A caterpillar mimics an onycophoran

Here’s a weird case of mimicry—or potential mimicry—involving an onycophoran and a caterpillar in Ecuador. It’s in American Entomologist, and is free (click on screenshot below, or see the pdf here).

First, in case you don’t know what an onycophoran is, it’s a group of 177 known species that occupy a single phylum, the Onycophora, which means “claw bearer.” Also called “velvet worms,” they are weird-looking, like worms with claw-bearing legs on a segmented body, big antennae and small eyes. They look like this:

And they have a bizarre behavior, described in the paper like this:

Although closely related to the arthropods, onychophorans are so unusual in their form, differing significantly from all other extant animals, that the taxon has been ranked at the level of phylum (Nielsen 2012Grimaldi and Engel 2005). The Onychophora is unique due to the possession, by all species, of an elastohydrodynamic squirt-system in the mouth region. Remarkable structures, including glands that open on oral papillae, constitute a mechanism that enables onychophorans to squirt oscillating jets of proteinaceous liquid “slime” using slow muscular contraction (Concha et al. 2015). The slime rapidly fires from each papilla on either side of the mouth, intersects, and forms a disordered net (Morera-Brenes and Monge-Nájera 2010Concha et al. 2015). The slime solidifies on contact with air and entangles small invertebrate animals; prey items or potential predators are quickly immobilized. Onychophorans then use their large-toothed, sclerotized jaws (Mayer et al. 2015a) to penetrate the victim, introduce saliva containing digestive enzymes, and partially digest the soft tissue prior to ingestion by sucking. Prey tissue may also be sliced up by the jaws and then swallowed (Lawrence 1953Newlands and Ruhberg 1979Hamer et al. 1997).

Here’s a National Geographic video showing an onycophoran sliming and then nomming a beetle:

Their appearance once made people think that onycophorans were a “missing link” (or rather something close to the common ancestor) between arthropods and annelids (segmented worms), and they were described as “living fossils”. But now they’re thought to be a sister group to arthropods + tardigrades, and not that closely related to annelids. Here’s their current phylogenetic position.

 

The new paper describes what may be a case of Batesian mimicy between a caterpillar and an onycophoran.  The hypothesis is that a caterpillar which is tasty and preyed upon (birds, small mammals, reptiles, etc.) has evolved by natural selection to physically resemble an onycophoran, which is presumably avoided by predators because it has that nasty slime as well as teeth. If the predator has learned (or evolved) to avoid eating onycophorans, it may also avoid eating caterpillars who resemble them, thus giving a selective advantage to any caterpillar that closely resembles an onycophoran and thus can fool predators.

The authors found both onycophorans and caterpillars that resemble them in a collection of vegetation from trees in Ecuador (onycophorans are susceptible to desiccation and thus live in humid places in the tropics and wet subtropics). Here’s one of the tree-dwelling onycophorans and the presumably mimetic caterpillar. The paper’s caption is below, and be sure to watch the video at the link (I think they got “a” and “b” reversed in the figure caption, so I switched them).

Posterior view of the head of the caterpillar (B) found together with an onychophoran (A) in a sample of arboreal bryosphere. Note that the surface texture of the tubercles on the head of the caterpillar resembles the surface papillae of the onychophoran (see supplemental video 2 showing the entire caterpillar and onychophoran moving about in a lab set-up inside the field station).

A.

B. 

That seems to be a pretty close resemblance, as the caterpillar has that pair of protruding bits that look like onycophoran antennae, as well as the body papillae that look like those on onycophorans.  The caterpillars have no obvious defense that the authors could detect, and so they could be edible but avoided Batesian mimics of the onycophorans.

Now this is only a possible case of Batesian mimicry, though it looks suggestive to me.  What we’d need to know to reach stronger conclusions is this information:

a. The caterpillar and onycophoran are attacked by a common species of predator (or more than one species of predator).

b. The predator has learned to avoid killing the onycophoran when it gets close to it, since the beast is nasty.

c. The predator will eat the caterpillar if it is “naive”, that is, if it hasn’t encountered an onycophoran and so hasn’t learned to avoid them. (This wouldn’t work if the aversion to onycophorans is evolved rather than learned.)

This could easily be tested in the lab (well maybe not that easily!). Just give a naive, hand-reared predator an onycophoran. See if it tries to kill it but then is repulsed and avoids them afterwards. At the same time, give other naive predators the caterpillars. They should be nommed readily.  Then give a predator who has learned to avoid an onycophoran a “mimetic” caterpillar. If this is a case of mimicry based on predator learning, the predator should now avoid the caterpillar.

As it is, this is a suggestive but not well-documented case of mimicry, but it could be strengthened with some lab work.

 

h/t: Dom

33 Comments

  1. BJ
    Posted July 2, 2018 at 10:34 am | Permalink

    I’m more interested in those crazy mouth jet things. That’s remarkable. What an amazing way to capture and incapacitate other animals.

