Field of Science

When Parsimony Goes Wrong: The Wings of Stick Insects

The stick insect Sipyloidea sipylus opening its wings. Photo by Drägüs.

One of the questions most commonly asked when looking at a phylogenetic tree is what that tree indicates about how the organisms on it evolved. What does it say about what their ancestors were like? What changes happened when? In answering those questions, the most commonly invoked tool is the principle of parsimony - in the absence of any reason to think otherwise, favour the explanation that is the most straightforward, and (in the case of inferring evolutionary history) requires the least number of changes. Parsimony is a popular tool because it's straightforward, relatively easy to apply, and it makes a great deal of intuitive sense - if a red animal occupies a deeply nested position in a clade of blue animals, then it seems fairly obvious that the ancestral animal was blue. However, like all analytical tools, the principle of parsimony is based on certain assumptions, and can be misleading if those assumptions are violated. Parsimony assumes that when comparing changes in a character between two states, change in either direction is equally likely. If, for whatever reason, a change is more likely to happen in one direction than another, then a parsimony analysis might be mislead about the ancestral condition. An elegant demonstration of this limitation of parsimony can be found in Collins et al. (1994) were the results were discussed of using parsimony to infer an ancestral DNA sequence (cytochrome b) for the marine gastropod genus Nucella. Nucella DNA is AT-rich (its base composition includes far more As and Ts than Gs and Cs). Inferring the ancestral sequence using parsimony implies an ancestor even more AT-rich than any of its descendants, despite the fact that the AT-bias remains fairly constant across all living members of the clade. Because GC bases are relatively uncommon for a given position, the parsimony analysis always tends to indicate them to be the derived state.

A few years ago, a paper appeared in Nature presenting a phylogenetic analysis of Phasmatida, stick insects or phasmids (Whiting et al., 2003). Phasmids include both winged and wingless taxa. In those taxa that do have wings, the forewings are greatly reduced and the hindwings are the functional pair. Whiting et al. (2003) found that the various winged phasmids were phylogenetically nested well within a series of wingless taxa. They therefore made the surprising suggestion that the common ancestor of living phasmids was wingless, and that those phasmids with wings had regained them secondarily.

Timema dorotheae, a member of the basalmost genus of Phasmatodea. Photo by David Maddison.

As remarkable as this may sound, it may not be impossible. Studies of embryonic development in animals have found that developmental regulatory genes often act in a hierarchical manner, so that a relatively small mutation in a gene acting on an early stage of development may have a significant effect on later stages of development. It has therefore been suggested that it might be possible for a given feature (such as wings in an insect) to be lost through a mutation causing that feature to start developing in the first place, without any change in the genes that shape how that feature develops once it starts. If the original regulatory gene was then to mutate back to its original condition in a later generation, the missing organ might spring back into its original position as if it had never left. It might be argued that the patterning genes rendered functionless by the original mutation might be suject to genetic drift, and degrade to useless pseudogenes that could not be reactivated even if the original mutation did revert, but Whiting et al. (2003) invoke another of the interesting features of developmental genetics - many genes are pleiotropic (involved in patterning different characters at once). For instance, insects use many of the same genes in patterning their legs as patterning their wings, so even if selective pressure to retain function for the one was removed, there still might be the need to retain function for the other.

While this may be theoretically possible in general, is it the case for phasmid wings in particular? Does the evidence offer strong support for regained wings in stick insects? Despite Whiting et al. (2003) being widely cited as a proven case of evolutionary regain of a complex character, I'm going to have to answer with a no, I don't think so. Stick insects are generally not highly mobile. Even those species that have fully functional wings fly only rarely. They are exactly the type of insect that one would expect to be prone to frequent flightlessness and wing loss. Whiting et al. (2003) themselves state at one point that a winged ancestor for crown phasmids became the most parsimonious reconstruction if wing loss was weighted as six times more likely than wing gain. This does not seem too unlikely a difference. Other potential evidence can be seen in the wings themselves. Whiting et al. argue that genes involved in wing development may have remained potentially functional if they were still being used for other organs. But how far can this argument be taken?

One of the most useful features in characterising insect wings is their venation. A generalised diagram of insect wing venation is given above, but different orders of insects have significantly different wing venation, enough so that relationships can be recognised for fossil insects known from wings alone. Comparisons between wing venation of different orders can also be very useful in establishing their relationships.

Wing venation of phasmids shares a number of distinctive characters with that of Orthoptera (grasshoppers and crickets). Both these orders have the forewings leathery, with the main veins running roughly parallel. It is the hindwings, however, that show the major similarities (Grimaldi & Engel, 2005). In both orders, the cubital veins (the veins marked Cu and in blue in the diagram above) don't run to a point low on the hind edge of the wing as they do in most orders, but instead run fairly straight out to near the distalmost tip of the hindwing. The veins in front of the cubitals, which enclose most of the wing space in other insect orders, are packed into the fairly small space between the cubitals and the front of the wings (this is the hardened part of the wing in the photo at the top of this post). Most of the hindwing in orthopterans and phasmids is composed of the anal fan, reasonably small in other insects but massively expanded in these orders. All veins in both wings are densely connected by numerous crossveins. The close relationship between phasmids and orthopterans suggested by these shared characters has also been supported by molecular analyses (Terry & Whiting, 2005), albeit with the inclusion of the webspinners, which have greatly simplified wings with a much-reduced venation. While pleiotropy might explain how wing-patterning genes remained functional overall, it is difficult to imagine how the form of the potential wings could have been maintained down to their very venation.

