Bacillus rossius, photographed by Lucarelli.

Belongs within: Holophasmatodea.
Contains: Platycraninae, Lonchodinae, Diapheromerinae, Cladomorphinae, Pachymorphinae, Eurycanthinae, Phylliinae, Necrosciinae, Tropidoderinae, Phasmatinae, Pseudophasmatidae.

The Phasmatodea, phasmids, include the stick insects and leaf insects. The bodies of these slow-moving plant-eating insects are modified to resemble the surrounding vegetation, providing them with excellent camouflage. The relatively short-bodied genus Timema, found in the western United States, is identified as the sister taxon to the remaining living Phasmatodea by its retention of several plesiomorphic features, including separate prothoracic ana- and coxopleurites, and prothoracic sternal apophyses (Grimaldi & Engel 2005).

When parsimony goes wrong: the wings of stick insects
Published 19 December 2008
The stick insect Sipyloidea sipylus opening its wings, photographed 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, photographed 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.

Systematics of Phasmatodea

Synapomorphies (from Grimaldi & Engel 2005): Prothorax bearing anterior dorsolateral defensive glands; males with vomer (modified sclerite on tenth sternite allowing male to clasp female during copulation); eggs with operculum (lid-like section of oocyte).

<==Phasmatodea [Areolatae, Cheleutoptera, Phasmatoidea, Phasmida, Phasmoptera]
    |--Timema [Timematidae, Timematinae, Timematodea, Timemidae, Timeminae]WBR07
    |    |--T. californicaR00
    |    |--T. christinaeBB16
    |    `--T. knuliiWBM03
    `--Euphasmatodea [Anareolatae, Bacillidae, Diapheromeridae, Phasmatidae, Verophasmatodea]WBR07
         |  i. s.: KorinninaeWBM03
         |         AschiphasmatoideaZ04
         |           |  i. s.: AschiphasmatinaeWBM03
         |           `--PrisopodidaeZ04
         |         PygirhynchinaeWBM03
         |         PlatycraninaeBH07
         |         Palophus Westwood 1859Z01b [PalophinaeWBM03]
         |         ArchipseudophasmatidaeWBR07
         |         Clarias brachysoma (Sharp 1898)WBR07
         |         LonchodinaeBH07
            |  `--+--PachymorphinaeWBM03
            |     `--+--Medauroidea extradentatumWBM03
            |        `--MedauraWBM03
            `--+--Bacillus [Bacillinae]WBM03
               |    |--B. geisovii Kaup 1866K66
               |    |--B. gerhardii Kaup 1866K66
               |    |--B. hookeriK66
               |    |--B. libanicusRD77
               |    |--B. lobipes Lucas 1846E12
               |    `--B. rossiusWBM03
                  |  `--CarausiusWBM03
                  |       |--C. excelsus Brunner 1907BH07
                  |       |--C. immundus Brunner 1907BH07
                  |       `--C. morosusWBM03
                  `--+--Phylliidae [Phyllidae]R96
                     |    |  i. s.: ClonopsisRD77
                     |    |--PhylliinaeWBM03
                     |    `--+--Neohirasea maerensWBM03
                     |       `--NecrosciinaeWBM03
                     `--+--+--Phobaeticus heusiiWBM03
                        |  `--+--+--TropidoderinaeWBM03
                        |     |  `--PhasmatinaeWBM03
                        |     `--XeroderinaeWBM03
                        |          |--Dimorphodes prostasisWBM03
                        |          |--Xeroderus Gray 1835 [incl. Cooktownia Sjöstedt 1918]BH07
                        |          |    `--X. kirbii Gray 1835 [incl. Cooktownia plana Sjöstedt 1918]BH07
                        |          `--Cnipsus Redtenbacher 1908Z01a
                        |               `--*C. rachis (Saussure 1868) [=Acanthoderus rachis]Z01a
                           |    |--+--Aretaon asperrimusWBM03
                           |    |  `--Sungaya inexpectataWBM03
                           |    `--+--Agathemera [Agathemeridae, Agathemerodea]WBM03
                           |       |    `--A. crassaWBM03
                           |       `--+--Heteropteryx dilatataWBM03
                           |          `--HaaniellaWBM03
                           |               |--H. dehaaniiWBM03
                           |               `--H. grayii Westwood 1859 [incl. Heteropteryx australis Kirby 1896]BH07
                                `--Heteronemiidae [Heteronemiinae]Z04
                                     |--Canuleius [Canuleiini]Z04
                                     |--Heteronemia Gray 1835Z01 [incl. Bacunculus Burmeister 1838 Z01; HeteronemiiniZ04]
                                     |    `--*H. mexicana Gray 1835 [incl. *Bacunculus spatulatus Burmeister 1838]Z01b
                                          |--Xiphophasma Rehn 1913Z04
                                          |--Parabacillus Caudell 1903Z04
                                          `--Paraleptynia Caudell 1904 [incl. Steleoxiphus Rehn 1907]Z04
                                               |--*P. forsteri Caudell 1904Z04
                                               `--*Steleoxiphus’ catastates Rehn 1907Z04
Phasmatodea incertae sedis:
  Pharnacia kirbyiGE05
    |--P. gracilipes Pictet in Berendt 1856P92
    `--P. lineata Pictet in Berendt 1856P92
    |--C. hookeriWFS04
    `--C. laeviusculusRD77
  Argosarchus horridusDGH93
  Anasceles Redtenbacher 1908BH07
    |--D. brevitarsis Redtenbacher 1908BH07
    `--D. vicinissima Redtenbacher 1908BH07
  Bactrododema hecticum (Lichtenstein 1796) [incl. Ctenomorpha haworthii Gray 1835]BH07
  Ophicrania striaticollis Kaup 1871BH07
  Entoria Stål 1875Z04
  Cuniculina impigra (Brunner 1907)P11
  Dixippus morosusR13
  Acanthoxyla prasinaRD77

