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Evolution

Deep-sea spiral fantasies

Pictures of strange, gelatinous deep-sea worms have intrigued zoologists, as they hinted at the solution to an evolutionary puzzle. But does the first specimen to be obtained in good condition back the theories up?

Zoologists dream of connecting up the evolutionary pathways among the ragbag of phyla that have been placed together in the super-phylum Deuterostomia1. This super-phylum includes the chordates — back-boned animals such as ourselves — and the hemichordates (‘half chordates’), which are mostly small, bottom-living marine organisms. Hemichordates arguably possess two chordate features: gill slits and a hollow, dorsal nerve cord. But in other ways, the two main hemichordate classes — the microscopic, tube-dwelling ‘pterobranchs’, which feed on suspended particles, and the much larger, mud-swallowing ‘acorn’ worms (the enteropneusts) — differ considerably from each other in lifestyle and anatomy. A reassessment of the evolutionary histories of the pterobranchs and enteropneusts is now prompted by Holland et al.2 (page 374 of this issue), who report the collection of the first good-quality specimen of a ‘lophenteropneust’ — the supposed ‘missing link’ between the two groups.

The story starts with photographs of the sea bed taken by US oceanographers in the 1960s using a camera dangled from a ship into an abyss in the southwestern Pacific3. These dramatically showed large spiral coils on the ocean bottom, and one photograph was thought to have actually caught an animal in the act of creating one of the enigmatic patterns (Fig. 1). The creature was tentatively identified as an enteropneust worm about a metre in length, with a transparent, gelatinous body 5 centimetres thick and a laterally swollen head end. It was a giant in comparison with shallow-water acorn worms and, rather than burrowing in the sea-bed ooze as the shallow-water worms do, it appeared on the surface of the mud. The characteristic spiral or sometimes looping faecal trail was proposed to be made as the worm moved forward, swallowing sediment and defecating. The evenly separated spiral or looping pattern reflects the side-to-side movement of the head as it forages for particles at the surface of the sludge. These animals turned out to be quite common and widespread denizens of the deep, as shown by photographs of spiral and looping traces at other locations on the abyssal sea floor, particularly in the Southern Hemisphere4(see Fig. 3 on page 375 for more examples).

Figure 1: Worm turns — the first photograph, taken in 1962, of an abyssal enteropneust worm lying on the sea bed near the eastern wall of the Kermadec Trench in the southwestern Pacific.
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The worm's body ends shortly past the first bend, where the faecal coil begins. (Reproduced from ref. 4.)

A few years later, Danish deep-sea biologists led by Henning Lemche studied these and other photographs archived at the Scripps Institution of Oceanography in San Diego, California. They came to the startling conclusion that the broadly expanded collar region at the worm's head end bore tentacles resembling the ‘lophophore’ used for feeding by other pre-chordate groups such as the pterobranchs5. The Danish researchers proposed that the worm had a pterobranch-like head end on an enteropneust body. On this basis, they tentatively designated these deep-sea worms as a new group of hemichordates that they termed the ‘Lophenteropneusta’, or lophophore-bearing enteropneusts. There was a degree of tacit acceptance of this intermediary body form1, from which some people inferred that the ancestral hemichordates were worm-like. But what was needed to determine whether this worm was indeed a living link between enteropneusts and pterobranchs was the recovery of a good specimen of one of these fragile worms for detailed examination.

Holland et al.2 filmed a lophenteropneust gliding over the northeastern Pacific sea bed at a depth of 1,901 m before collecting it using a remotely operated vehicle. These pictures and the authors' careful anatomical study reveal no evidence for any tentacle-like structure on the broad collar on the worm, which is from a new family, genus and species. Holland et al. also review a large number of deep-sea photographs showing broad-collared enteropneusts (including those examined by Lemche et al.), and conclude that none of the creatures has tentacles. The previous misinterpretation from low-quality photographs highlights the risks of trying to construe more than is perhaps wise from sparse and imperfect data.

Other questions, such as how these spiral traces seem to appear in isolation on the muddy ooze, are becoming clear from recent work. Time-lapse photography at 4,100 m depth off California6 suggests that the worms swim or drift to new feeding stations, rather than burrowing to them. The photographs show an enteropneust sweeping up detrital food using its collar, and forming a spiral faecal trace, over a period of 39 hours. The worm then completely emptied its gut and floated off the sea floor. Why don't these abyssal enteropneusts burrow? Perhaps it is because detrital food is limited in amount and quality at these depths, and swimming to a new location rather than burrowing would allow a much wider foraging range.

Other enteropneust species, however, might burrow. Another acorn worm was fortuitously recovered at 2,100 m in the deep northeastern Atlantic using a box corer (specially designed equipment for taking undisturbed samples from the top of the sea floor). The worm was found beneath a mound structure surrounded by burrow openings7. Moreover, numbers of yet another, unidentified, enteropneust species were found living on the surface of a soft, sandy contourite sediment at 850–1,000 m on the eastern flank of the Faroe–Shetland Channel off Scotland8, and multi-opening burrows were found deeper in the channel. But it is unclear whether the worms are responsible for the burrows.

It seems, then, that tentacle-bearing ‘lophenteropneusts’ can be relegated to the realm of fantasy, and enteropneusts and pterobranchs are not as closely related as some people had supposed. Whether or not the ancestral deuterostome body plan resembled today's worm-like enteropneusts is still unclear; what is more certain is that their body form and way of life reflect their modern-day habitats.

References

  1. 1

    Barnes, R. S. K. (ed.) The Diversity of Living Organisms (Blackwell Science, Oxford, 1998).

  2. 2

    Holland, N. D. et al. Nature 434, 374–376 (2005).

  3. 3

    Bourne, D. W. & Heezen, B. C. Science 150, 60–63 (1965).

  4. 4

    Heezen, B. C. & Hollister, C. D. The Face of the Deep (Oxford Univ. Press, 1971).

  5. 5

    Lemche, H., Hanssen, B., Madsen, F. J., Tendal, O. S. & Wolff, T. Vindensk. Meddr. Dansk Naturh. Foren. 139, 262–336 (1976).

  6. 6

    Smith, K. L., Holland, N. D. & Ruhl, H. A. Deep-Sea Res. (in the press).

  7. 7

    Mauviel, A., Juniper, S. K. & Sibuet, M. Deep-Sea Res. 34, 329–335 (1987).

  8. 8

    Bett, B. J. Cont. Shelf Res. 21, 917–956 (2001).

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