1. Growth forms and theoretical expectations
A unique feature, distinguishing plants and animals is the indeterminate growth that takes place in the meristems of plants. Meristem organization may be an important factor determining variation in life span and mortality patterns of different species. Variation within the plant kingdom ranges from unitary organisms to clonal species. A plant species with a unitary organization and determinate growth is expected to follow demographic patterns similar to model animal systems such as Drosophila. On the other hand, plants with unitary organization and indeterminate growth, or clonal species with more modular construction, will have multiple meristems, and this can have important implications for population dynamics. Production of new meristems may allow a clonal species to escape determinacy and may facilitate an escape from whole organism senescence.
Historically, the demography of plants was considered to be relatively intractable because of this variation in growth forms, specifically because an "individual" is sometimes difficult to delineate. For unitary species, identification of an individual is not difficult and age- or size-specific mortality and reproduction are relatively easy to follow. For species with clonal growth, Harper (1977) introduced the term "genet" to refer to all individuals that were derived from the same zygote, and "ramet" as the modules of a genet, which may in some cases become severed from the parent plant and grow as independent individuals. As long as the birth rate of ramets exceeds the death rate, a genet will survive in the population. Ramet demography may, in some cases, act as a buffer for the dynamics of a genet. In a computer simulation based on several years of data from populations of Ranunculus repens, it was found that the decay rate of the genet can be buffered by the decay rate of the ramets, which has the effect of conserving genetic variability within the population (Soane and Watkinson, 1979).
To date, there have been no comparative studies of the demography of ramets and genets, thus it is not known whether the demography of a population of genetically identical ramets reflects the vigor of the genet. With respect to studies on evolutionary processes such as senescence, it is critical that demographic studies be made at the level of the genet (Silander, 1985). There is limited evidence showing variation in age-specific demography of genets. In a study of the pasture grasses Agrostis stolonifera and Lolium perenne, Bullock et al. (1996) showed tiller production for different-aged genets changed in response to grazing. The existence of extremely long-lived clones is often cited as evidence that some clonal species lack whole organism senescence (cf. Watkinson and White, 1985; Nooden and Guiamet, 1996; Gardner and Mangel, 1997). Unfortunately, given their extreme longevity, it may be impossible to get a true understanding of late-age dynamics. There is clearly a need for more comparative studies of the demography of genets and ramets.
Variation in growth forms within the plant kingdom may necessitate a reevaluation of some of the evolutionary theories of senescence. In particular, the assumption of the theories that a species shows age-specific gene expression may be violated. A genet which grows to consist of a collection of ramets of different ages, cannot be expected to show age-specific gene action, particularly if the ramets are detached from the parent plant and grow independently. There is evidence, however, from bamboo that independent ramets show synchronized genetic control of flowering time, but the nature of this internal genetic clock and its interaction with the environment is not known (John and Nadguada, 1999). Moreover, even without independent growth, the turnover of tissues within an individual may allow an escape from senescence. For example, in the forest herb Arisaema, old tissue is sloughed off from the bottom of corms as new tissue is added to the top so that no part of any plant, even one 20 years old, is ever really over 4 years old. If there is complete turnover of tissue within an individual, in other words if no tissue ever achieves a chronologically old age, then there may be no reason to expect evolutionary senescence or any increasing mortality with age (Bierzychudek, 1982).
A second assumption of the evolutionary theories of senescence, which requires further evaluation with respect to clonal species, is the assumption that the force of selection declines with increasing age. This issue has been addressed in several recent theoretical papers. An analysis by Gardner and Mangel (1997) suggests that it is the rate of sexual reproduction relative to vegetative growth that is the important determinate of the strength of selection. Higher rates of sexual reproduction and lower rates of clonal reproduction result in a more rapid drop in the strength of selection with clonal age following an initial peak [see also, Orive (1995) and Pedersen (1995)]. Experimental results by Bell (1984) with six asexual freshwater invertebrates support this generalization, but there have been no comparative studies with plants of the demography of closely related species with different rates of sexual reproduction and clonal growth.
