of 'god of the gaps' that are particularly bankrupt, one scientific and one theological. Scientifically, god of the gaps is equivalent to suicide, an admission that one simply cannot imagine how to go on any farther. God of the gaps is giving up on science, with no reason to do so. Theologically, god of the gaps means that the realm of god gets smaller each time a gap in our knowledge is filled.


Here, I give two recent examples from my life where the molecular details of evolution have been explicated in greater detail. In neither case are the gaps fully filled - this can never be the case - split a gap in half and we have two smaller gaps. But the gaps are getting sooo small - is it really worth trying to stuff gods in those tiny little gaps?


First, I saw a seminar by Joe Thornton on his work on the evolution of steriod receptors. Joe uses statistical inference to reconstruct the sequence of ancestral proteins. Then he brings them to life in the lab and conducts experiments on the proteins. He is able to reconstruct the order of specific mutations that occurred and that change the function of the proteins he studies.

I found particularly interesting that one particular receptor could identify 3 different steroids at the origin of the protein. Later on, specializations occurred through particular mutations that Joe and his group could identify. When thinking about the evolution of novelty, we often assume that multiple functions are added over evolutionary time. However, Joe's results show how functional complexity can be the original state, and that structural complexity can follow by parsing an ancestral function across subsequently duplicated genes.

To view Joe's presentation, go here.


The second recent example is that a paper from my lab was recently published that reviews our progress on understanding the evolution of the molecular basis of vision (phototransduction). This paper is available for free from the Springer web site.

Todd Oakley and M. Sabrina Pankey (2008) Opening the "Black Box": The genetic and biochemical basis of eye evolution. Evolution Education and Outreach. [Link]

Optical Allusions Book Review

As mentioned at The Loom, and Genomicron, there is a new issue of Evolution, Education and Outreach available, devoted to my favorite topic, the evolution of eyes. I've contributed two pieces, one is available now, and is a book review of Optical Allusions, by Jay Hosler.


Jay Hosler, An Evolutionary Novelty: Optical Allusions by Todd H. Oakley




The other paper I contributed is inspired in part by Behe's claim of irreducible complexity of phototransduction in Darwin's Black Box. That paper is not available yet, but should be soon. For a small taste of the paper, I will quote from the it:

"Unfortunately, instead of pointing to the molecular evolution of multi-component systems as a rich area for new scientific research and synthesis, Behe chose to commit scientific suicide by incorrectly claiming that the only way for multi-step biochemistry to arise is by intelligent design."

Ostra-blog 4 - Colymbosathon ecplecticos

Last week, somewhere near the top of my mental list of candidate species for ostra-blogs was Colymbosathon ecplecticos. A couple years ago, this species burst on to the ostracod scene, causing a global media event. Ostracodologists are not used to seeing their favorite animals in the headlines, so Colymbosathon caused quite a sensation. On Friday, Eric at The Other 95% generated a post, Who's Got the Oldest?, with Colymbosathon playing the prominent role. Eric described some of the species' vitals. Yes, it's the oldest fossil with identifiable male parts. Yes, its species name means "amazing swimmer with a large penis". Eric's post prompted me to make Colymbosathon the star of this, ostra-blog #4.

Colymbosathon first exposed itself to me at a scientific conference. I was immediately drawn to its rather prominent.... eyes. We were in Seattle in November of 2003, about a month before the Science paper was to be published, and cause the aforementioned media blitz. So it came as a complete surprise to me when the first picture of this 425 year-old fossil flashed on the screen. I remember a seeing on the screen a photo similar to Figure 1 below.



Figure 1. Colymbosathon ecplecticos, a 425 million year old fossil ostracod. Image copyright Science Magazine.


I study ostracod eyes, and I've dissected many of them. My attention went directly to the compound eyes. One is marked "le" in the figure above for "lateral eye". That's the left eye, the right eye is higher on this figure, just below the "H" in the figure.

