Symbiosis DOI 10.1007/s13199-011-0106-6 Larval genome transfer: hybridogenesis in animal phylogeny Donald Irving Williamson Received: 15 October 2010 /Accepted: 4 January 2011 # The Author(s) 2011. This article is published with open access at Springerlink.com Abstract My larval transfer hypothesis asserts that mature Keywords Saltatory evolution . Sequential and concurrent adults became larvae in foreign animal lineages by genome chimeras . Hybridization . Recapitulation . Planctospheres . acquisition. Larval genomes were acquired by hybridization Echinoderms . Hemichordates . Lophotrochozoans when sperm of one animal fertilized eggs of another animal, often remotely related. There were no larvae in any phylum until the classes (and, in some cases, the 1 Background and significance orders) of that phylum had evolved. Since larvae were acquired by hybrid transfer, they are not directly related to Larvae are active immature animals that differ significantly the adults that metamorphose from them. The widely from the adults that will succeed them in ontogeny. The accepted classification that associates echinoderms and larval transfer hypothesis claims that basic forms of all chordates as deuterostomes, and annelids and molluscs as larvae originated as adults in other taxa, and they were trochophorates or lophotrochozoans, is flawed. Symbio- transferred by sexual hybridization between species at all genesis, the generation of new life forms by symbiosis, levels of relationship (Williamson 2003). The first larvae accounts for the discontinuous evolution of eukaryotic cells resulted when eggs of one species were fertilized by sperm from prokaryotes. Hybridogenesis, the generation of new from another species. The eggs hatched as larvae resem- life forms and life histories by hybridization in sexually bling one parent, then metamorphosed into juveniles (small reproducing animals, occurred at all taxonomic levels from adults) resembling the other. All descendants of this cross species to superphyla. Not only were larvae acquired by were animals with larvae, in which one animal form transfer from foreign adults from the late Palaeozoic to the follows another: they were sequential chimeras (Williamson present, but also complex animals were generated from 1991). Corollaries of the larval transfer hypothesis are that simpler ones by this process in the Cambrian explosion, larvae were later additions to the evolutionary histories of and organ systems were transferred between remotely species with indirect development, and they do not related animals. There are several types of evolution. represent evolutionary ancestors of such species. Metamor- Symbiogenesis and hybridogenesis are saltatory genome phosis represents a change of taxon during development. transfer processes that dramatically supplement the gradual Hybridogenesis is the generation of new life forms and accumulation of random mutations within separate lineages life histories by hybridization in sexually reproducing described by Darwin. animals. It accounts for the acquisition of larvae by many animals (larval transfer), and also for the production of complex animals from simpler ones in the Cambrian D. I. Williamson School of Biological Sciences, University of Liverpool, explosion, and for the transfer of organ systems between Liverpool, UK remotely related animals (component transfer). Symbio- genesis, the generation of new life forms by symbiosis, * D. I. Williamson ( ) accounts for the origin of eukaryotes from prokaryotes. 14 Pairk Beg, Port Erin, Isle of Man IM9 6NH, UK Hybridogenesis and symbiogenesis are both saltatory e-mail: [email protected] evolutionary processes that involve fusions of genomes of D.I. Williamson remotely related organisms. They dramatically supplement “the auricularia [of sea cucumbers], the bipinnaria [of the gradual accumulation of random mutations within starfish] and the pluteus [of sea urchins and brittle stars], separate lineages described by Darwin. but not the transversely ringed [doliolaria] larvae of the Darwin (1859) insisted that evolution is gradual, and he Crinoidea [sea lilies], can be reduced to a common type.” assumed that the larva and adult of any species had evolved He deduced that “the various existing types of [echino- gradually from a common ancestor. He thought that larvae derm] larvae must have been formed after the differentia- showed the true relationships of taxa, and he wrote, “Even tion of the existing groups of the Echinodermata; otherwise the illustrious Cuvier did not perceive that a barnacle was, it would be necessary to adopt the impossible position that as it certainly is, a crustacean; but a glance at the larva the different groups of Echinodermata were severally shows this to be the case in an