Sequences lead to tree of worms

Nematode worms are found just about everywhere, often in enormous numbers. Parasitic species live in almost all animals and plants, and only arid soils and the open oceans seem to be unsuitable for free-living species. Yet only about 15,000 species have been formally described, and some textbooks treat nematodes as one of the ‘minor phyla’. In spite of this, it is now believed that the number of living species should be counted by the million. Classification has been difficult because most of the species are small to microscopic in size, and they lack obvious distinguishing characteristics. But the first attempt at a phylogenetic classification — based on small-subunit ribosomal DNA sequences from 53 species — is presented by Blaxter et al. on page 71 of this issue¹. And, according to their findings, only one of the two classes of nematode that are recognized in the traditional classification is natural, consisting of an ancestral species and all its descendants.

Free-living nematodes are found in terrestrial soils and marine sediments, where they decompose plant and animal material. Parasitic species of nematode infect common crops such as potatoes, soya beans and corn, as well as livestock, including pigs, cattle and chicken. Human parasites include species that cause crippling or fatal diseases such as filariasis (elephantiasis), trichinosis and hookworm disease. Conversely, parasitic species of nematode are increasingly being used in biological control — some species directly attack and destroy the larvae or adults of plant parasitic insects, whereas others transmit bacteria that destroy the parasite (Fig. 1).

Figure 1

NIGEL CATTLIN/HOLT STUDIOS

The good — Steinernema bibionis, a free-swimming parasitic nematode used for biological control of vine weevil.

Most (but not all) nematodes are small and nondescript. For example, Placentonema gigantissima, which lives as a parasite in the placenta of sperm whales, grows to a length of 8 m, with a diameter of 2.5 cm. The free-living, marine Draconema has elongate adhesive organs on the head and along the tail, and moves like a caterpillar. But the general uniformity of most nematode species has hampered the establishment of a classification that includes both free-living and parasitic species. Two classes have been recognized (the Secernentea and Adenophorea), based on the presence or absence of a caudal sense organ, respectively. But Blaxter et al.¹ have concluded from the DNA sequences that the Secernentea is a natural group within the Adenophorea. Based on studies of free-living species, a paraphyletic nature for the Adenophorea — that is, a group comprising an ancestor but not all of its descendants — has previously been suggested (for example, by Lorenzen²), but the position of the various parasitic groups has always caused trouble.

One of the most interesting results of the new phylogeny is the discovery that there have been many parallel shifts of feeding strategy within the phylum. The ancestral form was obviously free-living, but the results of Blaxter et al. support the idea that parasitism has evolved independently many times. Of the plant parasites, for example, the order Triplonchida comprises only plant parasites, whereas Dorylaimida comprises both omnivores and plant parasites. And the sister orders Aphelenchida and Tylenchida both comprise fungivores, plant parasites — among which the eelworms (Fig. 2) parasitize many important crops, such as potato and sugar beet — and animal parasites.

Figure 2

BIOPHOTO ASSOCS/HOLT STUDIOS

The bad — eelworm (root knot nematode), which forms characteristic nodules on the roots of sugar beet and rice.

The animal parasites also belong to several groups that probably evolved independently. Outside the Secernentea, the Tricocephalida comprises mammalian parasites (such as the trichina worm) which do not have an intermediate host. But the Mermithida mainly comprises species that have a juvenile stage in which they infest insects. Within the Secernentea are the Strongylida and Rhabditoidea (which are probably sister groups), Strongyloididae, Apelenchida and Tylenchida. The Strongylida comprises vertebrate parasites without an intermediate host (an example is the hook worm). The Rhabditoidea, by contrast, comprises free-living species, such as the favourite experimental model Caenorhabditis elegans, and insect parasites. And the Strongyloididae comprises mammalian parasites, many of which infest horses, pigs and cattle.

Blaxter et al. also identified a large parasitic group within the Secernentea, comprising three groups of vertebrate parasites (the Ascaridida, Spirurida and Oxyurida) and one group of invertebrate parasites (the Rhigonematida). Of the Ascaridida, some species (for example, Ascaris spp.) live in vertebrate intestines. But others, such as species of Anisakis, have more complex life cycles, with a crustacean as the first host, a fish as the second host and a fish-eating bird or mammal as the final host. The Spirurida live in vertebrate tissues, and they are transferred by biting or sucking insects. Well-known species include the filaria worm and the whip worm. Of the Oxyurida, the pinworm is a common but harmless human parasite. Finally, the Rhigonematida comprises parasites of terrestrial arthropods.

The establishment of a natural — that is, phylogenetic — classification for the nematodes is an absolute necessity for all aspects of nematode studies, practical as well as theoretical. Moreover, the classification described by Blaxter et al. will be an invaluable tool for parasitologists, who search for relationships between parasitic species. They can use this information to look for freeliving relatives of important parasites that may be difficult to culture, or for ways in which to combat pests.