This fossil was preserved about 425 million years ago in three dimensions inside a volcanic nodule. The scientists break open such nodules in search of interesting fossils. When they find one, they make an image of the fossil at the point it broke, and then grind away a tiny bit of rock (10 microns or so, if memory serves) and take another picture. Doing this procedure over and over again gives them a stack of images, which they can put together computationally to yield full 3-dimensional reconstructions of the fossils. For ostracods and other small animals, this is completely amazing. For most ostracod fossils, only their carapace is preserved, it's made of calcium carbonate. On a few fairly rare occasions the "soft parts" of ostracods are also preserved. (Soft parts refers to the non-carapace parts, even though they are not all that soft, having a chitinous exoskeleton). But even when soft parts are preserved, there were no cases where the full 3-dimensional structure was visible. With digital reconstructions, movies can be made, and specific parts of the animal can be highlighted or removed in order to view other structures.

Figure 2 - Computer generated image of Colymbosathon (side view). Different parts of the animal are colorized differently to make them easier to see. Faint parallel lines are visible, which is where the original was ground, 10 microns at a time, to yield an image stack of the 3-dimensionally preserved fossil. Image copyright Science Magazine.


It was obvious right away that this was something very special. It clearly impacted my own work on ostracod eye evolution. This marked the oldest ostracod compound eye in the fossil record, pushing back the date some 200 million years. In 2002, I published a molecular phylogeny of ostracods that shows that ostracods with lateral compound eyes are nested phylogenetically within multiple groups that lack lateral eyes. One possible interpretation of this is that lateral eyes evolved within Ostracoda (of course eyes don't evolve from nothing, so if this idea is true, many of the genes used in all animal eyes should still be present in the ostracod lateral eyes). Colymbosathon doesn't itself change these conclusions because it is a member of the same group (myodocopids) that today have lateral eyes. Nevertheless, the Colymbosathon fossil pushes back the origin of ostracod compound eyes quite a bit.

Of course not many other people cared about the eyes. They had other things on their mind. In particular, many journalists really rose to the occasion, devising many very entertaining headlines. Some of my favorites are below, and I've taken the liberty to put them into a few categories.

1. The "size matters" category

l

• Scientists Discover Ancient Gargantuan Penis
• Sea creature impressive in its maleness
• Well-endowed sea creature is nearly half a billion years old
• He's 425 million years old and clearly virile
• Male fossil makes a big impression

2. The "age before beauty" category

• Ancient penis brings fame to lowly fossil
• Oldest male fossil bares all
• World's oldest genitals found in Scotland

3. Wonderful alliteration category

• Phallic fossil found

4. And last but not least, the winkle category, a clipping of which hangs in the lab

• Fossilised shrimp has the oldest winkle in the world

Evolutionary origin of a light sensitive nerve

The origin of a light sensitive nerve was almost certainly an early step in the evolution of animal eyes, and this was thought to have happened only once, some 600 million years ago. But new open access research on the nematode C. elegans indicates a heretofore unknown instance where a nerve evolved light sensitivity.

One of the common, but incorrect, claims of anti-evolutionists is that the origin of complex features like eyes cannot be explained by evolutionary biology. As an example (although perhaps not written by an anti-evolutionist) see the comment on this post. For some history and a response to the incorrect anti-evolutionists claim, see this post.

It turns out that, as is often the case, the difficulty in understanding comes from trying to make a continuum into a dichotomy. An eye or even the genetic machinery for light sensitivity doesn't have to be all there or all not there. Instead, these features can build up gradually, by classical Darwinian evolution.

An early step in the evolution of complex eyes was almost certainly the origin of a light sensitive nerve. Darwin imagined that nerves might easily become light sensitive, but because of a lack of understanding of the molecular basis of photoreception, not to mention the molecular mechanisms of heredity, he could not even fathom a guess as to how nerves came to see the light. But just because Darwin didn't know how the machinery of light sensitivity could be built gradually by evolution doesn't mean it couldn't occur gradually.

Light sensitivity is a multi-step genetic process, where one protein signals to another. But all those proteins were not "turned on" all at once to suddenly allow for light sensitivity. Instead, light sensitivity evolved from existing "senses". Many signals are detected outside of a cell and they trigger proteins to send a signal inside a cell. Even yeast use proteins to sense pheromones outside their single cell and direct growth toward a potential mating partner. Many of these signaling genes are shared across all of our senses, and we can pinpoint by comparative study when a signaling gene became a light sensitive protein called opsin (again see this).

This brings us to the worm research. C. elegans has no visible eyes and its genome lacks light sensitive opsin genes. Yet it does display sensitivity to UV light!

