This post is the first in a six post series outlining the evolution of mimicry within the ocean realm. These posts detail various ways in which organisms may copy other organisms in appearance and behavior, and the evolutionary context for how these mimic-model pairings have come to be.

In the human world, being a “poser” can have serious repercussions.

Well, at least if you are found out by those around you. No one appreciates a fake. A phony. A liar. A disingenuous, duplicitous slimeball. Someone who is, as a notably troglodytic hobbit habitually says, “false.” Someone who appears to portray themselves as something they are not tends to raise the hackles of anyone in their immediate social circle. Sometimes, the issue is a complete breakdown of trust, and an inability for anyone to take your word or feelings seriously. You become an actor. A poor one, one that nobody believes. Sometimes, the transparency of your guise just becomes annoying and exasperating. Like if you saw Little Dragon do a set “at Sasquatch one year” and that was the only time you ever saw them perform, before or since, but now all you do is talk to your friend about how much of a “huge fan” you’ve always been, even though I…I mean your friend…was listening to Machine Dreams back when you were still listening to Jason fucking Mraz like an uncultured jackoff….even though you didn’t know about their collab with Gorillaz, and when asked where they were based, you shat out something about “New York mostly I think.” IT’S GOTHENBURG, FOR FUCK’S SAKE. STOP ACTING LIKE YOU KNOW THINGS, JEFF, BECAUSE YOU DON’T.

….anyways, posers can rub people the wrong way.

But in much of the natural world, faking your way through life may be a great strategy to keep alive and produce lots of offspring. Any trait that gives you in edge in getting food, not becoming food, and making sure you can make lots of babies (which also can get food and not become food) is likely to proliferate in the population. Sometimes, this means using deceit, and looking and behaving like something you are not. When a species resembles another in behavior or appearance (or any other sense), this is known as “mimicry.” The organism that a mimic is imitating is referred to as a “model”, and importantly, mimicry only really works for the mimic if the model is found in the same area. Evolutionary biology is rife with examples, many of which are found in terrestrial ecosystems, and often involve insects…because, partially, there are likely millions of insect species on the planet from which instances of mimicry can evolve. There are swaths of moths that have evolved to resemble wasps, and the moths benefit by fooling predators into thinking they can deliver a painful, venomous sting. European bee orchids have flowers that look very much like the solitary bee Eucera, successfully attracting horny male bees, which then find themselves inadvertently dry-humping a cruel, floral-scented bee blow-up doll, all the while unknowingly satisfying the pollen transportation needs of the orchid. The chicks of the Amazonian cinereous mourner (Laniocera hypopyrra) appear to mimic a fuzzy, rust-colored variety of noxious caterpillar, which helps them not get harassed by hungry wildlife, but at the cost of looking like something that would scamper off the scalp of a particularly controversial 2016 Presidential candidate that shall not be named. These are just a fraction of the examples. In the history of life on Earth, mimicry has evolved over and over again, because, quite simply, it can really pay to pretend to be something you’re not.

Of course, since mimicry is a bit rampant on this planet, it’s perhaps not surprising that there are many examples in the ocean. By and large, marine organisms aren’t the go-to for examples of broad evolutionary and ecological patterns, mostly because they are less familiar and accessible than terrestrial lifeforms (seeing and interacting with marine organisms requires getting under the water or out on a boat, typically, which is far more difficult than just walking out into your backyard to see land-living counterparts). For this same reason, science is comparably in the dark about rather basic things about how ocean communities work that we’ve nailed down for terrestrial ecosystems long ago. Many details are missing, despite us being aware that the level of biodiversity in the ocean is likely nearly comparable to what exists on land. So, for this series of posts, I’m going to address some of what we do know about these tricky evolutionary dynamics that are going on in the relatively hard-to-access and hard-to-study briny deep. Frankly, insects have had their day in the sun…er….I guess somewhat literally in this case.

