Homeotic transformation in a centipede.

The suggested involvement of homeotic mutations in evolution1xHomeotic mutatants and evolution. Goldschmidt, R. Acta Biotheoretica. 1952; 10: 87–104Crossref | Scopus (15)See all References1 is controversial, and is rejected by most evolutionary biologists. However, an acknowledged difficulty is that these mutations are best known in Drosophila, which is a highly derived arthropod. Perhaps the severe fitness depression accompanying homeotic transformation would have been less pronounced, even absent, in a primitive arthropod with many similar segments. Centipedes provide a model for studying the effects of homeotic transformation as they might have been manifested in an ancient arthropod stem species. This is not to say that their particular body plan is not highly derived – it clearly is – but, rather, that it retains the feature of many broadly similar segments that characterized the first arthropods. The key question, then, is whether homeotic transformation in a system of this kind would be radically different in effect to its Drosophila counterpart.Despite more than a century of study of the morphology of centipedes, and the existence of at least 3000 species, there has until now been no observed case of homeotic transformation of a segment in any centipede. However, we have recently found a case of this in an adult male Strigamia maritima – a geophilomorph species of intermediate length – collected at Whitburn on the coast of NE England (grid ref. NZ 412615). This specimen (see Fig. 1Fig. 1) exhibits transformation of the most anterior of the normally legless terminal segments (the ‘intermediate’ segment) into a repeat of the posteriormost leg-bearing segment, giving it two pairs of specialized rear legs (male sexual characters) instead of one. This makes it the first centipede ever discovered with an even number of leg-bearing segments (48; normally only uneven numbers between 15 and 191 are observed).FIGURE 1Homeotic transformation in a centipede. (a) Normal and (b) transformed morphologies of the centipede Strigamia maritima. In the normal arrangement, there is a single segment with multiple coxal pores and with special rearward-pointing legs that are swollen in the male (pictured) but slender in the female. In the mutant centipede there are two such segments, the second deriving from the transformation of the normally legless ‘intermediate segment’.View Large Image | Download PowerPoint SlideThe symmetry of the transformed segment suggests a hereditary origin, perhaps involving a mutation of the Abdominal-B gene. [A homologue of this Drosophila gene was detected in one recent centipede study (M.L. Smith, PhD thesis, University of Cambridge, 1998) but not in another2xEvolution of the entire arthropod Hox gene set predated the origin and radiation of the onychophoran/arthropod clade. Grenier, J.K. et al. Curr. Biol. 1997; 7: 547–553Abstract | Full Text | Full Text PDF | PubMedSee all References2.] The mutant individual was viable under natural conditions: it had reached adulthood, and so must have been at least two years old3xThe life history and ecology of the littoral centipede Strigamia (= Scolioplanes) maritima (Leach). Lewis, J.G.E. Proc. Zool. Soc. London. 1961; 137: 221–248CrossrefSee all References3. Its fertility is unknown, although the genital segments, immediately posterior to the transformed one, appear normal. Although these observations appear to argue for an evolutionary role of homeotic mutation in this kind of body plan, there is a more pressing counter-argument. The homeotic centipede shares with the four-winged fly a morphological shift that appears never to have happened in evolution. Relative to the realized direction of evolutionary change, homeotic transformations seem to be always either ‘backwards’ (two-wings-to-four as opposed to four-wings-to-two) or ‘dead-ends’ (our centipede). So, even if the fitness problem is overcome, morphology itself argues against an evolutionary role for these mutations. However, in a final twist to the story, there is now evidence4xA role of Ultrabithorax in morphological differences between Drosophila species. Stern, D.L. Nature. 1998; 396: 463–466Crossref | PubMed | Scopus (174)See all References, 5xHox genes, homeosis and the evolution of segment identity: no need for hopeless monsters. Akam, M. Int. J. Dev. Biol. 1998; 42: 445–451PubMedSee all References that other (lesser) mutations of the Hox genes are involved in arthropod morphological evolution.