The Concept of Monophyly: A Speculative Essay

The concept of monophyly is central to much of modern biology. Despite many efforts over many years, important questions remain unanswered that relate both to the concept itself and to its various applications. This essay focuses primarily on four of these: i) Is it possible to define monophyly operationally, specifically with respect to both the structures of genomes and at the levels of the highest phylogenetic categories (kingdoms, phyla, classes)? ii) May the mosaic and chimeric structures of genomes be sufficiently important factors in phylogeny that situations exist in which the concept may not be applicable? iii) In the history of life on earth were there important groups of organisms that probably had polyphyletic, rather than monophyletic, origins? iv) Does the near universal search for monophyletic origins of clades lead, on occasion, to both undesirable narrowing of acceptable options for development of evolutionary scenarios and sometimes actual omission from consideration of less conventional types of both data and modes of thought, possibly at the expense of biological understanding? Three sections in the essay consider possible answers to these questions: i) A reassessment is made of major features of both the concept and some of its applications. Recent research results make it seem improbable that there could have been single basal forms for many of the highest categories of evolutionary differentiation (kingdoms, phyla, classes). The universal tree of life probably had many roots. Facts contributing to this perception include the phylogenetically widespread occurrences of: horizontal transfers of plasmids, viral genomes, and transposons; multiple genomic duplications; the existence and properties of large numbers of gene families and protein families; multiple symbioses; broad-scale hybridizations; and multiple homoplasys. Next, justifications are reassessed for the application of monophyletic frameworks to two major evolutionary developments usually interpreted as having been monophyletic: ii) the origins of life; and iii) the origins of the vertebrate tetrapods. For both cases polyphyletic hypotheses are suggested as more probable than monophyletic hypotheses. Major conclusions are, as answers to the four questions posed above: probably not, yes, yes, and yes.