REVIEW Molecular Phylogenetics and the Perennial Problem of Homology S. Andrew Inkpen 1,2 • W. Ford Doolittle 1 Received: 17 September 2016 / Accepted: 12 November 2016 Ó Springer Science+Business Media New York 2016 Abstract The concept of homology has a long history, during much of which the issue has been how to reconcile similarity and common descent when these are not coex- tensive. Although thinking molecular phylogeneticists have learned not to say ‘‘percent homology,’’ the problems are deeper than that and unresolved. Keywords Homology Á Molecular phylogenetics Á Philosophy of biology Introduction What can be more curious than that the hand of a man, formed for grasping, that of a mole for digging, the leg of the horse, the paddle of the porpoise, and the wing of the bat, should all be constructed on the same pattern, and should include the same bones, in the same relative positions? (Darwin 1859, p. 434) Darwin’s answer, and ours today, is that these curious anatomical correspondences are instances of homology— the same characters in organisms of different species. Most would say that homologies are simply similarities of character that can be traced to common ancestry. But the concept of homology predates the theory of evolution and, perhaps because of this, although it is central to biology, its material definition and determination remain controversial (Hall 1994; Wake 1994, 1999; Wagner 2014). Molecular phylogeneticists sometimes talk as if their discipline has resolved these controversies: it has not. Homology Before Molecular Phylogenetics Homology as Archetype Although correspondences between characters of different species were noted by Aristotle, and frequently cited throughout the early modern period, the most explicit, precise early formulation of homology was given by nineteenth-century morphologist Richard Owen (Belon 1551; Owen 1843; Panchen 1994, 1999). Drawing on a long German Naturphilosophie tradition—in particular, the work of Johann Wolfgang von Goethe, Carl Gustav Carus, and Lorenz Oken—and the work of French anatomist Etienne Geoffroy Saint-Hilaire, Owen argued that the way to make sense of the limb structures referred to in our epigraph, for example, was to think of them as instances of a more general theme or, what Goethe called an ‘‘arche- type’’: in this case, the vertebrate limb (Owen 1848, 1849; Richards 1992). According to Owen, themes like this should be thought of as God’s plan for the production of different vertebrates. God intended that variants of these themes would be differently adapted to different environ- mental circumstances—the mole’s forearm for digging, the porpoise’s for swimming (Beatty 2006). So, according to Owen, homologous structures were those based on the same theme. And we explain the forms of organisms we find in nature through the investigation of these common themes. They are powerful explanatory devices. Owen defined homologs as ‘‘The same organ in different animals under every variety of form and function’’ (Owen & W. Ford Doolittle ford@dal.ca 1 Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, Canada 2 Department of Philosophy, Dalhousie University, Halifax, NS, Canada 123 J Mol Evol DOI 10.1007/s00239-016-9766-4