Protura

Belongs within: Panhexapoda.

The Protura are minute soil-dwelling hexapods characterised by the absence of antennae, with the first pair of legs modified as sensory organs.

(Possibly) the world’s smallest tetrapods

Published 11 July 2007

The subject of today’s post are proturans. Proturans are rather unique little hexapods (though not, by the currently used definition, insects) that are apparently widespread despite being rarely seen (Imadaté 1991). I have to confess that I’ve never seen one yet in my time in entomology—I was reminded of them because one of my co-workers briefly thought he might have found one (but alas, not to be—it was probably some form of beetle larva). The title for the section derives from the fact that, despite being hexapods, proturans are functionally quadrapedal. They lack antennae, and instead the first pair of legs is held up and in front of the body as sensory organs.

Protura show a number of other unique features as well. They are the only insects to increase the number of abdominal segments over their life. And perhaps most notable of all, their spermatozoa are completely unlike any other hexapod (Baccetti et al. 1973). The proturan spermatozoon is non-motile, varying from a complicated twisted helical structure (Acerentulus traegardhi and Acerentomon majus) to a simple mammalian-blood-cell-like torus (Eosentemon transitorium). In those species that retain an axoneme (the flagellar ‘skeleton’) it shows an abnormal arrangement of microtubules. In the vast majority of eukaryotes, the axoneme has a ‘9 + 2’ arrangement – nine pairs of microtubules around the outside and two single microtubules in the centre (this is also the same arrangement as in spirochaetes, a clade of spiral bacteria, which has lead to rather controversial suggestions that the eukaryote flagellum may be derived from symbiotic spirochaetes – a suggestion I happen to be rather skeptical of). In contrast, proturan axonemes show a whole range of arrangements – 12 + 0, 13 + 0, 14 + 0 or even 9 + 9 + 2. Such unique features have lead to suggestions that proturans may not even be related to insects (there was an article in Simonetta & Conway Morris, 1991, that I recall, but I haven’t been able to find the specific reference), but as they are undoubtedly unique derived features of proturans they are completely uniformative as to outside relationships.

In terms of actual phylogenetic relationships, proturans are entognathous (that is, the mouthparts are recessed into a capsule under the head). Most authors have united them with the Collembola (springtails) in a clade called Ellipura, but most of the supposed characters of this clade reflect character losses, which are generally regarded as less trustworthy due to the higher chance of homoplasy. A couple of recent papers did not support the Ellipura grouping (Giribet et al. 2004; Luan et al. 2005), instead placing Protura with Diplura, but the former paper also found an unexpected polyphyletic arrangement of hexapods relative to crustaceans which requires further investigation.

Systematics of Protura

Characters (from Imadaté 1991): Very small, entognathous hexapods, mostly unpigmented; antennae absent; legs 5-segmented, fore leg modified for sensory purposes; abdomen 12-segmented in adult, with appendages on segments 1–3; cerci absent. Ovaries meroistic; spermatozoa non-motile. Juvenile development anamorphic.