unmistakable manner.” descended from the different types of larvae.” (Darwin 1859: 420). Barnacles go through nauplius and Garstang (1894, 1922, 1928) ignored Balfour’s works. cypris stages in their development, and both these larval He amended Haeckel’s theory of recapitulation by propos- forms had adult counterparts. Cambrian nauplii were non- ing that modern larvae represent ancestral larvae rather than crustacean adults, some descendants of which hybridized ancestral adults, and that, contrary to Haeckel, ontogeny with a variety of crustaceans to give them nauplius larvae creates phylogeny rather than recapitulating it. Garstang’s (Williamson and Rice 1996; Williamson 2006a, b). The innovation, however, was a modification rather than a cypris has its adult counterpart in the Cambrian crustacean rejection of the hypothesis that larvae represent ancestors. Canadaspis (Briggs 1978). Also, barnacle larvae resemble He drew attention to cases in which larvae of one taxon rhizocephalan larvae. Adult rhizocephalans are parasites of resemble adults in another, such as trochophore larvae and crabs and hermit crabs, and are totally devoid of crustacean adult rotifers, and he proposed that such adults are or arthropod characteristics (Williamson 2009). I agree that descendants of ‘persistent larvae’: animals that had barnacles are crustaceans, but not because of their larvae. matured in the larval state. Trochophore larvae, also Darwin regarded larvae as ‘active embryos’,andhe known as trochosphere larvae, resemble rotifers of the said, “As the embryonic state of each species and group genus Trochosphaera, and occur in some members of at of species partially shows us the structure of their less least eight phyla, including annelids and molluscs. modified ancient progenitors, we can clearly see why AccordingtoGarstang(1922), the phylum Rotifera ancient and extinct forms of life should resemble the evolved from a form resembling Trochosphaera,which embryos of their descendants—our existing species” originated as a trochophore larva that had matured without (Darwin 1859: 449). Haeckel (1866)madethisthebasis metamorphosis. He maintained that annelids, molluscs and of his ‘biogenetic law’,alsoknownas‘the theory of several other phyla evolved from a common ancestor recapitulation’. This postulates that larvae represent which had trochophore larvae. No-one, however, has ancestral adults, ontogeny is a short and rapid recapitula- proposed a feasible phylogeny of rotifers based on their tion of phylogeny, and major evolutionary innovations are evolution from a form resembling Trochosphaera. confined to adults. Applying his law to echinoderms, The affinities of the respective classes of adult echino- Haeckel reasoned that recent and fossil adults, all of which derms conflict with the affinities of their larvae. I, are primarily radial, had evolved from bilateral ancestors, independently of Balfour (1880–1881), decided that this similar to extant larvae. anomaly could be explained if early echinoderms had no Balfour (1880–1881) put forward a very different view larvae, and larval forms were ‘transferred’ after the on larvae. He distinguished between primary larvae, “which establishment of the extant classes. In other phyla, such as have continued uninterruptedly to develop as free larvae annelids, molluscs and bryozoans, the presence or absence from the time when they constituted the adult form of the of larvae is again consistent with the acquisition of larvae species”, and secondary larvae, “which have become after the establishment of the classes (or, in some cases, the introduced into the ontogeny of species, the young of orders) of the phyla. Many developmental anomalies are which were originally hatched with all the characters of the consistent with the hypothesis that genes prescribing larvae adult.” He regarded all extant larvae, except the planula had been transferred, and the only known process that could larvae of cnidarians, as secondary, but he made no transfer genes in sufficient quantity is hybridization, leading suggestions on the sources of secondary larvae. He inferred to mergers of genomes. In my early publications on the from the structure of the nervous system of adult and larval subject, I claimed that some larvae in eight phyla had been echinoderms that “adult Echinodermata have retained transferred from other taxa by hybridization (Williamson (Balfour’s italics), and not, as is now usually held, 1988a, b, 1991, 1992, 1996), and my publications from 1998 secondarily acquired, their radial symmetry; and if this is extended the larval transfer hypothesis to all larvae. admitted it follows that the obvious bilateral symmetry of Laboratory experiments on the fertilization of ascidian eggs Echinoderm larvae is