A reprint from American Scientist the magazine of Sigma Xi, The Scientific Research Society This reprint is provided for personal and noncommercial use. For any other use, please send a request to Permissions, American Scientist, P.O. Box 13975, Research Triangle Park, NC, 27709, U.S.A., or by electronic mail to [email protected]. ©Sigma Xi, The Scientific Research Society and other rightsholders The Origins of Larvae Mismatches between the forms of adult animals and their larvae may reflect fused genomes, expressed in sequence in complex life histories Donald I. Williamson and Sonya E. Vickers ince the earliest days of the field—when a Syoung Charles Darwin worked on his beloved barnacles, shelled shrimplike creatures, cemented to rocks, which lie on their backs and kick food into their mouths—evolutionary biologists have been fascinated by life’s myriad odd forms. The rigorous naturalist confronted with unexplained peculiari- ties of form, life history or behavior is compelled to search doggedly for a scientific explanation. Just such a search some 150 years ago gave the world The Origin of Species, which remains the founda- tional scientific explanation of how plants and ani- mals have changed through time. More animals are hatched or born than possibly survive to have offspring in their environment, Darwin wrote. Thus pressured to adapt, populations change gradually through time; they “descend with modification.” Darwin emphasized the gradual nature of change in living form that today we call evolution: the accumulation of changes, or mutations, through heredity. Not all modern theorists have accepted that change is gradual. Indeed, nature presents forms that can only be explained by sudden change. One of us (Williamson) has focused on such a case: D. P. Wilson/FLPA larvae, the distinctive young forms of many ani- Figure 1. Luidia sarsi, a starfish found in the North Sea and along the southern mals. These forms can differ so markedly from the and western shores of the British Isles, develops from a fertilized egg into a adults into which they develop that an observer larva with bilateral symmetry, inside which grows a juvenile form with the ra- is tempted to classify them as different species. dial symmetry of the starfish. In this unusual life history, the juvenile migrates And such an observer, we argue, might be right in to the outside and drops off the swimming larva (the translucent shape in this photograph); both continue to live independently for up to three months. a way. Williamson’s “larval transfer” hypothesis Author Williamson’s larval-transfer hypothesis explains this oddity as the ex- proposes that larvae, and the genes that specify pression of genomes fused when two ancestral marine animals hybridized, one them, have been transferred from one hereditary becoming the larva of the other. This argument is not only a radical proposal animal lineage to another by cross-species, cross- for solving open questions in the evolution of development but also one of genera and even cross-phyla fertilizations. We feel several proposals that suggests a bushier shape to the “tree of life” that Charles compelled to ask a question that is obvious to those Darwin proposed. © 2007 Sigma Xi, The Scientific Research Society. Reproduction www.americanscientist.org 2007 November–December 509 with permission only. Contact [email protected]. organisms came to the same solution to problems such as dispersal and feeding. In this article we will tell a differ- ent version of the origin of larvae, dis- tinct from the “same stock” concept but consistent with Darwin’s theory of natural selection: Larva and adult began as different animals, each developing from its own type of egg. At a point in their evolu- tionary past, their ancestors interbred and produced offspring. Most hybrid offspring did not survive. Genomes so unlike each other had many difficul- ties in expression—the translation of genes into proteins. The few hybrids that did survive solved the dilemma by expressing their combined genomes sequentially rather than concurrently, first the larval genes and then the adult. The new combined animal survived and went on to reproduce specialized forms, usually highly advantageous in a b c the procurement of habitat and food, then spread their genes as adults. The Figure 2. From Darwin forward, classical theory has viewed life’s evolutionary history as taking legacy left by the patching together of place through continuing adaptation and mutation. Darwin’s tree of life may be seen as a smooth- dissimilar ancestral lines is the perilous ly branching tree in which each bifurcation indicates common ancestry, and truncated branches transition we call metamorphosis, the indicate extinctions (a). In 1972, Niles Eldredge and Stephen Jay Gould, noting spurts of activity stage at which the larva transforms into in the fossil record, introduced the concept of “punctuated equilibrium,” pointing out that species the adult. The outcome is frequently appear