Here is a link to a video showing light sensitivity.

How does it do this without opsin? It turns out that a different protein has become light sensitive. In this case, homologous proteins are known to be taste receptors (Gustatory receptors) in insects. Therefore, at some point in evolutionary history, the worm protein
gained light sensitivity, independently of the opsin "light switch"!

This is really fantastic work that suggests many new lines of research. For example, the mechanism of photoreception is unknown for the worm gustatory/light receptor. If this could be understood, we could get a specific idea about how a protein gained light sensitivity during evolution. Second, it is not known when light sensitivity was gained, which would require comparative study. These genes are present in insects - are the insect genes light sensitive? It would be great fun to put an insect gene in a worm to see if it could rescue the loss of light sensitivity due to a mutation.

Finally, I'll point out that this work is similar to another study published just last month . That workfocused not on the receptor, but on genes later in the cascade; especially on the gene responsible for "firing" (ie changing the concentration of the ions in) the light sensitive nerve. It turns out that that the "firing" gene is homologous to the "firing" gene used in vertebrate rod and cone cells - another example of how evolution often uses similar tools to produce parallel results.

Quick impressions of “Evolve: Eyes” on the History Channel

I recorded the TV show Evolve:Eyes, which aired on the History Channel last night, and I watched it today. Last night during the original airing, I was in LA watching the Dodgers with my family. I think my son was quite taken with professional baseball. This was not his first game (I had to make sure that for both kids, their first game was in Milwaukee, where mine was), but I don’t think my son remembers seeing the Brewers in Miller Park. So when we walked through the gate of Dodger Stadium, I saw the awe in his eyes, as he took in the stadium’s brightness, the impossibly green grass, and as we heard 40,000 fans cheer together. There is something to be said for appearance and spectacle, which can make even things like playing baseball games seem important.

This was the primary strength that I found in the History Channel show Evolve:Eyes; it looked really slick; it had its share of spectacle. There were fantastic graphics. Three dimensional eye figures exploding into component lens, cornea, and retina. The linear progression of eye evolution was re-told graphically, a few photoreceptors morphing into a deepening pit. Then a lens appeared, until the human eye had “evolved” right before my own eyes.

There were also dramatic film sequences of real scientists. There was a re-enactment of my friend (we were postdocs together in Chicago) Nate Dominy of UCSC doing his field research observing primates (I’m guessing they filmed Nate in Santa Cruz with binoculars and cut in footage of primates). There was footage of my friend Chris Kirk (haven’t seen him for a while, but we were grad students at Duke at the same time) pulling eye balls out of jars, complete with lab coat (most biologists I know don’t wear lab coats, unless they’re being filmed, or maybe if their pulling eyeballs out of a smelly formalin/ethanol solution). And there was footage of my colleague Alex Goodell collecting Polyorchus (a cnidarian) and shining LED lights on them to watch their behavior: green light, then blue, illuminating the tank and animal like neon lights in the dark. Scott Edwards, alone in an arid landscape, artistically filmed full-body and off-center, commented on how many times eyes evolved, my proverbial red herring, deciding to re-tell the take of a fellow Harvard-man, the late Ernst Mayr. Spectacle. Beautiful.

But all was not positive from my perspective. Namely, the show fell into the two most common traps that plague the understanding of evolution by the public. 1) Evolution is not adaptive story telling and 2) Evolution has not progressed in a direct line from simple to complex; evolution most certainly does not culminate with the human species. In nature, humans are no more special than bacteria. We are just another twig on the great tree of life (that was for Eisen).

Very little of this show was actually about evolution, and most of the “evolution” that was mentioned did not explain the actual science behind it (there were of course some excpetions). Instead, there was a lot of adaptive storytelling. Eagles evolved amazing vision to allow them to be better hunters. I don’t doubt this is true, but this show very often simply asserted and explained current function, with little mention of how evolution of those traits proceeded. Jellyfish try to escape UV/blue because it is damaging. Again, this may be true, but it was simply asserted in the show. Evolution was simply assumed, with little mention of how we actually have established that evolution works.


