4. living long or dying young in plants and animals

Transworld Research Network 37/661 (2), Fort P.O. Trivandrum-695 023 Kerala, India

The Field of Biological Aging: Past, Present and Future, 2011: 61-82 ISBN: 978-81-7895-513-1 Editor: Abdullah Olgun

4. Living long or dying young in plants and animals: Ecological patterns and

evolutionary processes

Renee M. Borges Centre for Ecological Sciences, Indian Institute of Science, Bangalore 560 012, India

Abstract. Plants and animals are similar and different in many ways and comparing them provides an opportunity to examine whether ecological constraints affect senescence and longevity patterns similarly in them. This paper compares clonal versus non-clonal organisms, and social versus solitary taxa, since a survey of longevity patterns in such organisms would span life forms with varied life history traits. Co-evolving longevities in interacting organisms are discussed. Strategies such as dormancy in plants and diapause in animals that may contribute to prolonging total lifespan from embryo to adult are reviewed. Longevity patterns that are peculiar to plants and animals with special ecologies, e.g. deep sea forms, or special traits such as chemical weapons, are explored. Biomechanical and physical constraints on longevity are also examined. This review therefore attempts to provide an evolutionary and ecological framework using which longevity and ageing can be understood across organisms. It also suggests exciting and fruitful new areas for research in the ecology and evolution of ageing.

*This paper is dedicated to the great evolutionary biologist G C Williams (1926−2010) who contributed significantly to ideas on the evolution of senescence. Correspondence/Reprint request: Dr. Renee M. Borges, Centre for Ecological Sciences, Indian Institute of Science, Bangalore 560 012, India. E-mail: [email protected]

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Introduction In Hindu mythology, gods and demons battled for amrit or the nectar of life which conferred immortality. This amrit was obtained by the churning of the oceans with the help of the great snake Vasuki, and fell into the hands of demons. The powerful god Vishnu, by devious means that involved distracting and beguiling the demons by transforming himself into beautiful Mohini, regained amrit for the gods, making them alone immortal. The sweet-tasting amrit is analogous to ambrosia or the nectar of the gods in Greek mythology, a drink which also conferred immortality and which was supposed to have been brought by doves to the gods residing in Olympus. This cross-cultural similarity in immortality myths and the differences in detail are symbolic of the great similarities and differences in why and how plants and animals live long or die young. Plants and clonal animals rarely get cancer, while non-clonal animals do; naked mole rats and queen bees live long while other rats and worker bees die young; trees age slowly while shrubs age fast; fish and tortoises are long lived as are flying squirrels compared to flightless birds; ramets die but genets of clonal organisms may be immortal. How can this variation in longevity be explained, and are there differences between patterns of longevity in organisms within the plant and animal kingdoms? The geneticist Theodosius Dobzhansky has been quoted countless times for his aphorism “Nothing in biology makes sense except in the light of evolution”, and indeed this saying could not be more relevant for a review on longevity since ageing and longevity can only be viewed within the framework of evolution for any meaningful understanding of these phenomena. The study of longevity and of ageing is now rich with both evolutionary traditions as well as functional genomics and has entered the realm of what may be called evolutionary gerontology [1]. This paper evolved from an earlier mini-review [2] which emphasized the inherent plasticity that must underlie longevity in plants and animals. Since traditional boundaries between the study of plants and animals are in the process of fast dissolving, it is hoped that integrated reviews, such as this one, which attempt to move seamlessly between the kingdoms, will assist in providing an overall evolutionary framework to examine longevity in life forms with varied ecologies. In this paper, the major focus is on comparing longevity in clonal versus non-clonal organisms and in social versus solitary species, since these dichotomies cover the vast majority of growth and life history strategies of life forms on earth. Potentially co-evolving longevities of interacting species such as mutualistic or parasitic interactants will also be

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discussed. The impact on longevity of the differential ability of organisms to regenerate will also be addressed, as also the issue of dormancy and diapause. Proximate factors influencing longevity will be examined in some cases. Before examining longevity patterns and their possible causes, it is necessary to acknowledge the difficulties inherent in defining mortality [3] as well as the need to distinguish between the mortality and immortality of individuals and of lineages. It is also important to differentiate between organisms with determinate versus indeterminate growth, between clonal and non-clonal organisms, and between solitary, eusocial and colonial species. This is because growth and life history parameters have fundamental consequences for the longevity of individuals within species [4]. Definitions Evolutionary biologists define senescence as the reduction in reproductive output and the increase in the probability of mortality with age [5] while senescence for a physiologist or cell biologist is the decline in cellular or physiological function with age [6]. Determinate growth is when an organism’s growth trajectory is set early on in the ontogeny of the organism so that the organism cannot change this trajectory after an initial growth period; thus the organism reaches a fixed size [7]. Indeterminate growth is when an organism can continue to grow throughout its life and can also show considerable plasticity in growth pattern based on temporal variation in resource availability which may even result in body shrinkage [7]. Indeterminate growth that exhibits plasticity as well as an asymptotic function with age is often displayed by soft-bodied marine, freshwater and terrestrial invertebrates as well as some fish [7]; the asymptotic size can increase or decrease over an order of magnitude depending on habitat conditions and resource availability. Indeterminate growth is regarded as the major factor delaying senescence in fish [8]. Plastic and exponential indeterminate growth is exhibited by clonal or colonial organisms with a modular architecture [7]. Here each module contributes to the energy acquisition of the whole colony or clone. Plastic and attenuating indeterminate growth occurs when growth slows down with an increase in size [7]. This is the pattern of growth observed in trees [9]. The only real difference between determinate and indeterminate growth is that in the latter there is no genetically fixed upper size limit, and the organism can change its size throughout its life in response to changing environments. The problem of defining the individual [10] is a particularly acute one in understanding patterns of senescence and thereby longevity [11]. In

