I am fascinated with zombies. Always have been, but even more so since I took an interest in microbiology. The zombie apocalypse is the best known and best chronicled viral infection which hasn’t happened. But it could happen any day, so stock up on non-perishable food, medical supplies, water purification tablets, chainsaws, machetes, baseball bats, crossbows, semi-automatic firearms, and as many disposable acquaintances as you can get hold of. Signs of the zombie apocalypse may include your significant other turning a putrid-greenish shade of rotten and trying to chew your neck off. Beware of the differential diagnosis that they might just be using a bit too much makeup, are not wearing deodorant and feeling flirtatious. Remember to eliminate that possibility before cracking your beloved’s head open with a crowbar.

Here are three interesting studies all having to do with zombies.

The Zombie Roach

One problem that has to do with zombification is the loss free will. Do zombies have free will? More to the point, do humans have free will? 28 Days Later and both versions of Dawn of the Dead have survivors finding refuge from the zombie apocalypse at shopping centers. While at the shopping center, the survivors copiously consume the goods in the stores, making you think who really is the mindlessly-obsessed drone lacking free will. In two papers entitled A Wasp Manipulates Neuronal Activity in the Sub-Esophageal Ganglion to Decrease the Drive for Walking in Its Cockroach Prey and  On predatory wasps and zombie cockroaches — Investigations of “free will” and spontaneous behavior in insects, Ram Gal and Frederic Libersat from Ben Gurion University explore free will in cockroaches. Do cockroaches have free will, or are they just sophisticated automatons? And where do we draw the line between the two? Gal and Libersat  use the following definition for free will: the expression of patterns of “endogenously-generated spontaneous behavior”. That is, a  behavior which has a pattern (i.e. not just random fluctuations) and must come from within (i.e. not entirely in response to external stimuli). They cite studies where such behavior — which they define as a “precursor of free will in insects” — is observed. They then show how this behavior is removed from cockroaches when the roaches are attacked by a wasp. Their description of the process is so colorful, I shall simply reproduce it here. This is some of the most delightful and engaging prose I have ever read in a scientific paper.

Unlike most other parasitoids, this tropical Ampulicine wasp does not simply paralyze its prey to immobilize it. Instead, it stings a cockroach in the head (Fig. 1A) and injects a neurotoxic venom cocktail directly inside the cerebral ganglia (Fig. 1B). This turns the cockroach, metaphorically, into a submissive ‘zombie’: it gradually enters a long-lasting hypokinetic state, during which it becomes unresponsive to aversive stimuli and fails to self-initiate walking or escape behaviors. Although the stung cockroach is not paralyzed, it allows the wasp to cut both its antennae and drink hemolymph from the cut ends. The wasp then grabs one of the antennal stumps and pulls backwards, leading its prey into a pre-selected nest. The intoxicated cockroach, rather than fighting or fleeing its predator, actually follows the wasp submissively. In doing so it demonstrates a completely normal walking pattern, as if it was a dog led by his Master’s leash. The wasp then lays one egg on the cockroach’s leg, seals the nest and leaves the lethargic prey inside, still alive but powerless to escape under the influence of the venom. As the wasp larva hatches from the egg, it penetrates through the cockroach’s cuticle and feeds on its internal organs for several more days. Only then, roughly five days after the sting, does the cockroach finally die and the larva pupates inside its abdomen, safe from predators outside the nest.

A. The parasitoid Jewel Wasp A. compressa stings its cockroach prey inside the head. B. Schematic drawing of the cerebral nervous system (yellow) inside the cockroach's head capsule. the wasp's stinger (st., scanning electron micrograph drawn to scale) reaches to inject venom into both cerebral ganglia, namely the supra-esophageal ganglion (SupEG) and sub-esophageal ganglion (SEG). Scale bar: 0.5 mm. Source: Commun Integr Biol. 2010 Sep-Oct; 3(5): 458–461.

What they also found was that the venom injection does not affect the roach’s muscle, motor neurons or sensory neurons. Those are all intact. Stung cockroaches will walk slower and submissively follow their wasp mistress, but if placed in water they will start paddling frantically like unzombified cockroaches trying to save themselves from drowning. Indeed, the zombies paddle as frantically as non-zombies, but for a much shorter time, as if they despair quicker.

