This article was published in Scientific American’s former blog network and reflects the views of the author, not necessarily those of Scientific American
Few people will find delight in the dredge that is hauled from the ocean floor. But for the British biologist Ray Lankester, such hauls represented an unseen world of wonder. In his Diversions of a Naturalist he describes how an encounter with a creature from the bottom of the sea that filled him with so much joy that he completely forgot about his sea-sickness:
"I remember lying very ill on the deck of a slowly lurching ‘lugger’ in a heaving sea off Guernsey, when the dredge came up,and as its contents were turned out near me, a semi-transparent, oblong, flattened thing like a small paper-knife began to hop about on the boards. It was the first specimen I ever saw alive of the lancelet, that strange, fish-like little creature."~ Ray Lankester (1915)
Lankester had good reasons to be excited. For him and other naturalists, the lancelet was not merely another bottom dweller; it was a creature with the potential to resolve the ancient origins of the vertebrates, group of animals with a spine. But that's running ahead of the story. What kind of creature is the lancelet, to begin with? The German zoologist Pallas was the first to describe the lancelet in the scientific literature. He worked with a preserved specimen, and mistakenly classified it as a slug in 1774. Perhaps he would have recognized how un-slug like the lancelet really is if he had seen one alive, wiggling and hopping about.
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The 19th century naturalists Costa and Yarrell did have this opportunity. They were also the first to note that the lancelet resembles a vertebrate. Not only does the lancelet have a rudimentary spine that runs from their head to their tail, they also have segmented muscle bundles and a tail that extends past their anus, just like other vertebrates have.
Lancelets and vertebrates share a similar anatomy, but a lancelet is not a vertebrate quite yet. There is still a huge gap between the complex tissues of vertebrates and the simple organization of their lancelet equivalents. The lancelet's nerve cord is slightly swollen near its head, but this bulge is not yet a brain. Lancelets have contracting blood vessels that pump around blood, but no central heart. And then there are the organs that they lack entirely, such as a skull or a pair of eyes. Ernst Haeckel was right when he wrote that "the lancelet differs more from the fishes than the fishes do from man".
As a creature on the border between vertebrate and invertebrate, biologists first regarded the lancelet as a 'primitive vertebrate' and later as 'closest living cousin of vertebrates' (and other almost-vertebrates, such as hagfish). It was clear to all that these little paper-knives were important creatures for studying the origins of the vertebrate lineage. No one believed that the lancelets were the unchanged descendants of some proto-vertebrate, but biologists reasoned that since all traits shared between lancelets and vertebrates have been inherited from a common ancestor, the lancelet still offered a glimpse of what these distant ancestors might have looked like.
Fossil unearthed in Canada and China show that there is some truth to this logic. The ancient Pikaia already had a flexible proto-spine and segmented muscles, resembles the lancelet in these regards. Pikaia is not a direct ancestor of either vertebrates or lancelets, but palaeontologists agree that they represent some of our earliest relatives.
In short, for more than a century, all the evidence seemed to indicate that the family ties between lancelets and vertebrates were close. Until 2006, when a team of molecular biologists drove a chain-saw into the stem of the vertebrate family tree. Their DNA-analyses revealed that not lancelets, but sea squirts and their ilk (the tunicates) are the closest living relatives of vertebrates. Common zoological sense turned out to be wrong. Somehow these shapeless sacks, hardly recognizable as animals, are closer related to us than the mobile and gracile lancelets.
To be fair, biologists long knew that sea squirts occupy a branch close to the vertebrates in the tree of life. Adult sea squirts might be stationary filter feeding tubes, but their larvae look more like tadpoles than anything else. It was the Russian embryologist Alexander Kowalevsky who first noted that young sea squirts come complete with a head, tail and a proto-spine in 1866.
The lancelet genome, sequenced in 2008, confirmed that tunicates are the sister lineage of vertebrates and that lancelets branched off first. This redrawn family tree opens a whole new can of questions. If sea squirts really are our closest non-vertebrate cousins, how come we look so different from each other as adults?
Our genes hold some clues. The genomes of both tunicates and vertebrates show signs of widespread, but different kinds of, genetic upheaval. The first evidence that the genomes of the first vertebrates differed drastically from those of their forebears came from the observation that some of their gene families are overrepresented, often following a 4:1 ratio.
Take the famous Hox genes. These genes determine the shape of animals by regulating which segments develop into what kind of structure, such as a rib. Hox genes are arranged in clusters and are 'read' in a strict order during the development. Humans, mice, and chickens have four of these clusters, whereas invertebrates such as lancelets only have one. Confronted with this pattern again and again, biologists concluded that the entire genome of the ancestral vertebrate must have been duplicated twice, giving rise to a fourfold increase in genes. These two rounds of duplication were followed by massive gene losses where redundant and harmful copies were purged from the genome. Many biologists think that the genes that remained opened up the road to an increase in complexity, as genes acquired new roles and functions. More on this in a later blog post.
The genomes of sea squirts tell a different story. Instead of gaining genes, they have lost many of them over time. Of all the Hox genes that are present in the lancelet genome, 25 are missing from tunicate genomes. The remaining Hox genes have been shuffled around, generating scrambled versions of the traditional Hox clusters. As a cause or consequence, the development sea squirt larvae also proceeds in a way that is different from what we know of lancelet and vertebrate embryos. Their genes and genomes also seem to evolve at a higher rate and accumulating changes faster than the genes of lancelets and vertebrates do.
Vertebrates and tunicates thus seem to have evolved in completely opposite directions. Where the tunicates lost genes, the vertebrates gained them. As tunicates grew more simple and derived, the vertebrates became more complex. It's thrilling to realize that their starting point was the same: a strange, little fish-like creature, not unlike the humble lancelet. If only it were possible to travel back 500 billion years in time on a lurching lugger, dredging the Cambrian oceans seeing what wonders come up.
Images
Lancelet by Hans Hillewaert
Lancelet drawing from Yarrell's 'A History of British Fishes'
Ciona intestinalis by Havspappan
Sea squirt larva and tadpole from Lankester's 'Zoological articles contributed to the "Encyclopaedia Britannica"'
References
Lankester, E. R. Diversions of a Naturalist 2 (Methuen, London, 1915)
Yarrell, W. A History of British Fishes 468–472 (Van Voorst, London, 1836)
Haeckel, E. The Evolution of Man 2.17 (C. Kegan Paul & Co, 1879)
DONOGHUE, P., & PURNELL, M. (2005). Genome duplication, extinction and vertebrate evolution Trends in Ecology & Evolution, 20 (6), 312-319 DOI: 10.1016/j.tree.2005.04.008
Delsuc, F., Brinkmann, H., Chourrout, D., & Philippe, H. (2006). Tunicates and not cephalochordates are the closest living relatives of vertebrates Nature, 439 (7079), 965-968 DOI: 10.1038/nature04336
A. Kovalevsky, "Entwicklungsgeschichte der einfachen Ascidien", Mémoires de l'Académie Impériale des sciences de St-Pétersbourg, 15
Dehal P, & Boore JL (2005). Two rounds of whole genome duplication in the ancestral vertebrate. PLoS biology, 3 (10) PMID: 16128622
Holland, P. (2010). From genomes to morphology: a view from amphioxus Acta Zoologica, 91 (1), 81-86 DOI: 10.1111/j.1463-6395.2009.00427.x