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The way we were

Did the great-great-granddaddy of us all look like the tiny marine larva that's just grown up in a Tokyo lab? Caroline Williams reports

LOOKING down a microscope at small whizzy things is just so 19th century. After all, Victorian naturalists did such a great job of describing, cataloguing and classifying species that there’s nothing left to discover, right?

Well, actually no. There has been an embarrassing hole in our knowledge all along, in the shape of the larvae of the humble sea lily. For more than a century biologists have been trying, and failing, to get a look at this tiny creature. Some tried diving down and capturing the larvae alive, but they couldn’t go deep enough. Others tried to breed them in the lab, but the adults always died.

But earlier this year a team of biologists from the University of Tokyo announced that they had successfully bred a sea lily in the lab and taken a good, long look at its larvae. The announcement was greeted with sighs of relief from all over the world of biology.

One sigh was for the sake of the taxonomic jigsaw. We know what the larvae of all other echinoderms – starfish, sea urchins, brittle stars and sea cucumbers – are like, so it was nice to complete the picture at last. But there was another, more profound, reason for the collective relief.

According to a prominent theory, sea lily larvae hold the key to one of evolution’s greatest unsolved puzzles – the origin of chordates, the group to which we and all other vertebrates belong. In short, some scientists think that sea lily larvae look exactly like our distant ancestors from more than 570 million years ago.

Sea lilies, also known as stalked crinoids, are mysterious animals. They live on the deep ocean floor, around 400 metres down, where they filter-feed their adult lives away in almost total darkness. Little else is known about their way of life, especially during the larval stages.

But among evolutionary biologists, the sea lily is something of a celebrity. In taxonomy, the Echinodermata comprise a phylum, putting the group on an equal footing with, say, the arthropods and chordates. And it is not just any old phylum. Several theories cast it in a starring role in the history of life, at that pivotal point where the vertebrates and invertebrates diverged.

One of the most important theories dates back to 1894, when British embryologist Walter Garstang proposed that the echinoderms and the chordates evolved from a common ancestor. He speculated that this ancestor resembled an auricularia – a tiny, free-swimming larva which forms part of the life cycle of most modern echinoderms. Garstang was inspired by the fact that auricularia sport long, thin bands of hairlike cilia on their bodies, underlain by lines of nerve cells. Perhaps, he argued, these nerve cells fused and rearranged themselves at some point during evolution to become the defining feature of the chordates – the nerve cord.

To test the idea, Garstang needed to find the most “basal” member of the Echinodermata – the one that had been around the longest, and so retained the group’s most primitive characteristics. Then he had to look at its larvae. If these, too, went through the auricularia stage, the hypothesis was holding up. But if they didn’t, the hypothesis was dead in the water, as it would mean the auricularia stage evolved too late to be a prototype chordate.

But Garstang was fresh out of luck. The most primitive member of the echinoderms turned out to be the sea lily – with a fossil record stretching back 500 million years – and no one had ever seen its larvae.

It wasn’t for lack of trying. Sea lilies live far too deep for their larvae to be collected by scuba divers, and although the adults often come up in fishing nets, they are usually dead or damaged. Even if you are lucky enough to get hold of an undamaged specimen, they often refuse to reproduce in the lab. Nick Holland from the Scripps Institution of Oceanography in La Jolla, California, has been working on the problem for many years. “For some reason nobody knows, sea lilies are rarely collected with ripe gonads,” he says, “and even when they are, they will sulk in the lab and never spawn.”

Undeterred, Shonan Amemiya and a team of biologists from the University of Tokyo set off on their own sea lily odyssey. In the late 1980s they unearthed some old papers dating back to 1890 that described how adults of one species of sea lily, Metacrinus rotundus, could be found in two shallow bays southwest of Tokyo. Both bays were just 150 metres deep.

If adult sea lilies were living in such shallow water, surely there was a chance of collecting lots of healthy specimens? To find out, the team sought out local fishermen, who confirmed that the sea lilies often came up with the day’s catch, and in 1990 Amemiya negotiated a constant supply of healthy specimens for the laboratory.

The next problem was keeping the creatures alive in the lab long enough for them to reproduce. It was a laborious process. At first the sea lilies died by the dozen. Finally the team worked out that they needed darkness, a temperature of about 14 °C and a gentle one-way current. But even then the sea lilies sulked. It took until September 1992 to get one to spawn, and a further 6 years to successfully fertilise any eggs. Even then the embryos promptly died. The larvae, it seemed, were just as moody as their parents. Another 2 years passed before any embryos survived more than a few hours. Then, in late September 2000, the team saw what they had been waiting for (Nature, vol 421, p 158).

“When we first saw the larvae swimming, they looked like little spacecraft flying around,” says Amemiya. “We felt as though we were in the sea of the Cambrian period.” Even better, the larvae had an auricularia stage. Garstang would have been overjoyed.

But is the problem cracked? It depends on how far you go along with Garstang’s theory. “I was delighted,” says Claus Nielsen, invertebrate curator at the Zoological Museum in Copenhagen. “It fills a hole I’ve been trying to fill for some time…But it doesn’t contribute to chordate evolution.” Nick Holland agrees. “It’s damn good, and lucky, biology,” he says. “They have supplied a missing piece of evidence that gives insights into evolution within the Echinodermata. But it says much less about the origin of the vertebrates from the invertebrates.”

Nielson and Holland are not alone in their scepticism. At the last count there were more than 100 hypotheses about where the chordate nervous system came from, and to many scientists this new discovery doesn’t change a thing. The bottom line is that we may never know. Chordate ancestors may have been so small and soft-bodied that few fossils would have survived.

But the new discovery at least gives Garstang’s supporters something to go on. Now that they know sea lilies have auricularia larvae like other echinoderms, they can study the sea cucumber and its larvae instead, which are much less prone to the sulks, and look for molecular similarities between larval bands and our own nervous system. For supporters of the other 100 theories, however, the search for our elusive ancestor is a long way from over.

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