    • Jenny Haniver
      Posted July 2, 2018 at 11:58 am | Permalink

      “Those crazy mouth jet things.” Yeah.

      • BJ
        Posted July 2, 2018 at 1:54 pm | Permalink

        I don’t know how else to describe it, beyond the technical description given in the paper. In fact, I’m interested in how you would do it. You have quite a way with words.

    • Posted July 2, 2018 at 12:15 pm | Permalink

      Agreed. It is right up there with the Bombardier Beetle’s mixing chemicals to make a hot spray out its rear end. I can see a fun movie where giant ones of each species (the result of nuclear testing or DNA manipulation gone awry) battle it out with humans as collateral damage of course.

      • loren russell
        Posted July 2, 2018 at 1:00 pm | Permalink

        Best analogy is hagfish slimes, as seen entangling a Prius in this Oregon classic:

        • loren russell
          Posted July 2, 2018 at 1:01 pm | Permalink

          arggh, can’t get the URL into WordPress-ese.

          Just look up “slime eels car”

          • Posted July 2, 2018 at 3:10 pm | Permalink

            Uggh! I couldn’t watch but a few seconds. In the same vein, I remember when we had a root beer truck overturn on a local freeway and they called in the street sweeping machines which turned it into a lot of foam that drifted in the wind. They had to close the freeway for a while.

            • loren russell
              Posted July 2, 2018 at 10:13 pm | Permalink

              Topping Paul: There was the very hot summer afternoon of I-5 in south Tacoma. I found the right lane moving unusually fast. Unusual until I was caught in a mile-long spill cf cow entrails from a rendering-plant truck.. And no, no one let me back in the nearest unpolluted lane.

              • Posted July 3, 2018 at 10:19 am | Permalink

                Yuck! The poor people that live along that mile!

          • Diane G
            Posted July 3, 2018 at 1:26 pm | Permalink

            What a fantastic event! Thanks, loren!

      • BJ
        Posted July 2, 2018 at 1:56 pm | Permalink

        Holy shit. The only reason that hasn’t yet been made for the SyFy channel is the producers don’t know about these creatures!

        I’d like to see it made by a team of Bong Joon-Ho and Guillermo Del Toro.

        • Posted July 2, 2018 at 3:19 pm | Permalink

          Let’s talk to them! There are bound to be some good technical advisers among WEIT’s author and commenters.

          • BJ
            Posted July 2, 2018 at 4:17 pm | Permalink

            I can finally break into Hollywood with my script, Onychophorantopus Vs. Sharkodile.

            • Posted July 2, 2018 at 5:10 pm | Permalink

              How about “A Song of Fire and Slime”, with a not to Game of Thrones.

        • infiniteimprobabilit
          Posted July 2, 2018 at 8:46 pm | Permalink

          Giant oncyphorans or hagfish – which would be the most horrific? Please nobody tell Hollywood about them! Though I guess del Toro could make a convincing movie about them, monster movies have come a long way from the days of rubber monsters and cardboard props.

          (If that happened to my car I would be homicidal. Luckily it’s only a Prius…)

          cr

  2. Posted July 2, 2018 at 10:52 am | Permalink

    Very interesting.

  3. George
    Posted July 2, 2018 at 10:57 am | Permalink

    What is the difference between mimicry and camouflage? From all the “spot the …” posts, I assume that camouflage is more at a distance while mimicry is close up. And mimicry is more of hiding in plain sight while camouflage is just plain hiding.

    Now I am just thinking out loud and don’t really have a well formulated question.

    • Posted July 2, 2018 at 12:24 pm | Permalink

      The difference is a bit hair-splitty, but usually we think of camouflage as an animal (or plant) hiding itself by mimicking part of the environment, while mimicry, which need not involve hiding oneself, involves looking like another organism, usually to avoid predation. Mimics need not be camouflaged–Batesian mimics, for example, can be brightly colored to ape a toxic model species that is also brightly colored.

      • Posted July 2, 2018 at 12:36 pm | Permalink

        The variety of life is simply amazing! I imagine that there are actually some hair-splitting beetles out there somewhere. 😉

  4. Hempenstein
    Posted July 2, 2018 at 12:09 pm | Permalink

    So, in addition to the Creator, Onychophorans have a fondness for beetles.

    Meanwhile, is there any structural resemblance between spider silk spinerettes and the velvet worm slime cannons? Also, any amino acid sequence similarities between silk and the slime?

    • Hempenstein
      Posted July 3, 2018 at 6:44 am | Permalink

      OK, so I hadda look it up myself.

      Highly unstructured, proline rich proteins with high charged-residue content, unlike spider silk. Somewhere long ago I read that polyglutamic acid is an excellent underwater glue, so as that as a reference it seems entirely plausible that this slime protein makes an excellent sticky goo.