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Look at the photo of the pair of fish at the top of this blog post. It may interest you to know that those two fish are not of the same species. Ok, you may nod at your computer screen, that’s possible. “Cryptic species” (species that are essentially morphologically identical to one or more very closely related species, but based on divergence at the genetic level, are wholly separate species) are a common thing in nature (probably more common than we give it credit for), and are certainly known in marine fish. But, this is not what is going on in this case. These fish are not close relatives, only differing in the slightest of genetic differences. They aren’t even kissing cousins, and in fact, they are on fairly different branches on the “tree of life.” These two fish are actually in entirely different taxonomic families. Within taxonomy, a “family” is a fairly large division, and organisms that are within the same order, but different families, can be separated by many tens of millions of years. One of these fish has evolved to look virtually indistinguishable from another species…a species that it hasn’t shared a common ancestor with in many millions of years….a quantity of time for its lineage to experiment, evolutionarily, with a multitude of different body shapes, swimming methods, dietary changes, etc. in parallel (but not together) with the lineage that eventually gives rise to its model. This is almost the equivalent of two classmates from high school meeting again at a 20-year reunion; at one point, their world experiences and who they were as human beings was relatively close, being peers, but the combination of time and divergence of experience has left them, at the endpoints of their respective journeys, wholly different, long since separated entities. The distance between the tines of the fork in the timeline of their lives is far greater at the tips than at the initial split. The mimic is far removed in evolutionary time from its model, and the inherently different path its ancestors have taken have left its mark on its biology…and yet it manages to be a maddeningly convincing copy.

How convincing? Well, I originally had planned on sharing a completely different photo that showcased both model and mimic side-by-side. In fact, I had it sitting in a photo folder for hours, and I had spent quite a bit of accumulated time looking at it, between scrolling up and down this page as I was writing this blog post once I had slapped it up at the very beginning of the entry, and seeing it in the folder itself. It took me an embarrassingly long time before I stopped and stared at this photo, squinted in disbelief, and conceded that I had made a mistake, and that the featured photo actually showed two of the same species of fish, and that…pathetically….not even the person writing a fucking blog post about these fish could reliably tell them apart.

The composite photo above makes finding their differing features much easier (it’s basically one of those “spot five differences” puzzles), but this type of comparative scenario is about as ideal as it gets, especially compared to a grainy photo of entire school of these things, or in life/video, when these fish are flitting about.

The fish in the top photo is the model. It is a Valentinni’s toby (Canthigaster valentini), and is a variety of pufferfish (Tetraodontidae) also commonly referred to as a “sharpnose puffer.” This species is also called the “black saddled toby” or the “saddle puffer” in reference to the black bands on its back and sides. Tobies (genus Canthigaster) encompass nearly forty species, and are found in tropical and subtropical reef environments the world over (but with far more diversity in the Indian and Pacific Oceans). These fish are small by puffer standards, and often only reach a few inches in length.
On the bottom is the mimic that has evolved to resemble the saddle toby. It is the blacksaddle filefish (Paraluteres prionurus). Filefish make up the family Monacanthidae, and are found in warm ocean waters around the world. This species, unsurprisingly, has a distribution that mirrors that of its toby model, ranging from East Africa east through the tropical Indo-Pacific to Fiji, north up to southern Japan, and south to the Great Barrier Reef.

Pufferfish and filefish make up two families within the order Tetraodontiformes, which also includes other rather bizarre groups like boxfish, triggerfish, and the massive ocean sunfish. While this means that they are closely related within the grand scheme of fish evolution, these two families are separated by more than 60 million years of evolution, meaning that their most recent common ancestor may have been swimming in the oceans around the time the big, non-tweety bird categories of dinosaurs were snuffed out of existence. For some frame of reference, 60-65 million years is roughly how far you’d have to go back to find the most recent common ancestor of humans and aye-ayes. So yeah, these two lineages have had ample time to develop some very large physical differences from one another….yet the blacksaddle filefish does a fine job of passing itself off as a toby.

But why bother? Trying hard to look like something you’re not seems reserved for things like trying to be impressive on a first date, gliding past all your flaws for a job interview, and attempting to convince the pizza delivery guy that you really aren’t a sad, slovenly hermit who legit ordered an entire meat lover’s pie for yourself at 9 pm on a Friday. There must be a compelling evolutionary reason for this ruse.

And there is. Black saddled tobies are splendidly poisonous.

