Stepping into the same river twice: homologues as recurring attractors in epigenetic landscapes

The reunification of embryology with evolutionary biology is impeded by the perception that a phylogenetic view of homology is incompatible with a developmental approach. This dichotomy disappears when developmental information is viewed not as pre-existing within the zygote but as being constructed during development. Developmental information can be depicted as the surface of an epigenetic landscape. An epigenetic landscape, in turn, can be viewed as a series of aligned energy landscapes that change shape and become more complex as development proceeds. In this view, individual valley bottoms are attractors in state space that tend to reappear reliably in successive generations. Phylogeny can therefore be conceptualized as a succession of epigenetic landscapes, and homologues can be identified as corresponding valleys that have reappeared reliably since their origin in a single ancestral population. Epigenetic homologues can be robust to phylogenetic changes in developmental mechanisms, precursors, and lower level characters. Although application of the epigenetic homology concept is complicated by the lack of explicit information about the topography of epigenetic landscapes, comparative biologists can learn to identify recurring ontogenetic patterns in a manner that is analogous to the identification of input patterns by attractor neural networks. The correspondence of epigenetic valleys is therefore not defined by any essential criteria but by their overlap in multidimensional state space. Whether corresponding valleys are homologous to each other must be determined by a phylogenetic analysis using cladistic methods. Among the general implications of epigenetic homology for comparative neurobiology is that the concept of 'field homology' should be used with caution when dealing with novel characters. A case study, applying an epigenetic perspective to understand the variation in monkey visual cortex observed after developmental perturbations, is presented in a final section to make the concept of epigenetic homology more concrete.