A new and bizarre shape-shifting frog

Instead of going to church today, we can have our special Alain de Botton-Approved Religion Substitute by worshiping at the church of Our Lady of Natural History. There is in fact a wonderful new discovery about frogs, one described in a new paper in the Zoological Journal of the Linnaean Society by Juan Guayasamin et al. (reference and free link below; there’s also a precis in LiveScience).

I can state the results concisely: the authors found a new species of frog in Ecuador that can dramatically change its body shape from spiky to smooth in a matter of only a few minutes.  They then found another species, somewhat but not extremely closely related to the first, that can do the same thing. This kind of change in morphology, induced by the environment, is called phenotypic plasticity. And its observation in the frogs suggests two conclusions:

1. A lot more frogs can do this than have been described, but you need special conditions to see it, so it’s been largely undescribed. Other abilities of amphibians to change shape or color within a short time may also have been missed.

2. Since new frog species are often identified by their appearance after having been collected and pickled in alcohol, there may be described species that are identical to species with other names, but were misidentified because frogs collected at different stages of shape-changing could be mistaken for two different species. This is especially problematic because a large proportion of new species in both invertebrates and vertebrates (18% and 19%, respectively) are described from only a single specimen.

The paper gives other information as well, including genetic data, a phylogenetic analysis of the genus showing how the two shape-shifting species are related,  other genetic information about differences between populations, and a description of the frog’s call and morphology, important for describing it as a new species. But those issues are of more professional interest and need not detain us.

In amphibians, most variation among individuals of a species is in color, but those differences are permanent (like hair and skin color in humans) and don’t change over time. Those traits that do change over time in amphibian species, like crests in newts or tubercules in frogs, change during the breeding season, usually in males as a way to attract mates, and then revert back after the season. They thus change seasonally rather than over just a few minutes, like the frog described in this paper. The rapidity of change in the species is thus novel.

The new species, Pristimantis mutabilis (note the species name!), was first spotted in 2006 in the cloud forests of the Ecuadorian Andes, but its ability to change shape wasn’t detected until three years later. Under normal conditions the frog is spiky, with tubercules and points, but it changes when they’re picked up. As the authors describe in the paper:

All individuals of Prismantis mutabilis presented a markedly tubercular skin texture when found on vegetation or hidden in moss during the night. Large tubercles were evident on the dorsum, upper and lower lips, upper eyelid, arms and legs. After frogs were captured, they all showed a sudden and drastic change in skin texture; all tubercles became reduced in size, and the dorsal skin became smooth or nearly smooth (i.e., few tubercles are visible, mainly on the upper eyelid and heel). When frogs were returned to mossy, wet en- vironments, they recovered a tuberculate skin texture. We speculate that explanatory variables involved in frog skin texture change are stress, humidity, and back-ground. Our observations do not support light availability as a source of texture variation as we observed skin texture change at day and night. The time rate of skin texture variation might depend on the variables mentioned above; we only have one quantitative measure, which is summarized in Figure 2.

Here’s Figure 2: As you can see, the spiky frogs become relatively smooth within five minutes after capture. It’s not yet clear what physiological/biochemical systems are involved in this dramatic change:

Fig_xx_grandisonae_photos

Here are two more pictures of individuals changing:

In this photo, from Figure 3, a sub-adult male is first photographed in its natural habitat (A) and then in the laboratory (B). You can see the change very clearly:

Screen Shot 2015-03-29 at 8.28.26 AM

And here’s one more with the caption from the paper. These are small frogs, ranging in snout-vent length between 17 and 23 mm (0.7-0.9 inches):

Screen Shot 2015-03-28 at 8.35.04 AM

The authors also identified another species that does the same thing: a congener (frog in the same genus) named Prismantes sobetes. Since the two shape-shifting species are not closely related—a phylogeny shows many other species are more closely related to either than the two are to each other—either the ability to change body texture has evolved twice, or it’s present in some of the intervening species since it evolved in a common ancestor, or it is the remnant of a feature in their common ancestor that has been lost in all other species in the group. Since we don’t know about the abilities of those other species to shape-shift, more work is needed to distinguish among these explanations.

