Wednesday, December 31, 2008

Evolutionary Novelties: Faves of 08

As 2008 winds down, I thought I would look back at Evolutionary Novelties and pick some of my favorite posts of the year.

The major theme of this blog is to explore how it's possible that all life has a common origin and still has diversified into the riotous diversity/complexity/disparity that we see today. New features evolve through duplication and recombination (at all levels of biological organization).

1. Box Jellies and the Red Herring of Eye Evolution is one of my favorite posts. The main thesis is that people always ask an inappropriate question "how many times did eyes evolve?". I'd thought about this idea for quite a while, and when a paper came out in PNAS that re-inforced my thesis, I incorporated the new research into the idea.

2. Coming to grips with common descent discusses the idea that during the history of evolution, people have tended to forget that everything evolves from something else. This was not conceived as a blog post, but as a chapter of a book I've toyed around with writing. In some ways, blogging satisfies my urge to write a book, so the book probably won't happen for a long time.

3. Gould: Pluralism by Monism My thesis that Gould was practicing pluralism by taking an opposing stance to the whole field of evolutionary biology. This is perhaps my favorite post of 2008 because I've never seen anyone else with this idea, and the more I think about it the more I think it explains a lot, a general theory of Gould, if you will.

The above are posts that present an idea I've had. I've also recently been writing a few posts on others' research. I find that writing about the work helps me internalize and understand the work. I'm not a rocket-science journalist, but some of the posts have been okay, I think:

4. Evolutionary Novelty: Photosynthetic Slug

5. Evolutionary Novelty: Hair

I also have a series of posts about ostracods, my ostrablogs. I haven't had time to do these for a while, but I do have one half written, so more are coming. My favorites are probably:

6. Ostrablog 5 - Three shows and a funeral retells a story that I've told many, many times in person.

7. Ostrablog 3 - How we discovered chupacabra tells about our discovery of a new ostracod species.

8. Ostra-blog 2 - to e or not to e Ostracod or ostracode?

But much of what I do is promotion of my research and papers, or posting drafts of things I'm writing:

9. Phylogeny, evolution, biodiversity and ecology discusses some research recently published in PNAS. I also noticed this was featured at NESCENT.

10. Opsins: An amazing evolutionary convergence. Slightly expanded from part of an encyclopedia article I was asked to write.

Those are 10 of my favorites from this year. Happy New Year!!

Tuesday, December 30, 2008

Two New Blogs

Greetings from the frozen tundra. I've been in Milwaukee catching up with family and friends during the holidays. Visiting has been a full time job, and I've been online very little, but 2 new blogs have come to my attention, both by colleagues of mine:

First is "A Fish Eye View"

Next is "The EEB and Flow":

Friday, December 19, 2008

Opsins: An amazing evolutionary convergence

How predictable is evolution? If we could travel back in time 4 billion years and make a few changes, what would remain the same upon our return? This is an enduring topic of evolutionary inquiry (and movies and sci-fi shorts for that matter).

In his book Life's Solution, Conway-Morris made the case for a semblance of predictability in evolution. He argued that convergence - the independent origin of similar traits - represents an element of predictability in evolution. Octopus and humans have outwardly similar eye designs, so if we reply animal history over and over, these camera-type eyes would likely evolve in most replays.

Here I'll describe a truly amazing molecular convergence that was not discussed by Conway-Morris: the independent evolution of opsin proteins (a protein responsible for light perception) in two different groups of organisms. It turns out that a 7-transmembrane protein (opsin), bound to a light reactive chemical on the 7th transmembrane domain, has evolved twice to sense light!

If we could go back a few billion years and replay the evolution of life on earth a few times, chances are, opsins would evolve in many of our replicates.

[Disclaimer - the following is text from an encyclopedia article I've been asked to write on opsin evolution, so the writing style is a bit terse from here on out. I will add a little bit though, specially for the blog. But since many people I know think opsin originated only once, I feel it's my duty to spread the word of opsin convergence, starting here, at Evolutionary Novelties].

What is opsin and rhodopsin?
Opsins are a group of proteins that underlie the molecular basis of various light sensing systems including phototaxis, circadian (daily) rhythms, eye sight, and a type of photosynthesis. Opsins are sometimes called retinylidene proteins because they bind to a light-activated, non-protein chromophore called retinal (retinaldehyde). Opsins are also in some cases called “rhodopsins”, a name originally given to isolated visual pigments that contained both opsin protein and non-protein chromophore in a time before the two separate components were known. Today, the term “Rhodopsin” is used commonly to describe the opsin expressed in vertebrate rod (dim-light) photoreceptors, and the opsins of certain organismal groups, like bacteria. All opsin proteins are embedded in cell membranes, crossing the membrane seven times.

