Genome duplication, extinction and vertebrate evolution

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Vertebrate evolution has been punctuated by three episodes of widespread gene or genome duplication, which have been linked with the origin of vertebrates, gnathostomes and teleosts, respectively. These three events coincide with bursts of character acquisition and increases in phenotypic complexity, and many researchers have suggested a causal relationship between the two. However, this pattern is derived from data for living taxa only; we argue here that, when fossils are taken into account, bursts of character acquisition disappear and gen(om)e duplication in vertebrate phylogeny can no longer be correlated with the origin of body plans. If patterns of character acquisition or morphological gaps between higher taxa are a reflection of phenotypic complexity, then more inclusive data sets incorporating fossil taxa provide no support for hypotheses linking gen(om)e duplications and the evolution of complexity in vertebrates.

Section snippets

Duplication, duplication, duplication

The distinction between invertebrates and vertebrates has long been considered fundamental, and it pervades all discussions of animal biology. With the recognition that invertebrates are paraphyletic (see Glossary) and do not constitute a natural group, the distinction became little more than a convenient shorthand in communication, but discoveries in molecular biology over the past decade have revealed that the division has real genetic significance. Comparative analysis of invertebrate and

Evolutionary jumps, fossils and extinction

A fundamental problem with the hypothesis linking gen(om)e duplication events in vertebrates with evolutionary jumps is that extinct lineages are ignored. This is unfortunate because, in all three instances, the gulf between the living branches of the vertebrate tree is bridged by a series of extinct clades that are taxonomically and anatomically intermediate. These fossils can provide insight into the nature of morphological evolution through the period in which gen(om)e duplication is

Constraining the timing of gen(om)e duplication events

Although the elucidation of stem vertebrates, stem gnathostomes and stem teleosts refutes the hypothesis that dramatic jumps in character acquisition are associated with the origin of their respective crown groups, some authors have been careful to couch their hypotheses of causality between gen(om)e duplication, molecular and morphological evolution in terms that allow for these events to have occurred somewhere between extant lineages 6, 18, 43. Yet the precise timing of the inferred gen(om)e

Testing the congruence of genetic and phenotypic complexity

The hypothesis that gen(om)e duplications have been significant in facilitating or driving vertebrate evolution requires duplications to be congruent with increases in phenotypic complexity and/or morphological innovation and/or taxon richness. If only extant taxa are considered, the coincidence of character acquisition and taxon richness with duplication events in the lineages leading to living jawed vertebrates and to teleosts, for example, seems obvious, but it is an artefact of incomplete

Acknowledgements

We thank the following for discussion, comments and reviews of the article: Mike Bell, Mike Benton, Peter Forey, Anthony Graham, Philippe Janvier, Gunter Wagner and three anonymous reviewers. Funding from NERC (GT5/99/ES2 to P.C.J.D.; GT5/98/4/ES and NER/J/S/2002/00673 to M.A.P.) and NESTA (P.C.J.D) is gratefully acknowledged.

Glossary

Adaptive radiation:
rapid diversification of a lineage, linked with adaptation to a range of different ecological niches.
Apomorphy:
an advanced group-diagnostic character.
Basal clade:
a monophyletic group that occurs low within the topology of a phylogenetic tree.
Clade:
monophyletic group.
Crown group:
least inclusive clade encompassing the living members of a group and the extinct taxa that nest among them.
Monophyly:
the condition where a group contains the common ancestor of all its members and all

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