But ah, you say —  these cockroaches are not “real” zombies are they? Or rather, not the type of zombies from which the zombie apocalypse would be created. After all, a zombified roach is not infectious, and thus the disease would not spread from roach-to-roach in exponentially rising numbers by having mad roaches bite each other. In fact, the roach becomes catatonic and subservient to its mistress, more like the original Voodoo zombie, a reanimated corpse under the control of a shaman.

So how about molecular zombies?

Consider plants. Not zombie plants, but zombie genes in plants. Actually, transposable elements or TEs. TEs are DNA elements that self-replicate, in their own genomes or may be transferred into other genomes. Most eukaryotes have them. Indeed, 17% of the human genome is composed of Long Interspersed Integrated Elements or LINES. LINES simply replicate through the genome, and their contribution, if any, to the fitness of the organism is not known. some TEs are like internal viruses: replicating, adding their sequence, but little else, to their “host” genome. Only by increasing their numbers, they may at some point change their host genome. They may write themselves into some vital piece of DNA, and cause genetic damage that, if it does not kill the carrier while still an embryo, may cause long-term debilitating damage to the species by fixing itself in the population and moving down the generations. The genetic load of TEs in plants is huge: in Maize they make up the majority of the genome, with 85% of the genome coding for TE genes.

But the self-selection of TEs to spread in the genome is also their undoing. Small pieces of RNA derived from TEs are used by the host to target full TEs and degrade them through a group of processes known collectively as RNA silencing. Some TEs do generate an RNA or a protein end product. Those smaller, derived aberrant TEs were nicknamed ‘zombies’ in a paper by Damon Lish from University of California, Berkeley and Jeffrey Bennetzen from the University of Georgia, Athens. There is an ongoing battle between the TEs and the zombie TEs, with the latter silencing the former, yet metaphorically feeding off the original TEs existence. If the ‘live’ TEs did not exist, the ‘zombie’ version of them would not either. The more copies of TEs a genome has, the more zombie TEs it will have. TEs inserting themselves near active genes may subject these genes to silencing by zombie TEs. This ability of plants to silence their own genes by shuffling TEs around generates new patterns of gene expression. Also, the same genes that may be inhibited due to their proximity to TEs may, at some point, re-express themselves if the TE is removed from that position in the chromosomse. So zombie TEs, which are a form of defense against viral TEs that cause chromosome damage, are also a mechanism for generating new genes and expression patterns: an evolutionary tool.

Transposable elements ("jumping genes") are responsible for the different colors in Indian corn. TEs are controlled by their "zombie offspring": short interfereing RNAs whose sequences comlement those of the TEs, silencing TE expression.

Finally, there are the zombie ants

I have written about zombie ants before:

Here is a parasitic fungus that infects ants. The infected ant wanders away from its nest; the ant then reaches a leaf or another plant part. The fungus makes the ant to bite the leaf so powerfully, it hangs from the leaf until it eventually dies; and then (excited-by-gross-stuff six-year old emerging): the fungus grows an upside down stalk out of the dead ant’s head, releasing spores that fall to the ground. The spores are then picked up by ants that walk over them, causing them to wander away from the nest, bite other leaves…  Ad nauseam. Wow.

Briefly, once infected, the ant’s behavior is hijacked to  act as a delivery system for the fungus, which is finding a  good location to die and infect more ants.

 

Ophiocordyceps unilateralis is the fungus that wreaks this havoc on the ants. Indeed, an O. unilateralis infection in ants is the closest parallel we can find to the human zombie apocalypse. The infection changes the ant’s behavior to infect more ants, and can decimate whole colonies.