Worker of the army ant Eciton burchelli, with the reduced eyes visible. Photo by Alex Wild, via Ant Hill Wood.

For contrast, Alex Wild recently discussed a much better-supported case of character reversal. Army ants of the genus Eciton have functional eyes in the workers despite being descended from an eyeless ancestor. However, while other ants have eyes with well-marked facets and multiple ommatidia (lenses) like those of other insects, Eciton eyes are nowhere near as well organised. The separate ommatidia have become atrophied and fused together, so that unless examined at electron microscopic level they look like a single enlarged ommatidium. Eciton worker eyes resemble the eyes of other insects the way that a six-year-old child's drawing of a horse looks like a real horse. You can see that the idea's there, but the execution is still something of a shapeless blob. What makes this situation even more remarkable is that there can be no doubt that Eciton still possesses the genes for growing fully-formed eyes, because the winged males (which never lost their eyes in the first place) still have perfectly normal insect eyes.

While pleiotropic selection might preserve the overall position and maybe even shape of the wings, there seems little reason for it to preserve the fine detail. After all, there are countless different ways that wing veins could potentially be arranged to give similar shape and function - that's how venation can vary so much between orders in the first place. Even if loss and regain of wings in phasmids might seem the most parsimonious explanation, I just don't think that it is more convincing than the alternative suggestion that phasmids have a repeated bias towards wing loss.

Afterword: I had written all this before I found the commentary on Whiting et al. (2003) by Trueman et al. (2004), and the reply by Whiting & Whiting (2004). I'd recommend reading them.


Collins, T. M., P. H. Wimberger & G. J. P. Naylor. 1994. Compositional bias, character-state bias, and character-state reconstruction using parsimony. Systematic Biology 43 (4): 482-496.

Grimaldi, D., & M. S. Engel. 2005. Evolution of the Insects. Cambridge University Press: New York.

Terry, M. D., & M. F. Whiting. 2005. Mantophasmatodea and phylogeny of the lower neopterous insects. Cladistics 21: 240-257.

Whiting, M. F., S. Bradler & T. Maxwell. 2003. Loss and recovery of wings in stick insects. Nature 421: 264-267.


  1. if a red animal occupies a deeply nested position in a clade of blue animals, then it seems fairly obvious that the ancestral animal was red
    That's surely supposed to say "was blue".

  2. Quite right. I've corrected the offending sentence, and thank you very much for pointing it out to me.

  3. I remember being skeptical of recurrence when I read popularized descriptions of this research. Your summary and correlation of other work makes a strong case for skeptical of recurrence.

    To their credit, Whiting does point out that with an assumption of relative cost of 6:1, their tree does put a winged ancestor at the base. But the criticism that "They [Trueman] fail to specify, however, what cost ratio is acceptable or how this cost ratio is computed from their intuition" is a quibble. Whiting's arguments for lower cost ratios simply reflect heuristics like "all swans are white". While perhaps not intuitive, they are not really any better IMHO.

    I wonder how developmental studies on recurrence of eyes in blind cave fish reflect on this.

  4. Assuming that you are right in your summary, then surely this is a case in which parsimony of another kind, operating on gene expression, trumps parsimony of the standard phenotypic kind?

  5. One other, unreported problem with the Whiting et al paper is that some of their sampled "wingless" taxa at the base of the tree- while wingless themselves- come from groups that also have winged representatives, such that they ought to have been coded as polymorphic.

    Incidentally, the army ant photo is from; Ant Hill Wood was reproducing it from my site with permission.

  6. Multiple recurrence of flight within the Phasmatodea suggests strong selection pressures favoring such, a nonsensical conclusion given the fact that several of the lines that reacquired flight turned right around and lost it again. Which is it, selection for or selection against? It can't be both. I'm willing to entertain hexapods nested within crusties, and even my beloved tigers nested within carabids, but multiple flight recurrence in a group where so little value is placed on flight is a bit much to swallow.

    The whole thing reminds me of the man who wrote a math equation that proved nothing exists.


  7. I have a good feeling (yes, thats all it is at this point) that Wheeler et al. are correct. Isn't it possible that the whole sequencing for wings could be present in all taxa yet turned "on" or "off"? In that case it could be genetic drift that leads to the reemergence of wings rather than selection pressures. The reemergence of wings could be a more random event. Why it would have been retained after subsequently reemerging, I don't know.