But the most egregious to me was how the narrative and graphics re-enforced the non-existent linear progression from jellyfish to humans. In fact, the graphics were a line, shown between stories, proceeding from 600 million years ago to present day primates. In this hypothetical line, first came the “jellyfish” (they actually showed a hydromedusan). The camera simulated the “primitive” jelly’s blurry vision, far inferior to our own, no mention of the cubomedusan’s highly complex eye. Next came the trilobites, whose calcite compound eyes are among the oldest fossil eyes. (To the show’s credit, they did mention that trilobites are not direct ancestors of living arthropods, a slight nod to “tree thinking”. Also, the Cambrian and trilobite animations were pretty cool. More spectacle.)


Then came the vertebrates. Not much mention of fish, instead we jump to dinosaurs. More flash here, tremendous spectacle, shining lasers on models of T. rex, the icon of charismatic species. Then the story moves up the ladder to early mammals, “primitive mammals” eeking out an existence, with only “black and white” vision, living in the shadow of dinosaurs. Then the great KT event knocks out rex and mammals can finally flourish. This next bit really got me. They compare human (and some other primates’) vision to that of early mammals, saying how great we are to be able to see red. What a shallow point of comparison, just to inflate the human ego, and maintain the march of progress up to humans! Why not compare to our eyes to stomatopods (mantis shrimps), who see circular polarized light, and have upwards of 12-chromatic compared to our tri-chromatic vision. Or even compare us to adult maggots (i.e. flies), who see polarized and UV light that we cannot detect. In my book, the evolutionary ladder of eyes proceeds up to mantis shrimp, not humans.



But perhaps I am being a bit too critical, expecting too much nuance from a show aimed to keep viewers from switching to, say, ESPN to see how the Dodgers are doing (they won by the way). Spectacle can be something to celebrate!

After the Dodger’s game last night, I could tell my son was inspired by spectacle, not by nuance. In fact, I doubt he got any nuances of the game. He was oblivious to strategic pitching changes; clueless about a rare call that gave the Dodgers an extra run in a tight game (the Giant's left fielder juggled the ball out of play, something I’ve never seen, after many years of watching baseball, e.g. I’ve seen in person a triple play, and Ricky Henderson’s record breaking stolen base). No, it wasn’t nuance that compelled my son to ask when he gets to start soccer, and if I can video record his games so we can watch them on TV. It was spectacle, fan screaming, light flashing, ice cream in a Dodger helmet spectacle.

So who am I to complain if somewhere, some kid is taken by the spectacle of eye evolution, as so vividly portrayed last night? Taken by the idea of shining lasers on T. rex, or neon LED’s on pulsating jellyfish in dark rooms? Maybe an African-American kid saw Scott Edwards on TV last night, and dreamed a dream of studying evolution. Maybe the child of an anti-evolutionist now has some questions.

There is a place for spectacle. If spectacle can inspire, nuance can come later.

Eye evolution: post-dinosaur, pre-Noah's Ark

Back in January or so, I was interviewed by researchers at the History Channel over the phone. They were working on a new series on evolution, and one episode was to be about eyes. I guess they had seen our lab's work last year on cnidarian opsins in the news and decided to talk to me about it. Looks like they might mention this and/or research by Suga and Gehring published in Janurary on cnidarian opsins. Here is the blurb from the History Channel website:



They are one of evolution's most useful and prevalent inventions. Ninety five percent of living species are equipped with eyes and they exist in many different forms. Learn how the ancestors of jellyfish may have been the first to evolve light-sensitive cells. Discover how dinosaur's evolved eyes that helped them become successful hunters. Finally, learn how primates evolved unique adaptations to their eyes that allowed them to better exploit their new habitat, and how the ability to see colors helped them find food.


I remember from the interview that they were really probing for flashy stuff. They wanted to know what they would see if they came to film at UCSB. They didn't seem too interested in filming hydra sitting in a dish (although that's one of the things we are doing in the lab this summer). I can see from the abstract that they settled on dinosaurs and primates - the proverbial charismatic megafauna....


I just looked up the schedule, and the eye evolution program will air just after Dinosaur Fight Club, and just before a documentary about a flood 3,000 years ago that they are dubbing Noah's flood! Should be fun!

The date is Tuesday July 29, eye evolution at 10 pm.

I'll try to give an opinion on the Eye Evolution program here after it airs.

Evolutionary Origins of Phototransduction

Below is a section of an article I am drafting on eye evolution. Does it make sense? Any parts impossible to understand? Comments are welcomed!



