(Possibly) The World's Smallest Tetrapods

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 post 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. Christopher Tipping has a page with some neat pictures - in particular, check out the 1907 drawing at the top of the page like something on the cover of an Edgar Rice Burroughs book.

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.

REFERENCES

Baccetti, B., R. Dallai & B. Fratello. 1973. The spermatozoon of Arthropoda. XXII. The '12+0', '14+0' or aflagellate sperm of Protura. J. Cell Sci. 13: 321-335.

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.

Imadaté, G. 1991. Protura. In The Insects of Australia (CSIRO) pp. 265-268. Melbourne University Press.

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.