Classification and Non-Trees

In spite its role as a ‘central metaphor’ and two decades of effort to promote ‘tree-thinking’, evolutionary relationships are now being portrayed in ways other than the simple bifurcating tree, recent examples being the ‘ring of life’ (Rivera & Lake 2004), the interlinking, anastomosing networks of major eukaryote groups (Doolittle 1999, 2000, Doolittle & Bapteste 2007, for commentary see Arnold 2007, Lane & Archibald 2008, McInerney et al. 2008, Dagan & Martin 2006), interconnecting networks relating various taxa (Hertel et al. 2006), and so on, the idea being summarised in a recent New Scientist article “Why Darwin was wrong about the tree of life”.

Most of this recent batch of non-trees have resulted from analysis of molecular data, although the general argument – if biological classification is hierarchical, then it prevents the representation of ‘real’ reticulate patterns – was explored in a cladistic context some three decades ago (Bremer & Wanntorp 1979).
Significance (or explanation) for many of these molecular diagrams is offered via the process of Lateral (or Horizontal) Gene Transfer (LGT, HGT), the horizontal transfer of a gene or genetic material from one organism to another, distantly related organism (Dagan & Martin 2006), first outlined some years ago to support the theory of serial endosymbiosis (Margulis 1998) to explain the origin of chloroplasts and mitochrondria (see Journal of Phycology 44 (1) and Lane & Archibald 2008). LGT is a mechanism to explain instances of xenology (“foreign genes”, Gray and Fitch 1983, p. 64), “a form of homology (inferred common ancestry) in which the sequence (gene) homology is incongruent with that of the organisms carrying the gene, and horizontal gene transfer or transfection is the assumed cause” (Patterson 1988, p. 612). Xenology finds its closest morphological equivalent in parallelism, a term which remains hard to define but can be simplified by associating it with incongruent homologies (similarities); xenology finds its biogeographical equivalent in dispersal, a term equally hard to define but simply suggests incongruent distributions (Williams & Embley 1996, pp. 581—582). Parallelism (Arendt & Reznick 2008) and dispersal (Queiroz 2005) are being discussed again, within the fresh gloss provided by molecular data, although interpretations of parallelism never really disappeared (Roth 1984:14; Sluys 1989; Wagner 1989:55, 66; Brooks 1996; DeSalle et al. 1996; Gould 2002), with suggestions being made such as “the significance of this similarity [parallelism] is thus dependent on the existence of a relevant underlying process” (Sanderson and Hufford 1996:328). Even earlier, Simpson wrote:

“In the most restricted sense virtually all evolution involves parallelism. Homologous genes tend to mutate in the same way (p. 9)… Homology is always valid evidence of affinity. Parallelism is less direct and reliable, but it is also valid evidence within somewhat broader limits. It may lead to overestimates of degree of affinity, but it is not likely to induce belief in wholly false affinity (p. 10)” (Simpson 1945, pp. 9—10).

Simpson’s words turned out not to be so, for the parallelisms he noted simply mislead determination of exact relationships among mammals (McKenna & Bell 1997): those similarities identified as parallelisms (like xenology and dispersal) are simply incongruent characters.
All the same, it has been argued that reticulate networks allow incongruent ‘homologies’ to be accommodated on the same diagram relative to congruent homologies (Huson & Bryant 2006). The general idea seems similar to that explored by William Sharp Macleay and his circular systems: an attempt to represent what he called analogies and affinities (homologies) in one system (Macleay 1819, Fig. 6).

Yet if even orthologous (homologous) genes do not support ‘tree-thinking’ (Bapteste et al. 2005), incongruence among gene-trees presents problems for the effectiveness of these data, rather than provide alternative explanations for incongruence (LGT = parallelism=dispersal). Simply put: Cladograms deal with character distributions and their implications for taxon relationships (classifications), rather than vehicles for explaining incongruence.

