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1 January 2005 The Origins of Larvae
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The Origins of Larvae. Donald I. Williamson. Kluwer Academic Publishers, Dordrecht, The Netherlands, 2003. 261 pp., illus. $99.00 (ISBN 14020145143 cloth).

This book is a revised and enlarged edition of Donald T. Williamson's Larvae and Evolution: Toward a New Zoology, published in 1992 (Chapman and Hall). Williamson's goal is to present, and provide evidence for, the hypothesis that “larval forms (or the genes that specify them) have been transferred between groups of animals.” Instead of a bifurcating “tree” (cladograms), where major branches once separated do not rejoin, Williamson suggests that animal evolution is in fact reticulate, with hybridization occurring across large sections of the tree. He also argues that animals have hybridized several times with unicellular protists. If Williamson is correct, then our current understanding of animal evolution is fundamentally wrong, and many scientific careers have essentially been wasted. Williamson, now retired, is an honorary research fellow at the University of Liverpool's Port Erin Marine Biology Laboratory; apart from a series of publications on the topic outlined in this book, he has mainly published on Crustacea.

The Origins of Larvae begins with a general introduction in which Williamson defines larva as an immature phase of an animal that differs significantly from the adult and must, to become an adult, metamorphose (unfortunately, he does not define what amount of change this metamorphosis amounts to). He then points out that the larvae of some distantly related groups are more similar to each other than are the adults of those groups. The contemporary explanation for this, combined with phylogenetic hypotheses for the various groups, suggests either that there has been convergence in the evolution of larval forms or that basic larval forms have been retained as animals have diversified.

Williamson's radical hypothesis is that through cross-fertilization of very different organisms, the whole genome of one animal is added to that of another. However, they do not merge to form a bizarre chimera. Rather, Williamson's idea is that “metamorphosis” is the change from one taxon to another. The implications of this are that the caterpillar larval stage of a butterfly was “gained” by cross-fertilization between a velvet worm (Onychophora) and an ancestral lepidopteran. In fact, he posits that the caterpillar form found in various kinds of insects has been acquired through separate hybridizations with some onychophorans.

The bulk of Williamson's book is a survey of animal adults and larvae and a sweeping range of poorly supported hypotheses as to how larvae were gained in these various animal groups. For example, there is a large group of animals, including segmented worms (Annelida), molluscs, peanut worms (Sipuncula), and ribbon worms (Nemertea), that have a larval form referred to as a trochophore. While some, including myself (Rouse 1999), would suggest that these animals had a common ancestor that had a trochophore, Williamson proposes that the origin of the trochophore in each of these groups was through a hybridization event with a rotifer. Other propositions are that the various larvae found in echinoderms were acquired several different times from hemichordates, and that the zoea larvae found in some shrimps originated from hybridization with mysid crustaceans.

In his earlier book, Williamson suggested that the basic forms of some larvae in eight animal phyla had been transferred from other phyla. In the new book, he now claims that all embryos and larvae were transferred from other taxa, and all transfers can be traced back to animals without larvae. He provides a table to summarize his views, and he offers many other off-the-cuff proposals throughout; there is also a series of line drawings, but, unfortunately, they are often pixelated and of poor quality.

Beyond the fact that this proposal flies in the face of much of what we know about developmental genetics, the simple question this book raises is this: Is Williamson's hypothesis heuristic? In my opinion, the answer is no. Williamson would rather invoke an extraordinarily complicated series of hybridizations across animals than accept that some convergence may have happened in larval forms, or that our understanding of the animal phylogenetic tree is still (rapidly) developing. Williamson sees some of the incongruities from phylogenetic analysis of DNA, particularly the 18S rRNA gene, as providing support for some of his hybridization hypotheses, while ignoring the inference problems that this particular gene can present (Abouheif et al. 1998). Unfortunately, he disregards many of the recent papers on larval forms and the phylogeny of animals, and he takes no note of errors pointed out in a review of the first edition of his book (Strathmann 1993).

Apart from his broad comparative survey of larvae across animals, Williamson's major piece of evidence in support of his thesis is based on an experiment in which he produced hybrids from two very different animals. The frontispiece for The Origins of Larvae shows four adult sea urchins that are said to be hybrids of eggs from a tunicate, Ascidia mentula, and the sperm of the sea urchin Echinus esculentus. Williamson reported on this experiment in his earlier book and provides more details on the procedure here. Unfortunately, he has not repeated it or performed any other experiments, and an elegant paper by Hart (1996) proved that Williamson's hybrids were unlikely to be hybrids at all. Eggs contain numerous mitochondria and a nucleus, both containing DNA. Sperm also contain both of these DNA-bearing components, but the mitochondria found in sperm do not persist after fertilization. Thus an offspring of a sea urchin and a tunicate should have a mixture of parental nuclear genes but only maternal mitochondrial genes. Hart (1996) sequenced both mitochondrial and nuclear genes from one of Williamson's “hybrids” as well as individuals from “pure'” A. mentula and E. esculentus. His results showed that the putative hybrid contained only sea urchin DNA and probably lacked tunicate DNA, thus making a hybrid origin very unlikely. Williamson discusses the paper by Hart (1996), but he rejects it and reiterates that he made no errors.

So, do I think that there are research themes worth following up in this book? No, I don't, not on the evidence presented here. Williamson presented a challenge to scientists in his 1992 book. This was taken up, and his one solid piece of evidence was shown to probably be an error. Williamson provides no other new evidence from the intervening years to back his claims, he has gathered no collaborators, and he provides no new experiments or detailed phylogenetic analyses. Rather, he has simply expanded his theory and rhetoric.

References cited

1.

E. Abouheif, R. Zardoya, and A. Meyer . 1998. Limitations of metazoan 18S rRNA sequence data: Implications for reconstructing a phylogeny of the animal kingdom and inferring the reality of the Cambrian explosion. Journal of Molecular Evolution 47:394–405. Google Scholar

2.

M. W. Hart 1996. Testing cold fusion of phyla: Maternity in a tunicate x sea urchin hybrid determined by DNA comparisons. Evolution 50:1713–1718. Google Scholar

3.

G. W. Rouse 1999. Trochophore concepts: Ciliary bands and the evolution of larvae in spiralian Metazoa. Biological Journal of the Linnnean Society 66:411–464. Google Scholar

4.

R. R. Strathmann 1993. Book review: Larvae and Evolution: Towards a New Zoology. Quarterly Review of Biology 68:280–282. Google Scholar

Appendices

GREG ROUSE "The Origins of Larvae," BioScience 55(1), 81-82, (1 January 2005). https://doi.org/10.1641/0006-3568(2005)055[0081:IOVOAP]2.0.CO;2
Published: 1 January 2005
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