This leaves one big question: Why on earth do the frogs do this? Let’s assume as a working hypothesis that the shape change is an evolved one, and that individuals that could change shape had a selective advantage in the ancestral lineage. (It’s also possible that this is simply a nonadaptive physiological response to stress.) The authors suggest, probably correctly, that the tubercles and spiky appearance help camouflage the frog in the cloud forest, where it often sits among moss, vegetation, and epiphytes (plants growing on other plants); and they also raise one possibility for how they change their shape:

We suggest that skin plasticity is associated with environmental camouflage rather than sexual selection or dimorphism. Pristimantis mutabilis and P. sobetes are geographically distributed in montane cloud forest habitats that are abundant in epiphytes, vegetation, and moss. In these habitats, skin texture that has the appearance of moss or detritus likely conceals the individual from visual predators, such as birds and arachnids. While the physiological mechanisms of how texture changes in such a short time are unknown, we speculate that it could involve allocation of more or less water to existing small structures (e.g. warts and tubercles) on the skin.

But what’s missing here is an explanation for the change itself, which I can’t find in the paper. That is, why do they change from the presumably camouflaged shape to a smooth shape? And here I, who have no knowledge about amphibians, come up short. Perhaps being smooth helps you escape from predators if you’re caught, or helps the frogs jump better.  Experiments (some of them involving predation!) could help settle this.  I suspect some readers who know more about frogs than I (I’m looking at you, Lou Jost) can suggest evolutionary reasons why shape-shifting may be adaptive.  Please give your suggestions in the comments.

__________

Guayasmin, J. M. et al. 2015. Phenotypic plasticity raises questions for taxonomically important traits: a remarkable new Andean rainfrog (Pristimantis) with the ability to change skin texture.  Zool. J. Linnaean Soc. 173:913-928.

h/t: Barry

28 Comments

  1. Zwirko
    Posted March 29, 2015 at 10:02 am | Permalink

    Is a sun tan an example of phenotypic plasticity?

  2. Posted March 29, 2015 at 10:04 am | Permalink

    Wow, that’s amazing!!! We have very similar “spiky” new Pristimantis species in our reserves. Now we’ll have to check if they are shape-shifters. Juan Guayasamin is a friend and is the founding editor of a brand-new journal, Neotropical Biodiversity, so if any readers learn something more about this shape-shifting through experiments, they can submit their results there.

    I’ll make two speculations about the reasons for this. One, it is easier to grip a textured frog than a smooth slippery one, so stress might select for slipperiness; and two, maybe it takes metabolic work to make the spikes (ancestors were probably smooth) and under stress, all metabolic resources are needed for escape. But neither of these speculations seems particularly convincing to me. But they are testable.

    • W.Benson
      Posted March 29, 2015 at 12:59 pm | Permalink

      Lou, I like Jerry’s, Mark’s (see below), and your first adaptationist (just-so-story) hypothesis:
      Being smooth likely helps frogs “slip” away. I say that from experience, if not experiment.

  3. Diana MacPherson
    Posted March 29, 2015 at 10:05 am | Permalink

    Seems god has an affinity for frogs as well as beetles! Frogs are just amazing – they can hibernate and freeze up, they do crazy stuff with their skin, including poison enemies, they have pretty eyes and they are just so cute!

    • rickflick
      Posted March 29, 2015 at 10:12 am | Permalink

      Don’t forget – salamanders can regrow limbs. God can’t even do that.

      • Diana MacPherson
        Posted March 29, 2015 at 10:13 am | Permalink

        Yes, and lizards can regrow their tails and chameleons change their colours and those sticky feet of many geckos and frogs are fabulous!

      • Posted March 29, 2015 at 10:13 am | Permalink

        Yes he can–just not for other people!

        • Diana MacPherson
          Posted March 29, 2015 at 10:14 am | Permalink

          Careful, or you’re going to be accused of having a conception of god! 🙂

  4. Roel Wijtmans
    Posted March 29, 2015 at 10:49 am | Permalink

    That’s very interesting! Sure would be great to now why and how this works. Since it takes such a long time to change to smooth, I have a bit of a hard time believing this has to do with escaping predators, but you never know!

    I’ll put my money on camouflage, maybe the frog senses what the structure around it is and changes accordingly. It is, after all, sitting on smooth pieces of paper in the photos with smooth skin. Putting it on something with relief would be interesting.

  5. Mark Sturtevant
    Posted March 29, 2015 at 11:18 am | Permalink

    I recall some years ago you had a posting of a salamander whose ribs pierce its skin as a deterrent to predators. This seems a bit different, though, as it looks like the spikes here are to enhance camouflage in textured backgrounds.
    The smooth form might help them be more slippery. But how do they do it? Is is by muscles in the skin that raise and lower soft papillae? These little guys remind me of octopi that increase their skin texture for camo.