In The Origin of Species, Darwin hypothesized that the first step in the evolution of eyes involved the gain of photosensitivity in a nerve, writing, “…I may remark that several facts make me suspect that any sensitive nerve may be rendered sensitive to light…” Here, Darwin was making the assumption that variation leading to light sensitivity of previously non-light-sensitive nerves was abundant, and that natural selection could then act on that variation. But how did those specific variations originate? How does a nerve become light sensitive? In his notebook, Darwin suggested that it might be impossible to understand how a nerve gained light sensitivity. He wrote “to show how the first eye is formed, — how one nerve becomes sensitive to light, ...is impossible.” Since the mechanisms of heredity and the molecular mechanisms of photoreception were unknown in Darwin’s time, no specific hypothesis could even be posed about the genesis of light perception. One hundred and fifty years later, things have changed.


Today, through an understanding of the distinct evolutionary histories of the components of vision, and more specifically of phototransduction (the signaling pathway that turns light into a nerve signal), we can now pose a specific historical hypothesis for their origin: Phototransduction originated within animals by modifying an existing signaling pathway. More specifically, at some time before the divergence of jellyfish and humans, but likely after the split common ancestor of sponges and humans, the first light sensitive animal opsin protein originated. This protein did not originate from nothing, nor was it newly breathed into an ancient animal genome by a designer. Instead, opsins arose by mutation of an existing receptor to render it light sensitive. This historical hypothesis makes numerous predictions, and available data are consistent with the hypothesis. It also makes predictions that have not yet been tested, indicating promising areas for future research.






If the hypothesis that phototransduction arose within animals is valid, then some components of phototransduction should exist within animals, but should not exist (or should possess a different function) outside of animals. Such is the case for opsin, which is present as the primary photopigment gene in most animals. Recent research shows that various cnidarians, including a hydra, a sea anemone, a hydrozoan, and a box jellyfish, possess opsins (Plachetzki et al, 2007; Suga et al, 2008; Kozmik et al, 2008). At the same time, opsins are absent from sponges and non-animals (See Figure). In science, demonstrating the absence of something like a gene is difficult, because a skeptic can always invent a reason why the target was accidentally missed. In the case the opsins in question, scientists have determined the entire genome sequence of the sponge Amphimedon queenslandica, the choanoflagellate Monosiga and numerous fungi, making the presence of opsin in those organisms very unlikely. Some proteins of near-animals are in fact rather similar to opsins, but in every case the non-animal receptors lack characteristics that specifically define opsins. Therefore, although opsins might have been present at the origin of animals and lost in sponges, their absence instead strongly suggests that they originated within animals, before the split common ancestor of humans, insects, and cnidarians, all of which possess opsins.


With current knowledge that opsin is the basis of light sensitivity, Darwin’s question of how a nerve becomes light sensitive can be rephrased as, “how did animal opsins originate”? Proteins rarely originate from nowhere, and opsins are no exception. Opsins form a subfamily within a larger family of proteins called G-protein coupled receptors (GPCRs), also sometimes called serpentine proteins because they snake back and forth across cell membranes. Since serpentine proteins are present in all animals and their close relatives - including sponges, Monsiga, and fungi - this broad class of proteins long predates animals. In yeast (a fungus), these receptors are sensitive to pheromones and they even direct a signal through proteins homologous to non-opsin phototransduction proteins. As such, a signaling pathway exists outside animals, which is very similar to phototransduction, except the receptor protein detects pheromones, not light. Receptors outside animals share some characteristics with opsin, like snaking through a cell membrane seven times. It is one of these serpentine proteins that served as the progenitor of the first opsin protein, as evidenced by the similarity of opsins and other serpentine proteins.


Darwin’s question can be refined farther, to “how did a serpentine protein gain the ability to respond to light?” And since opsin’s light sensitivity is mediated by its ability to bind a light reactive chemical, called a chromophore, the question can be even further refined to ask how a GPCR must be modified to bind a chromophore. In the case of opsin, we know that a particular amino acid – a Lysine in the 7th membrane-spanning region – binds to the light reactive chemical. Presumably then, a mutation changing an amino acid in the 7th trans-membrane region of a light insensitive GPCR was involved in the acquisition of light sensitivity in animals. This fateful mutation coupled with numerous other mutations, are responsible for the origins of eyes and vision. Although science has not yet tracked down every single mutation involved in the evolution of vision, the origin of opsins clearly illustrate, in richer detail than Darwin might have imagined, the natural processes that gradually allow the evolution of complex features.