Another important distinction between plant and animal development is the timing of the differentiation between germ and soma plasma. In mammals, insects, and many other animals, the germ cells are segregated early in development, whereas in plants, the germ line does not segregate from the soma until just before reproduction. It was theoretically suggested that senescence should be found to be inevitable for any organism for which there is an early segregation between germ and soma (Williams, 1957). This has led several researchers to predict that patterns of evolutionary senescence may not be the same in animals and plants
(cf. Kirkwood and Holliday, 1979; Rose, 1991). Yet, the reason why this segregation is necessary for the evolution of senescence has never been explicitly stated (Roach, 1993). Two scenarios are presented below, in which the presence of multiple meristems and the late separation of germ and soma may influence patterns of plant senescence.
Individual longevity may be affected if somatic mutations result in intraorganismal selection. In long-lived plants with multiple meristems, a genetic mosaic may develop within individual plants, and this may have one of two consequences. On the one hand, intraorgan-ismal selection has primarily been seen as a mechanism for eliminating deleterious somatic mutations (cf. Klekowski and Kazarinova-Fukshansky, 1984; Otto and Orive, 1995). Natural selection can act among cells within an individual to eliminate deleterious mutations that appear in a ramet or module, with little or no impact on the fitness of the genet. Conversely, selection may allow the spread of a favorable mutation within a clonal plant, which may result in an evolutionary change if an advantageous mutation goes to fixation (Pineda-Krch and Fagerstrom, 1999). If somatic mutations occur at a level high enough to allow selective changes within the life span of an individual, then this could allow for a closer tracking of an individual with its environment thus potentially resulting in increased longevity. A recent stochastic model demonstrates that there is a high probability of an advantageous somatic mutation going to fixation through a mitotic cell lineage in the presence of intraorganismal selection (Pineda-Krch and Fagerstrom, 1999). Genetically different individuals may thus originate through a succession of chimeric ramet generations without sexual reproduction (Fagerstrom et al, 1998). The genetic mosaic within an individual may be evolutionar-ily important, particularly as a defense against rapidly evolving pathogens, parasites, and herbivores (Whitham and Slobodchikoff, 1981). Recent work on genetic polymorphism within the chloroplast genome in Senecio vulgaris has shown that there can be within-plant selection between different DNA chloroplast types (Frey, 1999). Additionally, work with Chenopodium album (Darmency, 1994) suggests that within-individual selection may be an important mechanism for the development of within-generation resistance to herbicides. With respect to the evolution of senescence, the important factor is whether or not there are some species which can escape senescence because intraorganismal selection allows individual genotypes to increase their longevity by becoming more "fine-tuned" to their environment over time. The evolutionary importance of intraorganismal selection in plants cannot be assessed until further studies are conducted (Pineda-Krch and Fagerstrom, 1999; Sutherland and Watkinson, 1986; Otto and Orive, 1995). Moreover, the importance of this to senescence across the plant kingdom is not known, but it will only potentially be relevant to extremely long-lived species with multiple meristems.
The lack of separation between germ line and soma may also be important in the evaluation of the age-specific quality of offspring, particularly if somatic mutations become incorporated into the germ line. If there is a decline in the quality of offspring produced at later ages, then the intensity of selection on late-life traits will decline and will result in the evolution of more rapid senescence. The chance of incorporating a somatic mutation into a gamete depends on how many cell generations there are before gametes are formed and how many cell lines produce germ cells (Jerling, 1985). It is clear that individuals in some species can live to extremely old ages, for example, clones of creosote bush are estimated to be 9,000-10,000 years old (Vasek, 1980). Furthermore, some species cover extensive areas, and thus can potentially have large numbers of meristems. Over time, and with a large number of meristems, there is thus the theoretical potential for mutations to become incorporated into the germ line. In a study of the effects of tree age on pollen, seed, and seedling characteristics in Great Basin bristlecone pine trees (Pinus longaeva), Connnor and
Lanner (1991) evaluated trees ranging in age from 23 to 4,257 years at both high and low elevation sites. They had hypothesized that there should be an increase in somatic mutations with age, particularly at high elevation sites since radiation can severely damage pollen. Their results showed no relationship between tree age and any reproductive variables and no differences between the two sites. To date, evidence suggests that vertical inheritance of somatic mutations is rare (reviewed in Schmid, 1990). Thus, with the possible exception of variation arising from intraorganismal selection, the late separation of germ line and soma does not appear to be an important factor in the evolution of senescence.
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