Tobies, like many members of the pufferfish clan (and the closely-related porcupinefish (Diodontidae)), embed their skin and organs with potent toxins, in particular saxitoxin and tetrodotoxin (TTX), the latter of which is a compound so aggressively neurotoxic that it has given puffers the fearsome reputation of being used to generate one of the most dangerous dishes in the world. These powerful poisons are an effective deterrent to becoming a much larger fish’s meal, and this, combined with the hallmark pufferfish capacity to inflate with seawater to several times their original size, makes black saddled tobies an unwise choice for a meal; if it doesn’t inflate in your throat and choke you, it’s bound to sicken or kill you following digestion. For this reason, most fish that share the waters with these tobies have either evolved to not see these fish as food, or have learned to avoid them through unsavory prior experiences. Black saddled tobies are an Untouchable caste on the reef, and this keeps them alive.

If you are small fish and you share an environment with a fish that predators won’t touch with a ten foot pole, being a copycat will end up having its benefits. This scenario, where a harmless species permanently cosplays as another harmful or distasteful species as a defense against a common predator, is a subtype of mimicry called “Batesian mimicry.” It is particularly well-known in insects, but it is also seen in this pair of fish; the filefish, without toxins of its own, exploits local predators’ aversion to small, white, diamond-shaped fish with black stripes and yellow tail fins by fitting this description to a tee. The filefish doesn’t actually need to be the coral reef equivalent of the ancient mystery Tupperware in the back of the office fridge that no one wants to eat, it just has to play the part. The blacksaddle filefish enhances this costume’s power even further by commonly shoaling alongside groups of its toby model. Some 5% of the fish making up aggregations of black saddled tobies are actually mimic filefish attempting to discreetly blend into the crowd.

As impressive as the mimicry is, there are still small ways to tell the two fish apart. The easiest way is to look at the dorsal and anal fins (the fins on the back and rear underside of the fish), which is actually a little surprising when you realize that both species have Saran wrap thin, transparent, hardly visible fins. In profile, you can see that the toby has narrow, oar-shaped fins, while the filefish has long, undulating fins that stretch a great deal down the back and along the underbelly. The ribbon-shaped fins of the mimic filefish are a component of its evolutionary legacy it hasn’t escaped in trying to imitate the black saddled toby. Another tell-tale sign that you are dealing with a filefish? A rigid dorsal spine, found in all filefish, that usually lays flat against the back to enhance the disguise, but when it is rarely erected, making the filefish look like a member of an undersea “Little Rascals”, it completely destroys the disguise like some kind of reverse version of Clark Kent’s glasses. There are some other minor hints as well, like how filefish generally have compressed, inflexible bodies shaped like an empty pita bread made out of leather, while tobies are a bit more like two Hershey Kisses fused together at their flat, wide ends. Of course, in profile view this diagnostic feature is nearly impossible to discern accurately. There’s also the presence of bluish stripes behind the eyes of adult male tobies, which are absent in their filefish mimics. If you think all these examples should make differentiation between the two fish easy as hell, give it a shot by watching the following video from The BlennyWatcher Blog; it’s not as easy as you’d think when the little bastards are all swimming around:

This model-mimic system is made more complicated when you realize there is potentially a second mimic trying to get in on the toxic toby action. Meet Plectropomus laevis, the blacksaddled coralgrouper, found throughout much of the tropical Indo-Pacific.

The fish above is a juvenile, and is only a few inches long (conveniently within the size range of a toby). Adults can be nearly four feet long, and as they age, their markings deviate further away from looking like the black saddled toby (more yellow on the fins and face, thicker black stripes, etc.). But, when these fish are young, they look very similar to Canthigaster valentini. It is possible that they, much like the mimic filefish, are also exploiting the toxicity of the model toby, and the fact that predators don’t mess with things that look like these tobies.