  5. Michael Hart
    Posted July 2, 2018 at 12:29 pm | Permalink

    Also reminiscent of this gem:

    https://whyevolutionistrue.wordpress.com/2009/09/04/worst-paper-of-the-year/

    • Posted July 2, 2018 at 11:33 pm | Permalink

      That connection came to me too. For readers who have forgotten, a crackpot biologist named Donald Williamson proposed that the larvae of butterflies originated from a hybridization event between an onychophoran and an insect. This is about as likely as hybridization between a goldfish and a porpoise. Williamson’s paper was pushed, by improper means, into Proceedings of the National Academy of Sciences by the late Lynn Margulis, a chronic contrarian. It later got partially pulled from PNAS after an uproar.

      The hypothesis was demolished by several papers, chief among them the paper by Hart and Grosberg (here). Yes, the Michael Hart to whom I am replying.

      Many thanks, Michael and Rick, for your decisive refutation of this outrageous nonsense.

  6. Posted July 2, 2018 at 12:32 pm | Permalink

    Another excuse to promote Richard Fortey’s brilliant Horseshoe Crabs and Velvet Worms. Read it!

    • Diane G
      Posted July 3, 2018 at 1:43 pm | Permalink

      Thanks for the suggestion–added to wish list.

  7. Posted July 2, 2018 at 12:50 pm | Permalink

    The video of the onycophoran sliming and then sucking the life out of the beetle was horrifying.

    • infiniteimprobabilit
      Posted July 2, 2018 at 8:52 pm | Permalink

      I didn’t watch it. I want to sleep tonight.

      (Add another line to the ‘God (the Creator) is a twisted sadomasochistic psychopath’ file, which is already several hundred pages long)

      cr

  8. loren russell
    Posted July 2, 2018 at 1:50 pm | Permalink

    Absent experimental work with naïve potential predators, we usually expect Batesian mimics to be noticeably divergent from their ancestral/outgroup with reference to the proposed mimetic features. [So, if arboreal/surface active onychophorans are geographically limited, we expect mimesis only within their range j[or perhaps where the model is recently extinct.

    Looking at this case, we don’t even know what family the caterpillar belongs to, so no information on any “premimetic” character state.

    Further, aside from the “horns” [which show up in a lot of larval lepidoptera, the dark coloration and papillate surface are pretty common in inverts living on the surface of rain-forest epiphytes [my experience in the Pacific Northwest coastal forests].

    Again, the onychophoran appears to be cryptic when at rest and rather rare [they note that nine specimens were recovered in their study]. So, less likely to be classic Batesian mimicry.

    Lovely beasts, but case not nearly proven.

    • een
      Posted July 2, 2018 at 6:38 pm | Permalink

      Yes, my first thought also was that the onychophorans would be rather too rare to be useful as a mimic. Here in NZ there are several species of onychophorans, but they aren’t common. Although I do remember a paper titled something like An Unusual Aggregation of Peripatus – which described exactly what it said in the title… Sad I can’t find it again for everyone’s delectation.

      Both the onychophoran and the caterpillar are cool little beasties though.

    • Diane G
      Posted July 3, 2018 at 1:48 pm | Permalink

      “… the dark coloration and papillate surface are pretty common in inverts living on the surface of rain-forest epiphytes …”

      A la Gloger’s Rule, though it’s supposed to apply only to endotherms.

  9. Christopher
    Posted July 2, 2018 at 2:28 pm | Permalink

    Arboreal Bryosphere. Never knew there was a term for that mossy tree environment. Very cool.

  10. Mark Sturtevant
    Posted July 2, 2018 at 5:55 pm | Permalink

    Very cool! But I would like to see a picture of the whole caterpillar.

  11. Mickey Mortimer
    Posted July 3, 2018 at 2:45 am | Permalink

    “Their appearance once made people think that onycophorans were a “missing link” (or rather something close to the common ancestor) between arthropods and annelids (segmented worms), and they were described as “living fossils”. But now they’re thought to be a sister group to arthropods + tardigrades, and not that closely related to annelids.”

    That’s really more of a consequence of nomenclature than a change in our phylogenetic hypothesis. The problem is that Onychophora has more recently been defined as monophyletic compared to tardigrades and arthropods, so that they cannot be the ancestor of arthropods. But in recent phylogenies (e.g. Smith and Caron, 2015), stem-tardigrades like Onychodictyon and stem-arthropods like Hadranax, Siberion and Megadictyon are basically onychophoran-grade organisms.

    It’s like how amphibians are now defined as monophyletic compared to amniotes, so that amphibians cannot be the ancestors of amniotes anymore. Yet taxa just outside the amphibian-amniote split (e.g. temnospondyls, anthracosaurs, seymouriamorphs in Marjanovic and Laurin, 2016- fig. 13) were considered amphibians before the cladistic revolution and are of ‘amphibian-grade’.

    References- Smith and Caron, 2015. Hallucigenia’s head and the pharyngeal armature of early ecdysozoans. Nature. 523(7558), 75-78.

    Marjanovic and Laurin, 2016. Reevaluation of the largest published morphological data matrix for phylogenetic analysis of Paleozoic limbed vertebrates. PeerJ Preprints. DOI 10.7287/peerj.preprints.1596v2


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