Phyletic phenocopies: a useful technique for probing the genetic and developmental basis of evolutionary change

Recent research on different molecules and structures that are evolving simultaneously in the same evolutionary line has shown that mosaic evolution (DeBeer, 1954) is commonplace. Evolution of some parts of the organism may be rapid and strongly influenced by natural selection, while other structures and molecules may evolve at a more leisurely, even pace and be little influenced by adaptation and selection; or the evolving difference may be nearly or quite neutral, being governed largely by stochastic processes (Wilson et al., 1974; Stebbins, 1983). In Metazoa and Metaphyta, visible evolution that can be followed in the fossil record or deduced by comparing related living species appears to be more strongly influenced by environmental change than is most evolution at the molecular or cellular level. Moreover, visible differentiation, at least at the level of species and genera, is probably brought about by the establishment of mutations that involve a relatively small number of genes, perhaps not more than 1 to 5 percent of the genotype (Gottlieb, 1984; Stebbins and Ayala, 1985). Consequently, the genetic basis of visible evolution will be greatly clarified if investigators can identify both the primary gene products that promote visible differentiation and the genes that carry information for these products. Two avenues of approach to this problem are possible. One is to identify mutations that produce effects similar to differences between extant taxa or between successive morphs in a fossil series and to study the nature of these mutations with respect to both altered information and altered pathways of development. Although many mutations of this kind are known in a variety of organisms (Redei, 1982), they have proved to be difficult to analyze, even by the use of modern molecular techniques. The most promising material for this kind of analysis is in lower plants and the simpler unicellular eukaryotes, in which sequences of development are relatively simple. Two examples, reviewed by Kuhn (1971), deserve particular attention. One is the liverwort Marchantia, in which a "progressive" type of mutation was recognized by Burgeff. The other is the flagellated phytomonad Dunaliella, in which different species are distinguished from each other simultaneously by visible characteristics (cell size and shape) plus an invisible one, variation in frequency of cell divisions as related to NaCl content ofthe medium. The second approach is the recognition or production of alterations that are here designated as phyletic phenocopies. We propose this term for changes in form or physiological response that mimic the normal form or reaction of a related phenotype, particularly one belonging to a different taxon. Using them, investigators have obtained clues to the developmental basis of evolutionary change, and occasionally to the nature and action of the genes involved. The most spectacular example is that of Kollar and Fisher (1979), who showed that epithelial tissue of chicken may be induced to differentiate rudimentary teeth under the influence of dental papilla tissue from a mouse. During the approximately 100 million years since ancestral birds had teeth, some of the genes coding for them have persisted, even though the cellular and histological environment of bird embryos inhibits their expression. Less spectacular, but no less significant, are findings that plants as evolutionarily diverse as leafy liverwort gametophytes and flowering plant sporophytes can manifest developmental capacities thought to have been "lost" (as were "hen's teeth") during the course of their evolutionary history (for reviews see Basile, 1969, 1974; Basile and Basile, 1984; Rosenblum and Basile, 1984). In every case, the species studied could be induced to p enocopy morphological features of other, extant taxa that are widely considered by morphologists to be more primitive and/or ancestral. For example, five species of leafy liverworts in which the normal genotype has a ?/2 phyllotaxy and dorsiventral symmetry were experimentally induced to express a phenotype of 1/3 phyllotaxy and radial symmetry that, in most cases, is not normally expressed either in the genera or the families to which the species belong. The induced phenotype is, however, characteristic of other taxa considered to be more primitive and is probably the ancestral condition for all leafy liverworts (Fulford, 1965; Schuster, 1966). Likewise, modes of branching characteristic of many genotypes among extant leafy