Intraorganismal genetic heterogeneity: is it a useful concept?
Version of Record online: 15 SEP 2004
Journal of Evolutionary Biology
Volume 17, Issue 6, pages 1180–1181, November 2004
How to Cite
Pannell, J. R. and Eppley, S. M. (2004), Intraorganismal genetic heterogeneity: is it a useful concept?. Journal of Evolutionary Biology, 17: 1180–1181. doi: 10.1111/j.1420-9101.2004.00810.x
- Issue online: 15 SEP 2004
- Version of Record online: 15 SEP 2004
It is well known that plants, among an assortment of diverse taxa (Buss, 1987), have turned a deaf ear to the Weissmannian insistence on a need to distinguish between germ line and soma. Although their populations yield to the same fundamental evolutionary forces as those of vertebrate species, the absence of a germ line in plants nonetheless may have important evolutionary consequences. For example, vegetative spread allows genetic individuals to forage for resources far from their initial growth points (Cain et al., 1996), while avoiding evolutionary death by fragmentation. Indeed, fragmentation may itself often serve as a strategic mode of reproduction for such organisms. The fundamental modularity of organismal structure and growth, predicated upon the lack of a germ line, may thus influence the evolution of life history and reproductive strategies.
In their review, Pineda-Krch & Lehtilä (2004) consider another potential consequence of plant modularity, i.e. the possibility that somatic mutations in organisms without a germ line will be passed on to subsequent generations. Theoretical analyses of the evolutionary fate of such mutations indicate that they may indeed be important (Antolin & Strobeck, 1985; Slatkin, 1985; Otto & Orive, 1995; Orive, 2001). On the one hand, the increased probability of fixation of beneficial somatic mutations, predicted under certain circumstances, has obvious implications for rates of adaptation. On the other hand, deleterious somatic mutations may be evolutionarily important if they augment the genetic load of a population. For example, we expect the evolutionary stability of outcrossing in plants to depend strongly on the genetic load, and the accumulation of somatic mutations in long-lived plants might thus explain their relatively high levels of inbreeding depression and low selfing rates compared with more ephemeral plants (Morgan, 2001).
Given the potential evolutionary importance of somatic mutations in modular organisms, it would be useful to know their frequency and fitness effects, both in terms of their differential spread within an individual as well as within a population. Unfortunately, Pineda-Krch & Lehtilä (2004) fail to bring these significant issues into clear focus. The basic difficulty is that they consider somatic mutations in the broader context of intraorganismal heterogeneity (IGH), which may be the outcome of two very different processes: the spread within an organism of somatic mutations, giving rise to ‘genetic mosaics’; and the coalescence of two or more genetically distinct individuals, producing ‘genetic chimeras’. By addressing chimeras and mosaics together as causes of the more general IGH, the appropriate theoretical context is blurred; nor is an assessment of the overall frequency of IGH very meaningful. The term IGH is as useful for evolutionary analysis as the name of a paraphyletic group is for systematics; both concepts define membership in terms of characteristics that provide little evolutionary insight. Our first point, therefore, is that IGH ought to be rejected as a unifying concept.
Our second point concerns the evolutionary significance of chimeras, as circumscribed by Pineda-Krch & Lehtilä (2004). Although there are good theoretical reasons for paying attention to somatic mutations and the resulting genetic mosaics, we believe that a convincing case for the significance of chimeras, in any coherent sense, has not been made. Pineda-Krch & Lehtilä (2004) review a variety of ways in which chimeras can be formed, and each case may indeed be evolutionarily significant – although for idiosyncratic reasons. The potential costs and benefits of multiclonal chimeras have been clearly demonstrated in slime moulds (e.g. Foster et al., 2002), and may generally be understood in terms of the evolution of cooperation. However, such examples can hardly be analysed in the same light as the apparent fusion of strangler figs (cited by Pineda-Krch & Lehtilä, 2004), which happen to have set upon the same host, and whose chimeric appearance is the outcome of the difficulty botanists face in distinguishing one genetic individual from another. The fact that the peculiar growth habit of climbing plants predisposes them to intermingle will almost certainly alter the nature of competition and their pollination biology in important ways, but it is not useful to consider these questions in the same terms as the advantages of cooperation in chimeric amoebae.
Finally, it is tempting to note that a literature search on the word ‘coalescence’ will unearth papers on two quite different topics of biological interest. The first concerns the coalescence of genetically distinct individuals into a chimera (somatic fusion, as reviewed by Pineda-Krch & Lehtilä, 2004). The second concerns the coalescence of genetic lineages as one follows them backwards in time towards their common ancestors (coalescent theory; reviewed by Nordborg, 2001). These two areas of biology are of course conceptually poles apart, but their common nomenclature brings into ironically clear focus the importance of distinguishing between mosaics and chimeras. The absence of a germ line in modular organisms means that genetic lineages with independent evolutionary futures may, if we look back in time, ‘coalesce’ at their common ancestors within the soma of an ephemeral individual, which might be a mosaic of lineages separated by somatic mutations. The irony is that, whereas somatic mosaics fit neatly into the edifice of coalescent theory, with its strong conceptual framework, the coalescence of lineages in the formation of a chimera does not.
We thank the National Science Foundation, USA, for financial support to S.M.E. (NSF grant INT 02 02645).
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