Introduction
While it is now accepted that nuclear and organelle DNA provide the main source of heritable information in living organisms, additional extranuclear sources of information have been recognised.1 This paper speculates on the properties and evolution of one of these alternative forms: information transmitted over generations by general causal cycles. To begin, a criterion for heritable information will be considered, followed by a brief review of known sources of heritable information.
An experimentally useful criterion is that heritable information exists for any attribute of a living organism in which a change can be inherited in the absence of its cause. Structural changes in germline DNA can be passed to future generations and thus fulfil the criterion: most externally caused phenotypic changes clearly do not. The qualification in the criterion concerning the absence of cause excludes changes confounded with environmental correlation between relatives and is of crucial importance in experimental attempts to demonstrate the inheritance of acquired characters. The criterion has a defect in that it excludes certain attributes against common sense, e.g. DNA sequences in which only dominant lethal changes can occur. An appeal to analogy might however be made in such situations.
Nucleic acid is an ideal hereditary material both for stability of information storage and ease of duplication and repair. From the viewpoint of information theory2,3 biological organisms are exceedingly complex and perhaps only nucleic acid can store efficiently the required large quantities of information. This may be true for molecular coding but morphological differences as between species may be achieved by simple transformations of scale4 and little information may be required to direct early egg development.5 It is also difficult to sustain the argument that efficient storage is important when much DNA in higher organisms is non-coding.
An advantage of molecular information storage is the resistance provided against thermodynamic decay.6 Heritable information could however be stored in any phenotypic attribute for example in the activity of molecules in a cell or the numbers or sizes of cells or organs provided that mechanisms exist for duplication and transmission. In fact the effects of polyploidy are the result of an inherited change in number of chromosomes rather than molecular structure.
Evidence now exists for evolutionary important types of heritable nucleic acid change other than those of base substitution, rearrangement and ploidy changes. Gene conversion and unequal crossing over, for example, may be important not only in the concerted evolution of multigene families but also in speciation and phenotypic trends.7 Another mechanism involving the capture of mRNA by endogenous RNA viruses followed by transfer of the information to germ line DNA after reverse transcription has been proposed to explain the inheritance of acquired immunological tolerance.8 This mechanism was extended as a general theory of evolution in which clonal selection and amplification of particular genes and mRNA species precedes transfer of the amplified information to the germ line.9 The theory, permitting inheritance of acquired adaptations, has however not been well corroborated even in the special case of immunological tolerance.10 It does involve transient information storage in numbers of particular cell types and RNA species before fixation in the structure of germline DNA.
Examples of heritable information storage in structure other than nucleic acid include the inheritance of changes in the cortex of Paramecium aurelia11 and other ciliates and in the cell wall of Bacillus subtilis.12 Phenomena similar to those observed in ciliates may also occur in the cortex of eggs.13 Evidence of information storage in molecular activity or concentration rather than structure include induction phenomena such as the galactosidase permease system in E. coli14 where either of two alternative stable steady states may be inherited to an extent independently of external inducer concentration. Mathematical analysis demonstrates that these properties can be explained by feedback systems.15,16 Other inherited phenomena which may involve feedback mechanisms or stable association of macromolecules with germline DNA include serotype transformation in Paramecium,17 environmentally induced changes in flax18 and tobacco,19 inheritance of the scrapie agent20 and extinction phenomena in rotifers.21 It must be emphasised that by the criterion of heritable information the alternative states of an operon system store information in addition to that stored in the nucleic acid sequences involved in the feedback circuitry.