It’s also possible that there’s an additional benefit provided by this mimicry. Blacksaddle coralgroupers are voracious carnivores, and spend their days stalking and snapping up smaller fish into their wide, extendable maws. Juveniles of the species are no exception. Tobies, on the other hand, aren’t exactly the terrors of the deep, despite their toxic defenses. Tobies have an unintimidating tiny mouth and beak (made out of fused teeth) used to prune tiny crustaceans and other invertebrates from the surface of rocks and coral, and are basically a derpy turkey baster bulb with eyes. Juvenile blacksaddle coralgroupers could also be using their decorative deception as a means of looking less dangerous than they actually are…like nothing more than a harmless, omnivorous toby…allowing them to approach prey fish (however, as far as I know, no one has documented this being an observable factor in feeding behavior for the coralgrouper). This “wolf in sheep’s clothing” variety of mimicry is called “aggressive mimicry”; it is imitation with the purpose of lulling a target into a false sense of safety, only to have that target learn that it is not at all safe in an abrupt and dramatic fashion. Aggressive mimics aren’t actually cognitively aware of their own deceptiveness. Rather, their mimicry is the result of selection for behaviors and appearances that positively impact fitness. Their craftiness is not driven by an actual conscious plan, because this would require the mimic to fundamentally be aware of the presence of the mind of its prey (and to be able to anticipate how it will respond to external events), and this is a capacity known to occur in only a precious few of the planet’s most intelligent species of animals…and, here’s a clue, one is reading this blog post right now.

I should also directly note why I have said that the juvenile blacksaddle coralgrouper is “potentially” mimicking the tobies. Mimicry is particularly difficult to “prove,” largely because it’s hard to disentangle two co-occurring species that look alike because one has evolved to look like the other, from two co-occurring species that look alike out of coincidence. Specific coloration patterns, for example, have evolved many times over the course of life on Earth, mostly because they can serve specific functions unrelated to mimicry. When two co-occurring species look alike and are closely related to one another, it’s also possible that their close evolutionary juxtaposition is more at play than anything else. In the case of the tobies and the filefish, the argument for the filefish’s conspicuous similarity to the toby being more than a coincidence is significantly bolstered by two things: 1) the modification of the general filefish body plan to look specifically more toby-like (when color AND form converge in the same direction, that’s a pretty good indicator that something very directional is at play), and 2) the fact that these filefish regularly school with the saddle tobies, enhancing the quality of the mimicry greatly. Usually a combination of traits, like coloration, body shape, movement, and behavior…all appearing to mimic those of another species…boosts any argument for a clear case of the evolution of mimicry.

Being a copycat runs in the family for these filefish, as the only other member of the genus (Paraluteres), its closest relative, is also a mimic of a species of toby.

The top photo is of the model, Canthigaster margaritata, also known as the pearl toby. It is endemic to the rich coral reefs of the Red Sea (meaning it is found there and nowhere else). Below it is Paraluteres arqat, also a Red Sea endemic species of filefish, which appears to be a mimic of the pearl toby.

These examples of Batesian mimicry are fairly simple. A single model with one (or maybe two) mimic species. However, there are instances where a single model species is surrounded by a cloud of mimics, all independently donning the ocean’s version of a leather jacket and shades to look far more badass than they are actually are.

Let’s play a game. Below is a grid of four fish photos; one of them shows a model species, and the rest are mimics. Can you tell which one is the real deal and which ones are posers? And no, the answer is not “that housekeeper lady, Alice.”

This wasn’t a game you were supposed to win, because unless you are a fish nerd like me, you would have no way of answering that question. The fish in this image that all the others have, we think, evolved to emulate is the one in the upper left-hand corner.

What exactly is the name of this popular fish with all the die-hard fans copying his signature look? Say hello to Meiacanthus grammistes, the striped poison-fang blenny. They are found on sheltered coral reefs all across the Western Pacific, from Papua New Guinea/northern Australia and throughout the Indo-Malayan Archipelago, to the islands of western Micronesia and the Ryukyu chain near Japan. Blennies (fish of the suborder Blennioidei within the order Perciformes) in general are a varied group, ranging from gigantic kelp-forest forms, to diminutive forms that perch cautiously on coral heads, to things like the sarcastic fringehead, which has apparently decided that it’s Steven Tyler. Most blennies are a secretive and benign bunch, opting to park their elongated bodies on a rock or coral branch, or hide in a hole, trying to remain still to avoid detection by predators and patiently waiting for food to drift or walk by, often in the form of a small crustacean or fleck of plankton.