References

Arnold, M. 2007. Evolution through Genetic Exchange, Oxford University Press, Oxford.
Arendt, J. & Resnick, D. 2008. Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends in Ecology & Evolution 23: 26—32.
Bapteste, E., Susko, E., Leigh, J., MacLeod, D., Charlebois, R.L. & Doolittle, W.F. 2005. Do orthologous gene phylogenies really support tree-thinking? BMC Evolutionary Biology, 5:33; doi:10.1186/1471-2148-5-33.
Bremer, K. & Wanntorp, H.-E. 1979. Hierarchy and reticulation in systematics. Systematic Zoology 28: 624—627.
Brooks, D. R. 1996. Explanation of homoplasy at different levels of biological organisation. In M.J. Sanderson and L. Hufford (eds) Homoplasy. The Recurrence of Similarity in Evolution, pp. 3—36. San Diego: Academic Press.
Dagan, T. & Martin, W. 2006. The tree of one percent. Genome Biology 7: 118.1—118.7.
DeSalle, R., Agosti, D., Whiting, M., Perez-Sweeney, B., Renson, J., Baker, R., Bonacum, J. & Bang, R. 1996. Cross-roads, milestones, and landmarks in insect development and evolution: Implications for systematics. Aliso 14:305—21.
Doolittle, W.F. 1999. Phylogenetic classification and the universal tree. Science 284: 2124—2128.
Doolittle, W.F. 2000. Uprooting the tree of life. Scientific American, Feb. 2000: 90—95.
Doolittle, W. F. & Bapteste, E. 2007. Pattern pluralism and the Tree of Life hypothesis. PNAS 104:2043—2049.
Gould, S.J. 2002. The Structure of Evolutionary Theory. Cambridge MA: Harvard Univ. Press.
Gray G.S. & Fitch, W.M. 1983. Evolution of antibiotic resistance genes: the DNA sequence of a kanamycin resistance gene from Staphylococcus aureus. Mol. Biol.Evol. 1: 57–66.
Hertel, J., Lindemeyer, M., Missal, K., Fried, C., Tanzer, A., Flamm, C., Hofacker, I.L., Stadler, P.F. and the Students of Bioinformatics Computer Labs 2004 and 2005. 2006. The expansion of the metazoan microRNA repertoire. BMC Genomics 2006, 7:25.
Huson D.H. & Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology & Evolution 23:254—67.
Lane, C.E. & Archibald, J.M. 2008. The eukaryotic tree of life: Endosymbiosis takes its TOL. Trends in Ecology and Evolution 23: 268—275.
Margulis, Lynn. 1998. Symbiotic Planet: A New Look at Evolution. New York: Basic Books.
McInerney, J.O., Cotton, J.A. & Pisani, D. 2008. The prokaryotic tree of life: Past, present...and future? Trends in Ecology and Evolution 23: 276—281.
McKenna, M.C. & Bell, S.K. 1997. [with contributions from G. G. Simpson et al.]. Classification of mammals above the species level. New York: Columbia University Press.
MacLeay, W.S. 1819—1821. Horae entomologicae: or Essays on the Annulose Animals, &c. Vol. 1, Pt. 1 & 2. S. Bagster, London.
Patterson, C. 1988. Homology in classical and molecular biology. Molecular Biology and Evolution 5: 603—625.
Rivera, M.C. & Lake, J.A. 2004. The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature (9th September 2004) 431: 152—155.
Roth, V. 1984. On homology. Biological Journal of the Linnean Society 22:13—29.
Sanderson, M.J. and Hufford, L. (eds) 1996. Homoplasy. The Recurrence of Similarity in Evolution, San Diego: Academic Press.
Simpson, G. G. 1945. The principles of classification and a classification of mammals. Bulletin of the American Museum of Natural History 85:1-350.
Sluys, R. 1989. Rampant parallelism: An appraisal of the use of nonuniversal derived character states in phylogenetic reconstruction. Systematic Zoology 38:350—70.
Wagner, G.P. 1989. The Biological Homology Concept. Annual Review of Ecology and Systematics 20: 51—69; doi:10.1146/annurev.es.20.110189.000411
Williams, DM. & Embley, TM. 1996. Microbial Diversity. Annual Review of Ecology and Systematics 27: 569-595.