Trends in Ecology & Evolution
Volume 15, Issue 11, 1 November 2000, Pages 454-459
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Review
Rare genomic changes as a tool for phylogenetics

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Abstract

DNA sequence data have offered valuable insights into the relationships between living organisms. However, most phylogenetic analyses of DNA sequences rely primarily on single nucleotide substitutions, which might not be perfect phylogenetic markers. Rare genomic changes (RGCs), such as intron indels, retroposon integrations, signature sequences, mitochondrial and chloroplast gene order changes, gene duplications and genetic code changes, provide a suite of complementary markers with enormous potential for molecular systematics. Recent exploitation of RGCs has already started to yield exciting phylogenetic information.

Section snippets

Rare genomic changes

We define RGCs as large-scale mutational changes that have occurred in the genomes of particular clades. Examples of RGCs (Table 1) include intron indels, retroposon integrations, signature sequences, changes in organelle gene order, gene duplications and genetic code variants. Most RGCs represent changes caused by single (or a few) mutational events; in our discussion of RGCs we do not include genomic characteristics that are, most probably, the end result of multiple processes (e.g. genomic

RGCs as ‘Hennigian’ markers

The field of phylogenetics has been strongly influenced by the founder of the cladistic methodology, the German entomologist Willi Hennig. Hennig argued that only shared derived characters (synapomorphies; Box 1) should be used as indicators of common descent. Plotting the distribution of synapomorphies is the essence of cladistic reconstruction. The principal hindrance to this task is homoplasy (see Box 1 for definition). In general, character states that arise rarely will not be prone to

Of fish and flies: intron indels as clade markers

The power and robustness of RGCs is well demonstrated by the study of Venkatesh et al.13, in which intron indels (Box 1) were used to investigate fish phylogeny. Venkatesh et al. identified seven intron positions (in five genes) that are present in the pufferfish Takifugu rubripes but not in the homologous genes of mammals. Four introns were also found in the rhodopsin gene that were present in the ancestral chordate rhodopsin gene (as inferred by their presence in basal chordates, such as

Of SINEs and LINEs

Retroposons (Box 1) belong to the group of transposable elements that use an RNA-mediated mode of transposition12. Retroposon integrations, especially from the class of SINEs (retroposons that lack the ability for self-amplification), have been used successfully as phylogenetic markers; an application pioneered by Okada and colleagues in the 1990s (Refs 18., 19.). It has been argued that SINE integrations come close to being ‘perfect’ markers of common descent because integration is apparently

Animals, archaebacteria and archezoa: the use of signature sequences

The complementary use of primary sequence data and RGCs for phylogenetic purposes is shown by attempts to reconstruct the interphyletic relationships of animals. Recent studies using 18S rDNA sequences have suggested a three-branched Bilateria (Box 1) tree comprising the Deuterostomia, the Lophotrochozoa and the Ecdysozoa3. Lophotrochozoans include spiral cleaving phyla, such as molluscs, annelids, platyhelminths and nemerteans, plus the lophophorates; whereas the Ecdysozoa include arthropods,

Deviant codes and shuffled genes

Several organisms use genetic codes that deviate from the standard ‘universal’ code. These ‘deviant’ codes can be useful markers for higher level phylogenetics. Keeling and Doolittle32 showed that a genetic code in which TAA and TAG codons encode glutamine, rather than termination, is used by almost all diplomonads, with the exception of the genus Giardia, which employs the standard genetic code. This argues for an early divergence of Giardia in the evolution of diplomonads and is in agreement

Other potential RGCs

The list of RGCs we have described so far is not exhaustive; several other categories of large-scale mutation exist, some of which have potential for phylogenetics. For example, gene duplications have not yet been widely exploited. One difficulty is technical: unless a family of genes is arranged in a tandem array, discerning whether a duplicated copy of a gene exists is difficult because absence of evidence does not equate with evidence for absence. This problem cannot be definitively overcome

A concluding mix of caution and optimism

One obstacle that makes some researchers feel uneasy about the use of RGCs is the absence of statistical evaluation4., 22.. This concern stems mainly from analogy with primarily sequence comparisons. Understanding the forces that shape sequence evolution is a necessary prerequisite to using sequence data for phylogenetics and for evaluating the statistical robustness of trees. To reach the same degree of sophistication in the analysis of RGCs demands greater knowledge about the mechanisms that

Acknowledgements

A.R. acknowledges partial funding from a NERC studentship; research in P.W.H.H.'s laboratory is funded by BBSRC. We thank G. Stone for his tolerance, and N. Okada and two anonymous referees for comments on this article. Special thanks to G. Brown, S. Ferguson, M. Kobayashi, J. Pemberton, and D. Remsen and the Marine Biological Laboratory for providing photographs. P. Preston very kindly allowed the use of specimens from the Natural History collections of the University of Edinburgh.

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