*Type species of generic name indicated


[BB16] Bai, M., R. G. Beutel, K.-D. Klass, W. Zhang, X. Yang & B. Wipfler. 2016. Alienoptera—a new insect order in the roach-mantodean twilight zone. Gondwana Research 39: 317–326.

[BH07] Brock, P. D., & J. W. Hasenpusch. 2007. Studies on the Australian stick insects (Phasmida), including a checklist of species and bibliography. Zootaxa 1570: 1–81.

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.

[DGH93] Daugherty, C. H., G. W. Gibbs & R. A. Hitchmough. 1993. Mega-island or micro-continent? New Zealand and its fauna. Trends in Ecology and Evolution 8 (12): 437–442.

[E12] Evenhuis, N. L. 2012. Publication and dating of the Exploration Scientifique de l’Algérie: Histoire Naturelle des Animaux Articulés (1846–1849) by Pierre Hippolyte Lucas. Zootaxa 3448: 1–61.

[GE05] Grimaldi, D., & M. S. Engel. 2005. Evolution of the Insects. Cambridge University Press: New York.

[K66] Kaup, J. 1866. Description of two new species of the genus Bacillus, Latr. Proceedings of the Zoological Society of London 1866: 577–578.

[P92] Poinar, G. O., Jr. 1992. Life in Amber. Stanford University Press: Stanford.

[P11] Pollard, S. D. 2011. A twitch in time: tibial spiracles have a role in an autonomous defence mechanism in harvestmen. Records of the Canterbury Museum 25: 59–65.

[R96] Rentz, D. 1996. Grasshopper Country: The abundant orthopteroid insects of Australia. University of New South Wales Press: Sydney.

[R13] Reuter, O. M. 1913. Lebensgewohnheiten und Instinkte der Insekten bis zum Erwachen der sozialen Instinkte. R. Friedländer & Sohn: Berlin.

[RD77] Richards, O. W., & R. G. Davies. 1977. Imms’ General Textbook of Entomology 10th ed. vol. 2. Classification and Biology. Chapman and Hall: London.

[R00] Ross, E. S. 2000. Embia: Contributions to the biosystematics of the insect order Embiidina. Occasional Papers of the California Academy of Sciences 149: 1–53, 1–36.

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

[WBR07] Wedmann, S., S. Bradler & J. Rust. 2007. The first fossil leaf insect: 47 million years of specialized cryptic morphology and behavior. Proceedings of the National Academy of Sciences of the USA 104 (2): 565–569.

[WBM03] Whiting, M. F., S. Bradler & T. Maxwell. 2003. Loss and recovery of wings in stick insects. Nature 421: 264–267.

[WFS04] Winks, C. J., S. V. Fowler & L. A. Smith. 2004. Invertebrate fauna of boneseed, Chrysanthemoides monilifera ssp. monilifera (L.) T. Norl. (Asteraceae: Calenduleae), an invasive weed in New Zealand. New Zealand Entomologist 27: 61–72.

[Z01a] Zompro, O. 2001a. A review of Eurycanthinae: Eurycanthini, with a key to genera, notes on the subfamily and designation of type species. Phasmid Studies 10 (1): 19–23.

[Z01b] Zompro, O. 2001b. A generic revision of the insect order Phasmatodea: the New World genera of the stick insect subfamily Diapheromeridae: Diapheromerinae = Heteronemiidae: Heteronemiinae sensu Bradley & Galil, 1977. Revue Suisse de Zoologie 108 (1): 189–255.

[Z04] Zompro, O. 2004. A key to the stick-insect genera of the ‘Anareolatae’ of the New World, with descriptions of several new taxa (Insecta: Phasmatodea). Studies on Neotropical Fauna and Environment 39 (2): 133–144.

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