Type I and Type II opsins
Two major classes of opsins are defined and differentiated based on primary protein sequence, chromophore chemistry, and signal transduction mechanisms. Several lines of evidence indicate that the two opsin classes evolved separately, illustrating an amazing case of convergent evolution.

Type I opsins are present in bacteria and algae and are referred to by various names, including bacteriorhodopsin, bacterial sensory rhodopsins, channelrhodopsin, halorhodopsin, and proteorhodopsin. Type I opsins have varied function, including bacterial photosynthesis (bacteriorhodopsin), which is mediated by pumping protons into the cell, and phototaxis (channelrhodopsin), which is mediated by depolarizing the cell membrane. Type II opsins are present in eumetazoans (animals not including sponges), but are unknown from sponges or any non-animals. Because opsins are known from cnidarians and bilaterian animals (animals with bilateral symmetry, including humans, flies, and earthworms), Type II opsins are inferred to have been present in their common ancestor, which lived about 600 million years ago. Type II opsins have varied function, including phototransduction and vision, circadian rhythm entrainment, mediating papillary light reflex (pupil constriction), and photoisomerization (recycling the chromophore).

Despite their functional similarity and despite both being 7-transmembrane proteins, multiple lines of evidence indicate that Type I and Type II opsins evolved independently. First, the primary amino acid sequences of Type I and Type II opsins are no more similar than expected by chance. For example, try to align a Type I (say bacteriorhodopsin) and Type II opsin together. I just tried this with blastalign, with the following result:

Exhibit A. Blast search find "no significant similarity" of the amino acid sequences.

Sequence 1: gi|163443|rhodopsin
Length = 348

Sequence 2: gi|208055|bacteriorhodopsin >gi|208057|gb|AAA72603.1| bacteriorhodopsin
Length = 249

No significant similarity was found
CPU time:     0.04 user secs.     0.02 sys. secs     0.06 total secs.

Second, the orientation of the transmembrane domains differs between the major groups. We now have crystal structure data for both Type I and Type II opsins, and the arrangements of the parts of the protein that are stuck in the cell membrane are quite different, inconsistent with a single origin of opsins (unless this changed a lot during evolution, which is not impossible).

Exhibit B. Type I on the left, Type 2 on the right. Denser lines are positions of transmembrane domains. Figure is from Spudich et al (2000)

Third, the major opsin groups differ in chromophore chemistry. Prior to light activation, the chromophore of Type I opsins is an all-trans isomer. Light activation then involves isomerization of the chromophore to 13-cis retinal. In contrast, prior to light activation, the chromophore of type II opsins is 11-cis retinal. Light activation of Type II opsins involves isomerization to all-trans retinal.

Exhibit C. Type I on the left, Type 2 on the right. Chromophore chemistry differs. Figure is from Spudich et al (2000)

Fourth, Type II opsins belong to the larger protein family called G-protein coupled receptors (GPCRs), which transmit varied signals from outside to inside cells by activating GTPase proteins, which in turn signal to second messengers that affect the state of the cell in various ways. Type I opsins do not activate G-proteins. Furthermore, Type II opsins are more closely related to non-opsin, light insenstive GPCR’s than they are to Type I opsins. So even if there is some very, very distant and *undetectable* common origin of Type I and Type II opsins, chromophore binding likely evolved twice. Since chromophore binding is what allows photosensitivity, it is the crux of being an opsin (but see), and the realization that Type II opsins are closer to non-opsin GPCR's than Type I opsins is strong support for two separate origins.

Exhibit D. (Dashed lines mean no sequence similarity beyond random. Light bulbs mean origin of chromophore binding=light sensitivity=opsin.)

Finally, with two CS students, I tested the single origin hypothesis in a different way and found no support. Type I opsins show similarity of membrane domains 1-2-3 and 5-6-7, consistent with an origin by duplicating a 3-domain protein (and adding one). However, Type II opsins show no such similarity. If they Type I and Type II share a single origin, the duplication pattern of the domains should be shared too (unless there were drastically different rates of evolution in the 2 lineages, which is not impossible). This work is described here: Larusso et al (2008) J Mol Ev.

John L. Spudich, Chii-Shen Yang, Kwang-Hwan Jung, Elena N. Spudich (2000). RETINYLIDENE PROTEINS: Structures and Functions from Archaea to Humans Annual Review of Cell and Developmental Biology, 16 (1), 365-392 DOI: 10.1146/annurev.cellbio.16.1.365

Wednesday, December 10, 2008

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.

Tuesday, December 9, 2008

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.

Monday, December 8, 2008

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


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)