The case for epigenetic inheritance in evolution

It is commonly thought that genotype is a property assignable exclusively to the nucleic acid genome while phenotype is a property whose assignment must be distributed among entities at many or all levels of biological organization. In evolutionary biology there is a problem of hierarchy in the theory of selection due to this requirement for distributive assignment: to which level(s) is the cause of a particular selective effect to be assigned? There appears to be no comparable perceived problem for theories of inheritance due to the asymmetry of genotype and phenotype. One might argue to the contrary that the genome has an architecture and that linkage, recombination, and gene interaction all point to a hierarchical structure ranging from nucleotides-as-units up to the genome as a whole (Lewontin, 1974). But this hierarchy presents no comparable problem because all of these genomic elements are part of a single inheritance system. The transmission rules used to track nucleotides are the same ones used to track larger genomic elements. In the narrowest sense, then, genotype means DNA (or RNA) sequence. Phenotypes are various, embodying all the morphologies, physiologies, and behaviors of living things. As such, phenotypes are the direct targets or subjects of natural selection and genotypes are the direct subjects of inheritance. However, the evolution of phenotypes depends not only on selection but also on their relation to genotypes that can be transmitted (or reconstituted) in inheritance. Selection without an appropriate genotype-phenotype relation does not result in an evolutionary response. Evolution by natural selection depends on inheritance and selection in equal measures. Belief that the asymmetry of genotype and phenotype is fundamental is reinforced by the fact that the mechanism of nucleic acid-based heredity is so well understood and provides such an exquisite explanation of the genotype-phenotype mapping. Although much is unknown about the details of the ‘‘epi-genetic’’ mapping beyond the primary coding of amino acid sequence, no other known