  6. marksolock
    Posted March 29, 2015 at 11:23 am | Permalink

    Reblogged this on Mark Solock Blog.

  7. Gregory Kusnick
    Posted March 29, 2015 at 12:18 pm | Permalink

    It seems a bit of a stretch to call this shape-shifting when it’s really just a change in skin texture. Heck, I can do that, and so can you, along with most mammals and birds.

    So now we know that amphibians can do it too (or something like it). That’s interesting, and I’m curious to know whether the mechanism by which they do it bears any resemblance to ours.

    • Posted March 29, 2015 at 1:01 pm | Permalink

      That’s related to the question I had in mind.

      What’s the actual physiology of the change? Is it in any way related to goosebumps?

      b&

  8. samphire53
    Posted March 29, 2015 at 5:27 pm | Permalink

    Could it be a ‘stealth’ camouflage which breaks up sunlight reflections from its skin?

  9. TJR
    Posted March 29, 2015 at 7:44 pm | Permalink

    They do it because god gave them free will.

  10. Shwell Thanksh
    Posted March 29, 2015 at 11:50 pm | Permalink

    Amphibian… hmmm. Something to do with the mossy structures being less adaptive for behaviors while in mud or water? That might justify rapid instead of seasonal shifting…

    • Shwell Thanksh
      Posted March 30, 2015 at 12:15 am | Permalink

      OK, on further reflection I’m refining this vague speculation to the specific possibility that the mossy tubercules look succulent enough to be nibbled on uncomfortably by other aquatic creatures… testable!

      • Posted March 30, 2015 at 9:56 am | Permalink

        Good guess, but these frogs are not aquatic. This genus doesn’t even have free-swimming tadpoles–the tadpoles develop into froglets inside the eggs. This independence from standing water has freed these frogs from a major life-history constraint, and resulted in the biggest evolutionary radiation of any vertebrate genus. There are 500++ species in this genus (all in the New World)!

        • Shwell Thanksh
          Posted March 31, 2015 at 2:29 pm | Permalink

          Thanks for the clarification. Good luck with your further experiments!

  11. livinginabox
    Posted March 30, 2015 at 3:26 am | Permalink

    Surely the smooth surface would be significantly hydrodynamically efficient (possibly aerodynamically different too, depending upon how much they spend in the air [rough surfaces can be good too (golf-ball roughness – dimples make the balls go further – although that needs rotation)]), whereas the spiky form is presumably significantly better from the point of view of camouflage / outline disruption – not looking frog-like or perhaps confusing to predators. Plus the ladies probably like it rough.
    Both states must presumably be worthwhile otherwise they wouldn’t change.

    • steve
      Posted March 30, 2015 at 5:05 am | Permalink

      Also bumpier is more surface area for skin evaporation which would be OK in a moist mossy environment plus its camouflage.
      But in a lab situation and on rocks in the forest the surfaces are smoother drier, so smooth surface provides camouflage and less surface area and therefore less evaporation from the skin.

      In other words it could be a two for one adaptation to humidity levels as well as camouflage.

  12. John Scanlon, FCD
    Posted March 30, 2015 at 7:24 am | Permalink

    I’m surprised to see this called ‘phenotypic plasticity’, which I first learned about in the context of hatchling skinks, incubated at different temperatures, having different body proportions, running speeds and thermal preferences: a matter of divergent ontogeny of the same genotype depending on environmental conditions. The Pristimantis trick is very different and seems to be well down a slippery slope from established usage: a matter of behaviour rather than development, and clearly reversible (which ontogeny normally isn’t). Can we call short-term colour shifts in lizards and fish ‘phenotypic plasticity’ now? Or think of the humble Porcupine Fish, one moment sleek, the next spiky. What about birds moulting feathers? What about any animal changing its position or orientation…?

    My initial guess for function is that the tubercular/smooth condition must make some difference to surface area, which could be used in response to changes in temperature and humidity. Seems too slow for the main function to be in predator escape.

  13. Andrew
    Posted March 30, 2015 at 8:54 am | Permalink

    How about surface area? By becoming smoother they keep their volume the same but reduce their surface area. By doing that, they dry out more slowly, a useful trait for an amphibian.

  14. Juan M. Guayasamin
    Posted March 30, 2015 at 10:06 am | Permalink

    We are already working in trying to understand the mechanisms underlying the skin texture change, which (I agree) is one of the most interesting questions that remains unsolved.

  15. Posted April 1, 2015 at 12:38 pm | Permalink

    Great post.


%d bloggers like this: