Molecular pathways to parallel evolution: I. Gene nexuses and their morphological correlates

Abstract

Aspects of the regulatory interactions among genes are probably as old as most genes are themselves. Correspondingly, similar predispositions to changes in such interactions must have existed for long evolutionary periods. Features of the structure and the evolution of the system of gene regulation furnish the background necessary for a molecular understanding of parallel evolution. Patently "unrelated" organs, such as the fat body of a fly and the liver of a mammal, can exhibit fractional homology, a fraction expected to become subject to quantitation. This also seems to hold for different organs in the same organism, such as wings and legs of a fly. In informational macromolecules, on the other hand, homology is indeed all or none. In the quite different case of organs, analogy is expected usually to represent attenuated homology. Many instances of putative convergence are likely to turn out to be predominantly parallel evolution, presumably including the case of the vertebrate and cephalopod eyes. Homology in morphological features reflects a similarity in networks of active genes. Similar nexuses of active genes can be established in cells of different embryological origins. Thus, parallel development can be considered a counterpart to parallel evolution. Specific macromolecular interactions leading to the regulation of the c-fos gene are given as an example of a "controller node" defined as a regulatory unit. Quantitative changes in gene control are distinguished from relational changes, and frequent parallelism in quantitative changes is noted in Drosophila enzymes. Evolutionary reversions in quantitative gene expression are also expected. The evolution of relational patterns is attributed to several distinct mechanisms, notably the shuffling of protein domains. The growth of such patterns may in part be brought about by a particular process of compensation for "controller gene diseases," a process that would spontaneously tend to lead to increased regulatory and organismal complexity. Despite the inferred increase in gene interaction complexity, whose course over evolutionary time is unknown, the number of homology groups for the functional and structural protein units designated as domains has probably remained rather constant, even as, in some of its branches, evolution moved toward "higher" organisms. In connection with this process, the question is raised of parallel evolution within the purview of activating and repressing master switches and in regard to the number of levels into which the hierarchies of genic master switches will eventually be resolved.