Clonal Senescence: Does the Genet Age? Ramet Mortality vs. Genetic Immortality

The early interpretations of senescence and most of the subsequent dogma are based on populations of age-structured, unitary, aclonal animals, i.e., situations in which an individual is obvious. The complications that arise where multiple and in many cases separate, physiologically independent subunits (modules operating at the level of ramets) constitute in aggregate one genetic entity (genet) warrant special comment (cf. Chap. 5). The clone is thus the uppermost organizational level in a hierarchy of units where one or multiple types of asexual reproduction at any lower level constitutes growth of the clone (whether intact or disaggregated), whereas sexual reproduction produces new clones (genets). As discussed in Chap. 5, clones arise in various ways such as by polyembryony, or by budding, fission, or fragmentation of the parental unit.

As discussed previously (Chaps. 2 and 5), most microbes are clonal, as are many plants (e.g., buttercup, clover) and animals (e.g., corals, anemones). While it is clear that senescence in all such organisms occurs at the level of the ramet, the key issue is whether it occurs also at the level of the genet. One must also be cautious in interpreting the literature as some authors take ‘the individual’ with respect to senescence to mean the physiologically independent ramet (e.g., Orive 1995), and others take it to be the entire clone or genet (Pedersen 1999). This is particularly important in the case of microorganisms (discussed in following subsection) where senescence at the ramet level is routinely misconstrued to imply clonal senescence. A second level of complexity is added where, as is commonly the case, clonal organisms are also reproducing sexually, i.e., producing new genets (clones) sexually as well as new ramets asexually (see Caswell 1985; Gardner and Mangel 1997).

Little can be said authoritatively about the full extent of clones in nature because their entirety has rarely been mapped exhaustively in the field by any method. With respect to animals, genets of clonal benthic invertebrates survive substantially longer than their constituent ramets (Cook 1985; Hughes and Cancino 1985; Hughes 2005), and fecundity and survivorship generally increase with size (of the physiological individual and, where known, of the genet; Jackson 1985). Sponges and corals, for instance, have been estimated at ages of from one to several centuries (Jackson 1985).

This has been taken by some authors to imply absence of senescence, but as noted above and in Fig. 6.6, longevity, in itself, is not evidence for or against senescence. With time, encrusting organisms may die locally, become subdivided, and thus come to exist as clonal fragments over an unknown area. Jackson’s review shows that sponges, hydrozoans, bryozoans, ascidians, and corals periodically degenerate (“regress”) locally, but regenerate from other areas and so may not senesce as a clone (Hughes 1989; Babcock 1991). This is in striking contrast to the rotifers, for example, where the zygote produces a species-specific number of cells after which subsequent cell division ceases (Buss 1985), the powers of regeneration are negligible, and senescence is well documented (Bell 1984; Chap. 2 in Comfort 1979).

With respect to plants, the shoot and ramet dynamics of many clonal perennials such as clover or woodland violets, noted above under ‘Plants’, are well known (Harper 1977; Cook 1983, 1985; Sackville Hamilton and Harper 1989; Roach 1993). Localized death, i.e., at the ramet level, may not decrease survival probabilities of either aclonal or clonal iteroparous plants (Watkinson and White 1985; however see conclusions from theoretical studies, below). Watkinson and White attributed both the relative absence of senescence and “considerable longevity” of iteroparous plants to the capacity for continuous activity of their apical meristems. They concluded in part (p. 31) that ... “insofar as they retain the capacity for rejuvenescence from apical meristems, genets of modular organisms do not senesce” and that whereas the longevity of aclonal plants may be limited by the problems associated with large size or the accumulation of dead matter, “clonal plants are, in contrast, potentially immortal” (see caveats and discussion by Klimesova et al. 2015).

As discussed in Chap. 5, clones of Populus tremuloides (trembling aspen) in British Columbia were thoroughly mapped by Ally and colleagues in a molecular study involving microsatellite marker loci over several years. This species forms clones composed entirely of male or female ramets (trees), which can reproduce sexually (beginning at 10-20 years) and asexually (after 1 year). The clones are potentially extremely large, extending up to about 44 ha and arguably as old as one million years. In one aspect of this multifaceted study the issue of senescence was considered (Ally et al. 2010). They found a decline in sexual fitness (significant reduction in average number of viable pollen grains per catkin per ramet) with age. This implies that long-lived clones might senesce as a result of accumulating somatic mutations, possibly because the deleterious mutations are recessive and masked in the diploid condition but revealed in the haploid pollen. In other words selection on sexual fitness does not occur during clonal growth.

There was no strong correlation between male fertility and various measures of clonal fitness, hence no evidence, such as higher asexual fitness of ramets associated with lower sexual fitness, that would imply involvement of trade-offs (negative pleiotropy). Technically, the affected clones are senescing if one adopts the attribute of the definition pertaining to declining fertility; however, this is really a study in clonal longevity and there is no evidence for or against age-specific mortality at the genet level. The impaired sexual reproduction does threaten the population (sexual) lineage and eventually the rate of asexual clonal expansion also may be impeded locally by environmental constraints.

Numerous theoretical analyses of clonal senescence have appeared since the 1990s. Among the most detailed are those by Pedersen (1995, 1999) who modeled clonal dynamics where ramets increase by asexual reproduction and new genets (clones) are produced sexually. He found that as ramets and clones aged the force of natural selection declined. This implies that natural selection could not prevent accumulation of deleterious genes with time, or that there may be selection for genes conferring beneficial effects early on with deleterious effects later (negative pleiotropy; see evolutionary theories later). Thus, Pedersen inferred that clones will senesce and cannot escape senescence by asexual reproduction alone.

Sexual reproduction provides an escape by, in his terminology (1995, pp. 306-308), “resetting the clonal level age clock” (as well as the ramet age clock); hence parental effects do not accumulate over generations. Of course, sexual reproduction marks the end of a genet and the origin of a new genet in the zygote. Pedersen’s model is based on somewhat different assumptions than the earlier one by Caswell (1985) though their conclusions are in general accord. Caswell argued that clonality does not necessarily prevent senescence but that it may do so by altering the intensity of selection acting on the various stages of the life cycle.

Orive (1995) applied a model to the demographic data of Babcock (1991) on the life history of three Scleractinian corals. Babcock had argued that there was no evidence that the older corals in his study underwent physiological senescence, though their clonal expansion was probably ultimately limited by factors such as colony morphology and availability of favorable terrain. The youngest genets and smallest ramets had the highest mortality. Orive concludes that clonality by itself retards but does not preclude the evolution of senescence. Gardner and Mangel (1997) reach essentially the same conclusion while focusing on the trade-offs between clonal and sexual reproduction by the same individual.

The generality emerging from the clonal models is that clonality, though admittedly important, is but one factor among many in the life history of a macroorganism that determine whether senescence will evolve.