Box Jellies and the Red Herring of Eye Evolution

Smoking a herring turns it red and imbues the fishy flesh with an extra strong odor, which can be used to throw bloodhounds off your trail, or to train hunting dogs to stay on the main scent trail, even if far less odoriferous. Such are a few hypotheses for the origin of the term "red herring", used to denote an enticing, yet ultimately uninformative beacon.

I've come to realize that my own field of eye evolution has a resoundingly pungent red herring that continually throws scientists and non-scientists alike off the trail of a deep understanding of how eyes, and more generally, photoreception, evolved. In this case, the rank fish is the simple and seemingly harmless question, "How many times did eyes evolve?"

Quite often, when I tell a newly acquainted colleague that I study eye evolution, he or she will pull the red herring out of their back pocket, and dash across the room, dragging the fish behind them. "So how many times did eyes evolve, anyway?” they ask, hoping I have a key to this deep mystery. When I was a younger bloodhound, I often took that bait, howling and bounding enthusiastically after that trail, circling the room again and again. But I've followed that trail enough times by now to know that it circles back on itself in a confusing and illogical way.

How many times eyes evolved, though enticingly simple, is an all but unanswerable question; at least in terms of a numerical answer that people crave. Eyes did not evolve one time, nor did they evolve forty to sixty-five times. The answer is that some components of animal eyes are shared in all animal eyes we've ever examined. Yet some components are new comers to organs that probably functioned as eyes even before those components joined the party. Asking how many times eyes evolved makes the implicit assumption that every component of that eye shares a congruent history, that an eye is either all there, or all not there. But eyes are complicated structures, and the evolutionary histories of its parts are varied.

A new paper by Kozmik et al in PNAS is an interesting piece of science that breaks new ground. Although it does not detract from the scientific value of their study, the authors have been beguiled by our ripe red herring. Still, they have elegantly streamlined the malodorous query in a way that will allow me to more easily explain the stench, and so I retell their work here. First, I’ll explain some of the new data then I’ll point out where I think they, like many others before them, lost the main scent trail.

The authors examined a box jellyfish, a group that includes the infamous sea wasp, the deadly nemesis of Australian beach-goers. Box jellies are cnidarians, the group including corals, anemones, and hydras, which besides sponges, may be the most distant animal relatives of humans. As such, the biology that is shared between humans and cnidarians likely originated very early in the history of animals, hundreds of millions of years ago. With this logic in mind, Kozmik et al focused on elucidating some of the components of the eyes of one particular box jelly that lives near Puerto Rico, a far less noxious variety than the Australian sea wasp. In particular, they elucidated some photoreceptor genes and some genes that produce a shading pigment in the box jelly’s eyes. Choosing these two particular components was no accident. They were chosen because they represent a common minimum definition of “an eye”. Some scientists argue that minimally, an eye must contain photoreceptor cells to register the presence of photons, and some type of shielding pigment to allow the owner to determine the direction of light. By focusing on these two components, Kozmik and colleagues were streamlining the question of whether eyes evolved more than once, asking whether we could find evidence that photoreceptor plus pigment joined forces multiple separate times, or whether their partnership dates back to a singular union.


Photoreceptor components

Simplifying the real biology a bit, there are two primary classes of phototransduction, which is the cellular process sensing a photon and firing a nervous signal. One pathway that I will call “r” was first elucidated in flies, the other that I will call “c” was first elucidated in vertebrates. It was once thought that the r-pathway is an invertebrate trait, and the c-pathway is a vertebrate trait. However, the last 5 years have brought good evidence that c and r are present in both vertebrates and invertebrates, although the c-pathway is a bit cryptic in invertebrates, and the r-pathway is a bit cryptic in vertebrates. Kozmik et al investigated three components of phototransduction, all three components showed some evidence of being more similar to the “c” class of phototransduction. This primary conclusion led Kozmik et al to choose their title “Assembly of the cnidarian camera-type eye from vertebrate-like components”.