But is there only one species of fungus? Harry Evans, Simon Elliot and David Hughes were inrigued by the original description of Torrubia unilateralis, as it was called at the time. In 1865, Louis René Tulasne a French mycologist, described a leaf-cutting and as the host for the fungus. His brother, Charles Tulasne, worked with him and illustrated their findings. Charles’s drawing of an infected ant does not depict the leaf-cutter: rather, it appears to be a carpenter ant, with its characteristic spines. The fungus has only ever been found infecting carpenter ants. Could Louis have made a mistake? Maybe there other species of ant-zombifying fungi out there?

a. Original plate from the 1865 Selecta Fungorum Carpologia of the Tulasne brothers, illustrating the holotype of Ophiocordyceps (Torrubia) unilateralis and said to be on the leaf-cutting ant, Atta cephalotes; b. Detail from plate showing the distinctive pronotal plate of Camponotus sericeiventris, as well as a side view of the host which is clearly a carpenter ant and not a leaf-cutter; compare with c. Live worker of C. sericeiventris showing the spines on the pronotal plate (arrow). Source: doi:10.1371/journal.pone.0017024.g001

Indeed there are, and the authors of this study found four new species in the Brazilian rain forest, all distinct by shape and development. All infecting carpenter ants, (no leaf cutter ants found to be infected yet!)  but four different species of carpenter ants: Camponotus rufipes, C. balzani, C. melanoticus and C. novogranadensis – are each attacked by a distinct species of Ophiocordyceps. Plenty of great pictures in the paper describing the differences between the ant-zombifying fungi.

Happy zombie-bashing! (Warning: Pop-up link to an external flash game).

Gal, R., & Libersat, F. (2010). A Wasp Manipulates Neuronal Activity in the Sub-Esophageal Ganglion to Decrease the Drive for Walking in Its Cockroach Prey PLoS ONE, 5 (4) DOI: 10.1371/journal.pone.0010019

Gal, R., & Libersat, F. (2010). On predatory wasps and zombie cockroaches: Investigations of free will and spontaneous behavior in insects Communicative & Integrative Biology, 3 (5), 458-461 DOI: 10.4161/cib.3.5.12472

Lisch, D., & Bennetzen, J. (2011). Transposable element origins of epigenetic gene regulation Current Opinion in Plant Biology, 14 (2), 156-161 DOI: 10.1016/j.pbi.2011.01.003

Evans, H., Elliot, S., & Hughes, D. (2011). Hidden Diversity Behind the Zombie-Ant Fungus Ophiocordyceps unilateralis: Four New Species Described from Carpenter Ants in Minas Gerais, Brazil PLoS ONE, 6 (3) DOI: 10.1371/journal.pone.0017024

Not a cell wall

So, for example, when I am developing computational metagenomics analysis tools, they invariably tend to target both bacteria and archaea. However, these tools are usually not good for microbial eukaryotes, due to different rRNA size, the larger genomes with more non-coding regions, lack of operons, organelles genomes, introns, etc. So for this utilitarian purpose, “prokaryotes” would be a good verbal shortcut to the cumbersome “bacteria and archaea” when describing or documenting the software. So can we all agree on “prokaryotes” as a verbal shortcut of necessity but not as a taxonomic definition? Or am I missing something substantial here?

An illustrative example of the rational, cool-headed debate that may ensue:

Herpetology Credit: xkcd.com

Yes, it’s that time when we all get together in front of the screen to watch another beautiful game played by that fantastic team contributing to the Carnival of Evolution. This time hosted on the lovely green pitch of Byte Size Biology. So get your popcorn, sunflower-seeds, crisps or any other culturally-appropriate sports-watching food and…… the referee whistles! The game has begun!

Phenotypes! How do they happen?

Kicking off is Grrlsicentist from Punctuated Equilibrium telling us How the Penguin got its Tuxedo. While skillfully dribbling across the field, she tells the story of fossilized feathers from a giant, extinct penguin which contain fossilized melanosomes: intracellular structures whose shape can that tell us of the feather coloration of the bird. No, it was not black and white, but rather brownish and gray. However, melanosomes also strengthen the feathers, and today’s giant melanosomes, giving the familiar black coloration may have evolved as a results of a selection for feather strength, rather than color. Feather-minded (but far from feather brained!) she touches the ball across the defender and reports on how the parrot got its beautiful plumage. (Norwegian Blue?) Would you have thought resistance to bacteria degradation?! A short pass to Jerry A. Coyne who, while on the same topic, explains in Why Evolution is True about the evolution of cat coat-patterns and other issues relating to genetics of the coat in cats.  He makes a quick pass to Bjørn Østman who may have personally discovered the next stage* in feline evolution: the six digit cat! Bjørn toe-punches the ball hard and…