<==Protura [Acerentomida, Myrientomata]
    |  i. s.: Protapteron [Protapteridae]W39
    |           `--P. indicumW39
    |--EosentomoideaI91
    |    |--SinentomonRD77 [SinentomidaeI91]
    |    |    `--S. erythranumRD77
    |    `--EosentomidaeI91
    |         |--StyletoentomonCI90
    |         |--AntelientomonI91
    |         |--IsoentomonI91
    |         |    |--I. pseudosaharenseI91
    |         |    `--I. serinus Szeptycki 2004F05
    |         `--Eosentomon Berlese 1910W39
    |              |--E. australicum Womersley 1939I91, W39 [=E. millsi var. australicaW39]
    |              |--E. canarinum Szeptycki 2004F05
    |              |--E. millsi Womersley 1939W39
    |              |--E. oceaniaeI91
    |              |--E. swani Womersley 1932W39
    |              |--E. transitorium [incl. E. armatum]RD77
    |              |--E. westraliense Womersley 1932W39
    |              `--E. womersleyiI91
    `--AcerentomoideaI91
         |--Protentomidae [Fujientomidae, Hesperentomidae, Meroentominae, Protentominae, Proturentominae]I91
         |    |--HesperentomonCI90
         |    |--ProtentomonI91 [incl. MeroentomonW39]
         |    |--NeocondeellumCI90
         |    |--HuhentomonI91
         |    |--ProturentomonCI90 [incl. ParaentomonW39]
         |    |    `--P. minimumCI90
         |    `--CondeellumCI90
         `--Acerentomidae [Acerellidae, Acerentominae, Berberentomidae]I91
              |--FjellbergellaCI90
              |--TuxenentulusCI90
              |--ProacerellaCI90
              |--Gracilentulus gracilisI91
              |--Berberentulus capensisI91
              |--VesiculentomonCI90
              |--YamatentomonCI90
              |--FilientomonCI90
              |--NipponentomonCI90
              |--Verrucoentomon canadense (Tuxen 1955) [=Acerella canadensis, Nosekiella canadensis]CI90
              |--AlaskaentomonCI90
              |--Paracerella Imadaté 1980CI90
              |--MicroentomonW39
              |--Australentulus tillyardiI91
              |--Tasmanentulus tasmanicusI91
              |--BaculentulusI91
              |    |--B. pseudonitidusI91
              |    `--B. tianmushanensisMG06
              |--Acerentomon Silvestri 1907W39
              |    |--*A. doderoi Silvestri 1907W39
              |    `--A. majusBDF73
              |--AmphientulusI91
              |    |--A. alienusI91
              |    `--A. ambiguusI91
              `--AcerentulusI91 [incl. AcerentuloidesW39]
                   |--A. australiensis Womersley 1932W39
                   |--A. confinusRD77
                   |--A. danicus [=Acerella danica]RD77
                   |--A. occidentalis Womersley 1932W39
                   |--A. sexspinatus Womersley 1936W39
                   |--A. tiarneusRD77
                   |--A. tillyardi Womersley 1932W39
                   |--A. traegardhiBDF73
                   `--A. westraliensis Womersley 1932W39

*Type species of generic name indicated

References

[BDF73] Baccetti, B., R. Dallai & B. Fratello. 1973. The spermatozoon of Arthropoda. XXII. The ’12+0′, ’14+0′ or aflagellate sperm of Protura. Journal of Cell Science 13: 321–335.

[CI90] Copeland, T. P., & G. Imadaté. 1990. Insecta: Protura. In: Dindal, D. L. (ed.) Soil Biology Guide pp. 911–933. John Wiley & Sones: New York.

[F05] Fernández, J. 2005. Noticia de nuevos táxones para la ciencia en el ámbito Íbero-Balear y Macaronésico. Nuevos táxones animales descritos en la península Ibérica y Macaronesia desde 1994 (IX). Graellsia 61 (2): 261–282.

Giribet, G., G. D. Edgecombe, J. M. Carpenter, C. A. D’Haese & W. C. Wheeler. 2004. Is Ellipura monophyletic? A combined analysis of basal hexapod relationships with emphasis on the origin of insects. Organisms, Diversity and Evolution 4: 319–340.

[I91] Imadaté, G. 1991. Protura. In: CSIRO. The Insects of Australia: A textbook for students and research workers 2^nd ed. vol. 1 pp. 265–268. Melbourne University Press: Carlton (Victoria).

Luan, Y.-X., J. M. Mallatt, R. D. Xie, Y.-M. Yang & W.-Y. Yin. 2005. The phylogenetic positions of three basal-hexapod groups (Protura, Diplura, and Collembola) based on ribosomal RNA gene sequences. Molecular Biology and Evolution 22: 1579–1592.

[MG06] Mallatt, J., & G. Giribet. 2006. Further use of nearly complete 28S and 18S rRNA genes to classify Ecdysozoa: 37 more arthropods and a kinorhynch. Molecular Phylogenetics and Evolution 40: 772–794.

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

[W39] Womersley, H. 1939. Primitive Insects of South Australia: Silverfish, springtails, and their allies. South Australian Branch of the British Science Guild: Adelaide.