The first component they studied was opsin, a protein that binds to a light reactive chemical to initiate light perception in animals. With opsin, they argued for “c” type phototransduction, as opposed to the “r” type of fly compound eyes. Opsins form multiple sub-families, and the box-jelly opsin might be within the c-opsin subfamily based on their phylogenetic analyses. However, the analysis presented in the supplement of this paper is actually rather inconclusive about c-type status, although it is definitely not an “r”-type. We did a quick reanalysis and found the box jelly opsin might actually belong to a cnidarian-specific opsin sub-family that we discovered last year and which we named “cnidops”. None of the cnidops genes were included in the Kozmik phylogenetic analysis.

Regardless of its sub-family type, this opsin was found to be expressed specifically in the box jelly eyes. One of the most interesting new pieces of science in this paper is that Kozmik et al were able to match the function of the protein itself with that of the jellyfish eye. To do this, they functionally activated box jelly opsin in cell culture and measured the protein’s function. Cell culture is the practice of growing isolated animal cells under controlled conditions, without an animal itself. Introducing the box jelly opsin protein to cells in culture allowed the protein to fold properly and bind to a light- reactive chemical that was separately introduced into the cells. By shining lights of particular wavelengths (“colors”) on to the cells, the authors could see which colors of light activated the box jelly opsin protein. As expected if the opsin in question is used in box jelly eyes, the authors found that the opsin is sensitive to similar wavelengths as the jellyfish eye itself (light we would call blue-green, of about 465 nm wavelength). The match between the animal's light response and that of the expressed opsin protein is a very good piece of evidence supporting the idea the opsin they studied is involved in the animal's light response. This is one of the first times that an invertebrate opsin has been studied in cell culture, and certainly the first Cnidarian opsin, so this is a very exciting experiment.

Evidence for other components of the “c”-pathway being used in box jelly eyes are preliminary. The authors did find that the mRNA of genes similar to vertebrate c-pathway genes were present in the box jelly eye. However, this was as far as the present study went with the non-opsin components. Namely, they did not yet investigate protein expression, nor did they yet conduct any biochemical experiments to demonstrate the interaction of opsin and the other phototransduction components they found. Granted, these additional experiments represent a lot of work. The authors also did not report any experiments to show that r-pathway or other similar genes are not expressed in box jelly eyes (but I note they did not mention the presence of these genes in their library of genes from the box jelly eye, so perhaps they really are absent from the library). In the end, it remains a bit of a leap of faith to conclude that the opsin is actually interacting with the other genes, reported only from mRNA. Nevertheless, the authors have taken some important steps in that direction, so for this essay, we can give the authors the benefit of the doubt that a c-pathway is interestingly being used in the box jellyfish eyes. Even if our hunch is true that it is actually our new “cnidops” class of phototransduction, it doesn’t change the main message here; the herring will remain red.

The second criterion, besides the presence of photoactive cells, required to satisfy a minimal definition of an eye, is the presence of one or more pigmented cells. Here again, Kozmik et al found that pigment-components of a box jelly eye are very similar to pigment-components of vertebrate eyes. Here, the data are quite conclusive. The authors found genes homologous to vertebrate melanin genes expressed in parts of the jellyfish eyes that contain abundant pigment. In addition, there is a direct chemical test for melanin, which box jelly eyes passed. Interestingly, box jelly cells have dual function as photoreceptor and pigment-bearing cell.

The conclusion
Based on these data, Kozmik and colleagues favor the conclusion of parallel evolution – the separate assembly of homologous (“the same”) components to form eyes. In other words, they argue that box jellies and vertebrates separately evolved eyes, but happened to use the same components in each case, opsin and melanin. This conclusion is a bit of a curveball given how I introduced the study above. The conclusion is that the jelly and vertebrate eyes share the same components, so why do they not conclude a common ancestry of the eyes? They actually do point out that this is an alternative possibility. However, they favor parallel evolution based on what boils down to inferring phylogenetic history of these components and of eyes more generally. Unfortunately, they only use verbal arguments, instead of the well established statistics of phylogenetics and ancestral state reconstruction, which could’ve been used to test their claims statistically (see this paper for examples).
The main verbal argument of Kozmik for parallelism, and against common ancestry, is that many animal phyla do not have eyes. As such, it would seem that eyes would have to be lost in many phyla, if common ancestry of box jelly and vertebrate eyes holds (this is where a real phylogenetic statistical test would be nice – undergraduate honor’s project anyone?). In addition, they point out that cnidarians and vertebrates utilize different transcription factor genes in the specification of eyes during development. So basically, they are assuming a priori, based on previous evidence, that the eyes are of “independent origin”, and so based on that assumption, it is surprising to find that they use the same components.