fully formed (b). Williamson’s larval-transfer theory introduces another wrinkle: the notion not transformation but death. that one animal can become the larva of another, even distantly related animal by hybridization, thus establishing a connection between two branches of the tree of life (c). The diagrams trace the ancestry of a hypothetical starfish (red), one of several species that may have acquired larvae The Tangled Tree of Life through hybridization (blue arrows). (Adapted from a diagram by Sonya E. Vickers.) Darwin’s Origin gave science a pow- erful metaphor: the tree of life. The not trapped in conventional evolution- In 21st-century scientific language, we Darwinian view of life’s history is ary thinking: Could animals with larval would say that a portion of one ani- a tree whose central trunk is root- forms be hybrids, the products of suc- mal’s complement of genetic material, ed in common ancestry. The tree’s cessful fusions of genomes that are ex- or genome, was acquired by another, branches—main limbs from which pressed in sequence during the animal’s creating a chimeric organism. further branches diverge, each bifur- life history? Following Darwin, most biologists cation indicating common ancestry— Larvae, familiar as immature stages today assume that a larva and its adult represent the diversity of life that arose in many animal life histories, are espe- began as a single individual and that over time. Most branches fail to reach cially common in marine plankton. The over time, the young gradually became the top (the present), as more than 99 caterpillar larva that spins the chrysalis more and more different from their adult percent of all past life on Earth is esti- from which an adult butterfly emerges forms. This can be labeled the “same mated to belong to extinct species. lives on land, but most dramatic lar- stock” or “direct filiation” assumption. A new concept, “punctuated equi- val-adult transformation takes place in Until recently, there was no alterna- librium,” was introduced by Niles El- the sea. Clams, starfish and sea urchins tive theory and no need to defend the dredge and Stephen Jay Gould in 1972 cast their eggs and sperm into the sea, presumption. There were unexplained to replace Darwin’s gradually branch- where they merge in fertilization. The anomalies, but these were regarded as ing tree. Eldredge and Gould pointed larval-transfer hypothesis proposes that mere curiosities. Conventional think- out that the fossil record contradicts all larvae transferred into their present- ing offers convergent evolution as the the “numerous, successive, slight mod- day lineages from other distantly relat- dominant explanation for the similarities ifications” described by Darwin. “A ed animal groups by cross-fertilization. of many larvae, speculating that many species does not arise gradually by the steady transformation of its ancestors,” they argued; rather, “it appears all at Until he retired in 1997, Donald I. Williamson was Reader in Marine Biology at the University of Liv- once and fully formed.” The concept erpool in the United Kingdom. He specialized in marine plankton, particularly marine larvae. Most of his publications are on crustacean larvae. He is the author of Larvae and Evolution: Toward a New of punctuated equilibrium explains the Zoology (Chapman and Hall, 1992) and The Origins of Larvae (Kluwer, 2003). Sonya E. Vickers is fossil record by spurts of activity fol- a teacher and naturalist. She has traveled extensively within the U.S. and around the world to sites of lowed by stasis. The Eldredge-Gould natural interest. Address for Williamson: 14 Pairk Beg, Port Erin, Isle of Man IM9 6NH, UK. Internet: replacement for Darwin’s tree looks [email protected] like a candelabra. © 2007 Sigma Xi, The Scientific Research Society. Reproduction 510 American Scientist, Volume 95 with permission only. Contact [email protected]. Larval transfer is one of a number of phenomena that imply a bushier sort of tree, one whose branches occasionally fuse. Although less tidy, the concept is not new. In sexual animals, fertiliza- tion routinely fuses genomes, usually those of members of the same spe- cies. But genome fusion can even take place between biological kingdoms, as in the formation of the composite life forms called lichens. These gray-green patches on rocks and trees represent fu- sions between a green alga in the protist kingdom (or often a cyanobacterium in 2 1 the prokaryote kingdom) with specific ascomycetes in the fungus kingdom. And as this article was going to press, 4JQVODVMB "OOFMJEB .PMMVTDB SPUJGFS the genome of the fruit fly Drosophila ananassae was found to have encapsu- Figure 3. Rotifers have simple life histories, but these small marine and freshwater animals may have lated within it the entire genome of the contributed a larval stage to the life histories of other animals, explaining the scattering of so-called bacterium Wolbachia, each generation of trochophore larvae through unrelated phyla.