…the ball travels high forward left  to be intercepted by Eric Michael Johnson from The Primate Diaries in Exile. He high-knees the ball twice while asking whether our ancestors were polygamists, monogamists, or happy sluts? All this in his post: “Sex Evolution and the Case of the Missing Polygamists“. Eric launches it off with a strong left kick, the ball arches and jumps once on the ground, only to encounter  Jason Goldman’s knee, bouncing the ball while showing a movie which presents two different hypotheses explaining how wolves were domesticated into dogs. The first: young wolves would be adopted into the camps of early humans. Only those who were most tame would breed with eachother, and over many generations, the domestic dog would emerge. The second: wolves “chose” to be domesticated – they noticed a lot of tasty trash around human encampments, and if they were unafraid enough to hang around, they got to eat lots of leftovers, and those individuals would mate, and over generations, the domestic dog would emerge. His theory-and-ball juggling are interrupted by Kevin Z who takes over smoothly and talks about eyes and sex in lizardfishes posted at Deep Sea News. Kevin now with a square pass to John Wilkins who ponders a rather big question in our understanding of speciation: how many concepts of species are out there? He passes the ball all the way to Hannah Waters in the 16 meter box, who cleanly intercepts the ball while asking a related question: are Eukarya actually part of the Archaea domain, making life a two-domain system, or does the three-domain system still hold? But just as she is about to turn the ball around preparing for a shot at the goal, the referee (whom some say is biased towards the now-defunct 5 domain hypothesis) whistles for an offside violation, prompting loud boos from the crowd! Hannah grudgingly relinquishes the ball, which is given to the other team.

Evolution and Creationism

ProbabilityZero dead-balls a strong and furious kick. Furious over the agenda of the US Tea Party that includes teaching creationism in US public schools. All this in the recurial blog. The ball travels to Jayson D Cooke who is asking in an open letter why the University of Southern Queensland in Australia is hosting a creationist event under a scientific guise, he also defended his opinion on the air. Meanwhile in the stands, Michael D. Barton is selling cartoons of Darwin and evolution (from both sides of the fence, also here) from The Dispersal of Darwin. Some of the football fans accuse Michael of selling products of a man who advocated “Might is Right”. That is patently untrue, for many different reasons, the chief one being a misunderstanding of the word “fittest” in “survival of the fittest”. Fittest does not means “strongest”, but “the best able to reproduce”. However, Michael’s business associate, Eric Johnson decides to talk to the crowd about Darwin as a compassionate person, as manifested in his opposition to vivisection.

Lucas Brouwers from thoughtomics appears from ProbabilityZero’s blind-side, grabs the ball and, considerably faster than plate tectonics, advances up the pitch to the rival penalty box. Although, speaking of plate tectonics, Lucas talks about how freshwater crabs help us map continental drift. He is tackled by a rival player, falls, gets up, picking burrs from his socks, and wondering how they evolved? (The burrs, not the socks.) The answer comes from Melissa who while out walking the dog talks about the burry man, the burry dog and burdock. Why she is walking the dog in the middle of a football game? No idea.

Lucas forward-passes to another player concerned with speciation, Jeremy Yoder at Denim and Tweed talks about the speciation of rockfish: it appears that in many cases depth, not geographic distance, is the allopatric factor in rockfish speciation.  He passes it to DeLene Beeland who takes this question even further: how do we define species in the first place? She turns the ball around, sets for a kick and… goooooaaaaaaal!!!!! Yes! In the stands, Digital Cuttlefish dances with joy.

The referee whistles for halftime, and the players, sweaty and covered with mud and burrs step off the pitch.

Halftime

While we are waiting for the second half to begin, Bjørn Østman tells the viewers at home why intelligent people watch more TV. Or, perhaps not? Read to find out. This public service announcement has been sponsored by Time Tree: just enter the names two species, and find out how long ago they diverged! While the players are resting, they audience watches a beautiful video of the Applied Evolution Summit in Heron Island, courtesy of R. Ford Denison from This Week in Evolution. Also, Bjørn announces the long-awaited results of the Carnival of Evolution Readers Survey. One interesting point that came up is the contentious phrasing of the question: “do you believe in evolution?”