Back to the red herring

So, both vertebrates and box jelly eyes may use c-pathway photoreception and both use melanin as a shielding pigment. You might be wondering where I stand – for parallelism or for common ancestry? Arrrooofff. Bow, wow, wow. Did I catch you? Has your mind been bounding down that pungent scent trail, sniffing and howling enthusiastically? Or have you kept the main, fainter trail, taking my advice that this question of number of origins is misplaced? Perhaps some more explanation will help you understand my point, and wizen your inner bloodhound. Let’s follow the red herring trail and see where it leads.

First, in case it’s not already clear, I’ll point out that the question of parallelism versus common ancestry of box jelly and vertebrate eyes is asking about the number of eye origins. It is our red herring question. Parallelism implies two origins, two separate unions of photoreceptor and pigment. Common ancestry implies a single merger, at least for the two eyes in question.

The reason I don’t like the red herring question, is that it puts the focus on “the eye” rather than on the components that define the eye. The Kozmik et al study is about the components – they elucidated for the first time some of the molecular components of a box jelly eye. This is noteworthy. But what do we gain from saying that eyes originated more than once? I think very little, and in fact such a conclusion masks some of the interesting biology. For example, stating that “eyes originated more than once” fails to recognize the common ancestry of some of the components, notably opsin. Any animal eye that has been examined to date, in addition to photoreceptive cells not in eyes, utilizes a homologous gene family (opsin). This point gets lost when simply stating that eyes evolved more than once.

A related difficulty is that this perspective neglects an intermediate stage in the complexity of photoreceptive structures. Someone unfamiliar (say an anti-evolutionist) who reads “eyes evolved more than once”, imagines the genesis of complex eyes from nothing. But that is not how evolution works. Evolution uses building blocks used for other functions in new combinations. This is illustrated by the conclusion of parallelism of Kozmik et at. In their model, opsin-based phototransduction existed unassociated with pigment cells. Once phototransduction and pigments became associated, perhaps separately in the box jelly and vertebrate lineages, the organisms came to posses a minimum definition of “an eye”. But this definition is just a human construct. Again, to my mind it obscures the fact that much of “the eye” was already there, it just took a new association of components (photoreception plus pigment) to evolve an eye. [For the cynics arguing that this just pushes back the real origins, I recognize this, which is why my lab is studying the origins of phototransduction – by studying the evolutionary history of each of the components separately. The bottom line – phototransduction evolved by using existing and newly duplicated and diverged components, a common theme in evolution].

You may be asking what if the opposite answer of the red herring question holds. What if we conclude “eyes share a common ancestry”, which could be concluded based on the Kozmik et al data of shared opsin and pigment components in vertebrates and box jellies. Again, I would argue that we gain little by making this statement. In this case, such a statement can only be made for the components in question. Perhaps it can serve as a sort of “null hypothesis”, where it serves as a prediction for new data that we don’t yet know about, which has some value. However, we already know that for eyes, not all components have the same history, which is implied by the statement “eyes only evolved once”. We already know that different lens proteins are used in different types of eyes. We also already know that components of phototransduction cascades differ. For example c-phototransduction utilizes the ion channel protein CNG, whereas r-pathways utilize the unrelated ion channel protein TRP. Saying that all eyes have a common ancestry does not account for these details. Again, it is about the components. Different components have different histories, and this cannot be accounted for in the simple dichotomy of “one versus more than one origin”.

The question of the number of eye origins has been around for a while now. But I argue that it is time to move beyond this question, and to recognize it for the red herring that it is. The fact of the matter is that some eye components are shared and others are not, and this varies depending on the time scale and species examined. Of value is to fill in the narrative of this amazing evolutionary story. We now have the ability to understand to the level of specific molecular changes how vastly different types of eyes evolved. This is the main – though perhaps fainter – scent trail.