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Over the last two decades intraorganismal genetic heterogeneity (IGH) has been regularly invoked, usually under the guise of the genetic mosaic hypothesis (GMH), as a basis upon which selection may act. It has been especially prominent in the literature on modular and clonal plants (e.g. Whitham & Slobodchikoff, 1981; Gill & Halverson, 1984; Silander, 1985; Gill et al., 1995). IGH has now come in for another airing by Pineda-Krch & Lehtilä (2004), who review its potential costs and benefits.

We believe that their review has two fundamental problems. The first is the issue of individuality. Pineda-Krch and Lehtilä are aware of this problem, stating that ‘individuality is lacking a clear definition’. We believe that the real problem is that any one definition of individuality can have only limited applicability across different types of organism, and that several forms of individuality can be recognized within some types of organism. This immediately undermines simple comparisons between organisms as dissimilar as, for example, unitary and modular organisms, or slime moulds and clonal plants. Tuomi & Vuorisalo (1989) have provided one of the best analyses of the complexity of individuality as a concept. If their categories of individuality are accepted, many modular organisms exhibit individuality on at least three different structural levels. For example, individuality in clonal plants can be recognized at the levels of developmental individuals (all products of a single zygote or other single cell stage), genetical individuals (genetically uniform material within a developmental individual), and functional or physiological individuals (material interacting as a cohesive whole in response to the environment). We could also recognize structural individuals (physically continuous structures, including clonal fragments of various sizes even down to single modules or ramets that have the potential to be independent). Costs and benefits of IGH could, in theory, be calculated for individuals defined at most of these levels, but the balance between these costs and benefits would be different in each case. For genetical individuals, the total absence of IGH would actually preclude such calculations.

The second problem is that whereas methodological advances have made it easy to identify extremely small differences between the genetical properties of different parts of the same organism, demonstrations that these differences form a basis either for adaptation or for generating measurable costs and benefits to the individual, however defined, are still largely lacking, at least in modular plants. Despite its plausibility, the lack of progress in the last 20 years in accumulating evidence about the adaptive significance of IGH begins to suggest that the hypothesis may not be sustainable. As Harper (1988) pointed out forcefully, there is too much willingness (shown by the repeated reviews of the potential importance of IGH in the literature) to accept the hypothesis without supporting data. Little seems to have changed since Harper's cautionary comments. There are considerable difficulties in moving from identification of IGH as a phenomenon to demonstration of its significance in an ecological or evolutionary context. Ideally, such a demonstration would be made under field conditions, but very stringent conditions would be required to demonstrate unequivocally that IGH itself is responsible for differences in module proliferation rates or differences in fitness. The fact is that the links between specific cases of IGH, and appropriate measurements and experiments to demonstrate their adaptive qualities, have not been made. Moreover, several of the sources cited by Pineda-Krch and Lehtilä to illustrate the adaptive role of IGH cannot be used in this way. For example, despite claiming the ‘first direct evidence of an adaptive role for genetic variation within plants’, Edwards et al. (1990) only inferred such a role. They provided no direct evidence of genetical differences between those branches on single trees of Eucalyptus melliodora that were defoliated or avoided by herbivores. Dawson & Bliss (1993) recorded high levels of intra-plant physiological variation in Salix arctica, but evidence to show that differences in genotype were responsible was neither presented nor claimed. Notoriously, an earlier study that has been widely cited as amongst the strongest evidence of IGH causing different levels of herbivore damage between branches, carried out on Hamamelis virginiana, was later refuted by the original authors when different explanations came to light (Gill et al., 1995). In summary, although modular organisms may well be predisposed ‘towards becoming genetically heterogeneous over time’ (Pineda-Krch & Lehtilä, 2004), there is still very little evidence that genotypic heterogeneity is an important factor in the adaptive response repertoire of modular plants. We do not dispute that it may be, but science should proceed by gathering sufficient evidence to support hypotheses before those hypotheses are accepted. Repeatedly with IGH, proponents accept the hypothesis without ample evidence being available. Until such evidence is available, proposals for analysis of the evolutionary costs and benefits of IGH are premature.

There are several potentially misleading assumptions and simplifications in Pineda-Krch and Lehtilä's views about the behaviour of modular organisms, at least as far as plants are concerned. For example, they state that ‘In modular organisms, the open-ended development with a low degree of integration allows advantageous lineages to be selected through intraorganismal selection’. The comment about selection of different lineages might be true if integration was always low, but the details are more complicated than this. Here again we encounter the problem of individuality. Many modular organisms exhibit strong integration at least at some structural levels [the functional or physiological individual (Tuomi & Vuorisalo, 1989) or the ‘integrated physiological unit’ or IPU (Watson & Casper, 1984)], but little integration between such substructural levels. Within these levels of organization there is evidence of integration, coordination and cooperation, even including division of labour (Marshall, 1990; Price et al., 1992; Alpert & Stuefer, 1997). Coordination within physiologically integrated parts of modular plants can avoid the tragedy of the commons scenario referred to by Pineda-Krch and Lehtilä: in situations where different plants, or different physiological individuals might display evidence of conflict (Gersani et al., 2001), physiologically integrated parts of the same plant exhibit much more restrained interactions (Falik et al., 2003). In addition, Pineda-Krch and Lehtilä state that ‘several genetically distinct lineages interact so that their combined phenotype is different from the sum of their separate phenotypes, a novel phenotype emerges – the phenotype of the individual cannot simply be derived from the phenotype of its component lineages’. This does not apply to modular plants. (The term ‘individual’ as used in this passage by Pineda-Krch and Lehtilä could have a number of alternative interpretations!) From what we know of modular plants, they display neither an average phenotype throughout the organism nor phenotypes with novel properties (e.g. Slade & Hutchings, 1987). This is partly because many resources and signals travel acropetally (i.e. from more basal parts of the plant's structure towards growing tips) and partly because autonomy or semi-autonomy of physiological individuals permits local adaptation through phenotypic plasticity. This tendency to develop localized phenotypic differences, rather than an average or novel phenotype, enhances performance in heterogeneous environments at all levels of individuality. Thus, each physiological individual can produce a phenotype that both depends on local conditions and may differ from that of other connected physiological individuals. Moreover, if conditions are variable at scales smaller than that of the physiological individual there will also be phenotypic variation within the physiological individual.

In conclusion, Pineda-Krch and Lehtilä's discussion of the costs and benefits of IGH is in our opinion premature, because supporting evidence for IGH as a basis upon which selection may act is still too scarce. Their review also appears flawed, at least with respect to modular plants, because several issues are not represented accurately enough. The forerunner of IGH – the GMH – was criticized by Harper (1988) for lack of evidence to support its beguiling plausibility. Harper's criticism may have been somewhat answered by new findings since 1988, but we should still be wary of assuming that IGH provides variation upon which selection acts. Harper cited Schaal (1988), who had documented extensive somatic mutation in Solidago canadensis and Brassica campestris. Her conclusion was cautious: ‘whether this somatic variation is inherited and enters into the gene pool remains to be determined…. The significance of these processes in population biology is yet to be determined.’ Harper described several cases where the differences between modules of the same plant did not have genetic causes. Since then there have been many more demonstrations of this than of cases where IGH contributes to evolution. As Harper concluded, ‘The extent of our ignorance is not easily mapped if exciting ideas are rapidly assimilated into a body of literature before they have become more than ideas or hypotheses’.

References

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  2. References
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