The second half begins. A short pass by Greg Laden explaining what is the most important human adaptation. (Hint: no, not bipedalism.) Zen Faulkes sprints forward – and wonders: did sprinting behavior shape the stings of scorpions, or is this explanation yet another “just so” evolutionary story? Cross-pass to R. Ford Denison who talks about the evolutionary benefits of cooperation and kin selection. Specifically, that Hamilton’s rule still holds, even though it has recently come under fire in a much publicized article in Nature. Competition is also an adaptive force, and Becky Ward tells us about the weird competition between a spider and a plant: both of which are predators! She passes to Lucas Brouwers, who makes small adjustment to the ball’s trajectory before passing it on, noting that evolution also generates novelty through subtle tinkering.

So how does the game end? It doesn’t. Evolution does not end. It just keeps going on and on and on… The next Carnival will be hosted at This Scientific Life. It is never to early to submit.

Despite our best attempts to remove species from the face of the Earth, there is still quite a bit of life out there and it is still quite diverse. Also, there are still quite a few people who want to document, describe and make the rest of us aware of the magnitude and diversity of life. In the time-honored tradition of natural history they take the tools of their trade to the field to sample, collect, identify, tag, photograph, film, mount and otherwise understand and advertise Nature’s progeny.  There are probably thousands of web sites dedicated to taxonomy of families, genuses genera and species. Trouble is, they are all “out there”, and require quite a bit of searching to find those that are of interest to you. And what if you just want to browse, the Internet equivalent of going through a natural history museum?

Museums were historically the place where natural historians brought their findings from far away places to be studied and displayed (if lucky) or simply archived. If the finding was still alive, it would go to the zoo or the botanical garden.  And people would go to the museum, zoo or garden to see the  latest wonders of life.

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(From Life Through a Lens: the Natural History museum (of London) 1880-1950)

Virtually every biology lab with some taxonomic interest in  a given species, genus or family would have such a site. That’s a lot of taxonomic information , but is not very accessible or organized! What if all these sites could be rounded up together, connected in some contextual fashion, some semblance of standardization? Then we could have an online Natural History museum, where the displays accumulate, are constantly updated, and we can walk through virtual halls looking for the plant or animal of our fancy.

Scratchpads is a cool way of getting to that online Natural History museum. Actually, it is hosted in the great-grandaddy of brick-and-mortar natural history museums, the one in London.

Scratchpads are an easy to use, social networking application that enable communities of researchers to manage, share and publish taxonomic data online. Sites are hosted at the Natural History Museum London, and offered free to any scientist that completes an online registration form. Key features of the Scratchpads include tools to manage:

	Classifications		Phylogenies
	Bibliographies		Documents
	Image galleries		Custom data
	Specimen records		Maps

Users control who has access to content, which is published on the site under Creative Commons (by-nc-sa) license.

Data added to a Scratchpad are automatically classified and grouped around a taxonomy that is supplied by the users or imported from EOL. This is optionally supplemented with information from high quality web accessible databases, to automatic construct content rich web pages about any documented taxon. Currently these sources include Genbank, GBIF, Biodiversity Heritage Library, Yahoo! Images, flickr, Google Scholar and Wikipedia.

When you start a Scratchpad site, you are given a template on which you can build your taxonomy site. the template includes a tree-building widget, space for image galleries, a blog area, a bibliography area etc. You insert the content, and your site links back to the scratchpad mother site.  The Scratchpads linked from the mother site are in various stages of construction, which is actually pretty cool as you can see a village of taxonomy sites being constructed. Some are fairly complete and interesting to browse through, like the Scratchpad about freeloader flies or the one about nanofossils.

Time will tell if Scratchpads will catch on with taxonomists. I certainly hope it does. It seems  quite a bit of thought has gone into balancing standardization with creativity, and making scratchpading easy and manageabe. The authors have chosen templates based on the Drupal content management system, which has a very gentle learning curve. I am waiting on my own scratchpad account, where I intend to… well, you’ll see it on this blog eventually, I hope.

So if you are involved in taxonomy in some way, consider getting your own Scratchpad. This could make for a great student project, by the way.  If you know someone who is a taxonomist, pass this information on to them.