But the striped poison-fang blenny is not like most members of its family (the combtooth blennies, Blenniidae), and stays about as still and serene as an eight year-old stuck inside a library an hour after shotgunning one dozen Red Bulls. Meiacanthus blennies tend to be active swimmers, and dart around well above the reef bottom, doggedly protecting it’s turf from everything the general vicinity with all the confidence and righteous swagger of someone who just ran into their ex and saw just how unattractive they have become since the breakup. These torpedo-shaped, yipping “sea chihuahuas” may only grow to three inches long or less, so you’d think they’d be an easy little snack for a predator to snap up while passing through the neighborhood, especially considering how brightly colored so many species in this genus are (some of them look like they mush have shanked Jeff Bridges to flop out of the Grid and escape into the ocean, and others look a gas stove flame and brought it to life).

But they aren’t. In fact, predators won’t go anywhere near the angry little bolts of fishy lightning. It turns out those bright yellow markings and bold stripes on Meiacanthus grammistes aren’t just there to show how severely and fashionably punk rock these teeny hellions are, but primarily serve as a stern warning to the rest of the reef….a warning that says “I AM VENOMOUS AND I WILL BITE YOU. I WILL BITE ALL OF YOU.”

Yes, blennies in the genus Meiacanthus are collectively, and colorfully known as “poison-fang blennies” for the very real fact that they have a pair of enlarged, sharp canine-like teeth in their lower jaw that has a groove on its front side that is connected to a venom gland embedded in the jaw below. These fish, as far as I know, are the only fish in the world to have evolved a venomous bite; venomous stings, in contrast, have evolved in many groups of fish (scorpionfish, stingrays, rabbitfish, weevers, and stargazers just to name a few).

The biting action compresses the venom gland, sending venom up the groove in the curved fangs, and straight into the flesh of whatever decided it wanted to have a bad day that day. Poison-fang blennies only appear to bite other animals in its environment as a means of self-defense, or in defending its territory, not for acquiring prey. Poison-fang blennies are partial to plankton, mostly. While the venom doesn’t appear to be very effective on humans (outside of the pain of being stabbed with a pair of tiny, blood-drawing daggers when getting a bit too close when attempting to clean the aquarium), possibly due to huge difference in size (envenomation may be made difficult due to the small size of the fangs, comparatively, and the sheer size of a human body might dilute the effect of the dosage injected) it apparently does the trick against just about everything around it in its natural habitat…because nothing dares to touch it. On the reef, the poison-fang blenny definitely has a bad reputation, and much the same vein as Joan Jett, this fish really doesn’t give a damn about it.

This nasty reputation is ripe for exploitation by mimics, and this is why there are at least three different species, all from distinct evolutionary lineages, all converging on the same strategy of acting like the friendly neighborhood MMA fighter with terrifyingly unresolved anger issues. From an evolutionary standpoint of these mimics, the striped poison-fang blenny isn’t a belligerent, piscean d-bag with a butterfly knife, but a go-getter worthy of shamelessly plagiarizing, an idol of sorts, the Most Interesting Fish in the World….

The mimics are, counterclockwise from the upper left corner, Petroscirtes breviceps (a non-venomous species of fangblenny in the same family as Meiacanthus), a juvenile Scolopsis bilineatus (the two-lined monocle bream), and Cheiliodipterus nigrotaeniatus (a species of cardinalfish). The fangblenny is a close relative of Meiacanthus, but the monocle bream and the cardinalfish are both in different, distantly related families.

But it doesn’t just stop with this particular species of Meiacanthus, several other species of poison-fang blenny have “inspired” a cluster of satellite mimics…many of them also different species of monocle bream, fangblenny, and cardinalfish. Hell, the juveniles of Scolopsis bilineatus look differently in different parts of their geographic range, having evolved to mimic whatever resident species of poison-fang blenny has set up shop on the reef. Say what you want about the monocle bream potentially taking their inherent lack of originality overboard, but that’s some “loconomics”, community-minded, sustainably harvested shit right there.

This post series will continue: Part 2 will delve into the select few fish who not only pull off looking nothing like themselves, but nothing like any fish in the sea….

Image credits: intro image of toby-filefish pair, toby-filefish comparison: toby / filefish, Plectropomus laevis, Red Sea toby-filefish comparison: toby / filefish, grid image: mimic fangblenny / Meiacanthus grammistes / mimic monocle bream / mimic cardinalfish, Most Interesting Fish in the World modified from this photo by Klaus Steifel

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