Abstract
Owen's pre-evolutionary definition of a homolog as “the same organ in different animals under every variety of form and function” and its redefinition after Darwin as “the same trait in different lineages due to common ancestry” entail the same heuristic problem: how to establish “sameness.”Although different criteria for homology often conflict, there is currently a generalized acceptance of gene expression as the best criterion. This gene-centered view of homology results from a reductionist and preformationist concept of living beings. Here, we adopt an alternative organismic-epigenetic viewpoint, and conceive living beings as systems whose identity is given by the dynamic interactions between their components at their multiple levels of composition. We posit that there cannot be an absolute homology criterion, and instead, homology should be inferred from comparisons at the levels and developmental stages where the delimitation of the compared trait lies. In this line, we argue that neural connectivity, i.e., the hodological criterion, should prevail in the determination of homologies between brain supra-cellular structures, such as the vertebrate pallium.
Highlights
The Problem of HomologyThe concept of homology has long been implicitly used by biologists, as comparison has been the basis of our classification of the natural world at least since Aristotle (Russell, 1916; Nordenskiold, 1928)
The study of structural correspondence moved to the foreground (Russell, 1916; Coleman, 1971) in the first half of the nineteenth century, when biology emerged as an independent science and morphology became its core discipline
Why does developmental genetics face such hindrances when attempting to provide an absolute criterion for homology? We believe this to be the consequence of one of the most prominent characteristics of living beings: they are dynamic systems organized into multiple levels (Jacob, 1970; Mayr, 1982)
Summary
The concept of homology has long been implicitly used by biologists, as comparison has been the basis of our classification of the natural world at least since Aristotle (Russell, 1916; Nordenskiold, 1928). According to Cuvier, every animal followed the body plan of one of the four embranchements of the animal kingdom: vertebrata, mollusca, articulata, and radiata (Cuvier et al, 1817) With his loi des connections (law of connections), according to which the connections held between homologous organs in different animals remain constant, Saint-Hilaire established various homologies between vertebrates and invertebrates, which resulted in the indignation of Cuvier. One of his audacious proposals was that the body plan of a lobster, an articulata, was the same as that of a vertebrata, only with its dorsoventral axis inverted (Saint-Hilaire, 1998 [1822]). Could we confidently ascertain as homologs any neural and digestive systems that are specified by the same early developmental mechanism? Neither, since common developmental mechanisms can generate different structures
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