  8. Alex - my apologies for the misattribution. I've added a link to your site underneath the photo. And if Whiting et al. have underestimated the number of winged clades in phasmids, that does rather undermine their thesis.

    Kai - I agree with you (contra Ted) that, if the scenario posited by Whiting et al. is correct, then the reappearance of wings could be a more or less random event. The problem is that while the genes are deactivated, genetic drift in the absence of stabilising selection would be expected to result in their varying fairly randomly. If so, then if wings did randomly reappear, one would expect them to do so with somewhat random morphology. This is not what we see, so there would need to be some explanation as to why the wing morphology remains conservative (so I suppose John is right - the most "parsimonious" explanation is perhaps not the most parsimonious after all). I can think of two possible conditions that might lead to this - (1) the genes remain active and so subject to stabilising selection for some other function, or (2) some strong selective pressure favours that wing morphology, so that even if the initial recurrent wing morphology varies, it converges back towards the shared morphology over time.

    As I said in the post (and with the realisation that I'm potentially making an argument from incredulity), while I can believe that pleiotropic selection might preserve the overall morphology, it seems to be stretching things to expect it to maintain the fine detail. Also, when a biological feature is serving two functions, there is often a selective conflict that results in the organism evolving towards a median that is best overall but not quite optimal for each function taken alone (like what has been suggested for the Irish elk - antler size increases faster than body size, so selection for larger body size is retarded to a certain extent by selection against the antlers becoming too huge). If that is the case, then one would expect the removal of one function to be followed by a rapid period of directional selection as evolution is able to re-optimise towards the other function. If so, then pleiotropic selection might actually work against maintaining inactive functions.

    The other possible explanation, canalising selection, is also unconvincing. As referred to in the post, different orders of insects are able to achieve broadly similar wing morphologies through different combinations of more specific characters (for instance, Drosophila subobscura populations in Europe and North America have independently evolved larger wings overall in the northern parts of the populations, but its a different part of the wing that has actually enlarged in each case). So even if there is significant selective pressure for a specific overall morphology, there doesn't seem to be much reason for selection for specific fine details.

    Which I wonder if it relates to Mike's point about eye recurrence in cave fish, because with eyes there might be more selective pressure towards a specific morphology once the character reappears.

  9. Christopher, this doesn't have anything to do with your insect wings post, but I wanted to thank you for your comment on my giant sea spider. I've amended my post. I always need correction.

  10. Chris, do the papers you mention in the Afterword change anything in your opinion overall?

    For how long did insects have wings before the stick insects lost them? I'm imagining genes (and gene fragments) necessary for wing development also being involved in many other developmental pathways, not just one other, which it seems to me would add a tendency to conserve details. The older the character, the more interdependent become the genes for it and other characters. No?

  11. The two papers mentioned at the end don't really change my opinion over all - what they do do is give a better discussion of the statistical supports in the original paper. I have to admit, I'm not that great at statistics, so I'm happy to defer to those more knowledgeable in appraising them.

    As I've already noted, the amount of time that insects had wings before phasmids lost them isn't really relevant here, because the question is the detailed patterning of the wings more than the overall wing form itself. If the distinct shared features of orthopterans and phasmids such as the far distally-directed cubital vein and the massively expanded anal fan are homologous (which is not certain, but is still a viable hypothesis*), then the divergence of these two orders rather post-dates the origin of wings.

    (The nuisance factor here is the presence of Embioptera in the clade including Orthoptera and Phasmatodea, and Embioptera rather than Orthoptera are the closest relatives of Phasmatodea. Embioptera don't share the wing characters of the other two orders. Unfortunately, Embioptera have a terrible fossil record, and it is an open question at present whether the reduced wing venation of Embioptera is derived from an ancestor with more orthopteroid venation, or whether the Orthoptera and Phasmatodea derived their wing venations separately from a more simple-veined ancestor.)

    I don't necessarily see the case for older characters necessarily being connected with more tightly interconnected genes - after all, I believe there are also many cases of once pleiotropic functions of a single gene becoming divided between multiple genes. However, I have my suspicions that there is a vast insufficiency of research into how pleiotropy works and evolves.

  12. As an aside, the venation may serve to maximize stiffness-to-weight ratio, and so I would expect the pattern to be correlated with mechanism of flight (e.g. flapping forward flight vs. hoverability) and maybe to location of center of mass of the insect, for example. According to "mechanical parsimony" the material should not grow/be deposited requisite (but that is assuming that natural systems are always optimised). Did anyone study such beyond observations of D'arcy Thompson?

  13. Hi sorry to dig up an old thread but did you see this:

    Stone and French
    Evolution: Have Wings Come, Gone and Come Again?
    Current Biology. Volume 13, Issue 11, 27 May 2003, Pages R436-R438

    with regard to Whiting et al.

    They showed that the same facts could be interpreted without the need for re-evolving wings at all.

    Thought you might like, sorry.

    -a random stranger :)-


Markup Key:
- <b>bold</b> = bold
- <i>italic</i> = italic
- <a href="">FoS</a> = FoS