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non-clonal plants, the zygote develops into a single rooted unit (the genet), while in clonal plants, the zygote (genet) is duplicated asexually via multiple rooted units (clones) that may continue to be connected to the genet via root sprouts or by rooted stems such as stolons or rhizomes. The genetically defined individual (the genet) that is the product of sexual reproduction and that can reproduce itself asexually (via the ramet) may be immortal while individual ramets are mortal [12]. Therefore, a distinction between the longevity of genets and ramets is important. The evolutionary framework The three most popular theories explaining patterns in the evolution of longevity are the antagonistic pleiotropic theory of Williams [12], the mutation accumulation theory of Haldane [13] and Medawar [14] and the disposable soma theory of Kirkwood [15]. In the mutation theory of Haldane and Medawar, late onset genetic diseases contributing to senescence and mortality will encounter only weak negative selection since reproduction is over at the time of their onset. This theory has been supported experimentally [16]. In the disposable soma theory, there is a trade-off between investment in the maintenance of somatic and reproductive tissues; consequently ageing sets in when somatic tissues become disposable after reproduction has ceased, and when the organism is no longer likely to survive. Several good reviews of these theories exist [4, 17, 18] and they will not be dealt with in detail in this paper. The antagonistic pleiotropy theory will, however, be given more attention. According to the antagonistic pleiotropy theory, senescence occurs because certain genes that are beneficial in early life may have a negative effect during life after reproduction; natural selection is therefore unable to remove such genes from the population owing to their combined beneficial and antagonistic effects. Consequently, this theory uses the concept of life history trade-offs such that early fecundity is obtained at a cost to later-life reproductive success. Important deductions from this theory which are relevant to an examination of the diversity of longevity patterns seen in nature and discussed in this paper are: a) low adult extrinsic mortality rates should be coupled with low rates of senescence, and b) organisms with determinate growth should show greater senescence than those with indeterminate growth. Additional predictions are available in Williams [12] who also claimed that senescence would only be found in those organisms where there is a distinction between germline and soma. The relevance of this claim for senescence and longevity patterns [19] will be discussed later in this paper. Perhaps the best direct test of this evolutionary theory of


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senescence was conducted in Drosophila, where flies that were subjected to different adult mortality rates evolved shorter lifespans when subjected to higher adult mortality [20]. At proximate, mechanistic levels, many theories and processes have been invoked to explain ageing and thereby longevity in organisms. The following are the principal processes and associated theories affecting ageing at various levels: a) Molecular (gene regulation, codon restriction, error catastrophe, epigenetic); b) Cellular (telomere reduction, free radical theory, wear-and-tear, programmed cell death or apoptosis, autophagy); and c) Systemic (neuroendocrine, immunological, rate-of-living). These processes have been ably reviewed by several authors [17, 21–33], and will not be dealt with in any detail here. Only selected examples of some of these theories with relevance to particular cases of longevity in plants and animals will be discussed. The Methuselahs of the plant and animal kingdoms Humans crave an understanding of outliers. What causes progeria? What makes an Usain Bolt? Why were tyrannosaurs so large? So too with longevity. Why do adult mayflies live for only a few minutes while larvae of cicadas live for 17 years? The oldest living plants are either trees or clones of non-woody species. The gymnosperm Pinus longaeva is recorded to live for about 4700 years [34, 35], the cedar Thuja plicata regularly lives for between 800–1000 years [36] and clones of the shrub Lomatia tasmanica (Proteaceae) have been dated to 43,600 years with individual ramets living for about 300 years [37]. Rockfish are known to live for 157 years [8], while lifespans of whales and tortoises can exceed a couple of centuries [38, 39]. Longevities of clonal and non-clonal organisms While trees can reach great ages, this extreme longevity applies to their meristematic lineages and not to individual cells or modules that may not be more than a few decades old. Indeed much of the tree consists of dead cells in the form of heartwood, cork and bark. Still, long-lived trees or plants with tree-like forms can also have long-lived cells; e.g. the ray parenchyma cells of the giant saguaro or tree-cactus Carnegiea gigantea and the cortex cells of the barrel cactus Ferrocactus wislizenii [40, 41] can live for 100 years. Human neurons can also reach great ages, even more than a century, but humans do not live to be as old as trees.

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Recently Aarssen [42] has sketched an interesting scenario to provide a solution to “the problem of the small” via an analysis of plant reproductive economy. This scenario has useful implications for an understanding of how plants might be strategizing longevity. In this view, plants are competing for limiting resources such as space and light, and woody plants are selected to grow into tall trees as a result of this competition [43]. Trees do not usually reproduce clonally. By virtue of their indeterminate growth and meristematic tissue, trees reproduce for extended periods of time by meiosis in their germlines; this results in ovules or pollen that can form zygotes which may be vectored to new germination sites. Small and usually short-lived plants adopt another strategy. Besides sexual reproduction, these plants also reproduce clonally and thus ensure the longevity of the original genet. According to Aarssen [42], clonality can provide a survival advantage to small plants since it can move the genet from areas of competition or nutrient deprivation to more suitable sites. Correspondingly, a trade-off between sexual and clonal reproduction can influence clonal senescence since greater asexual reproduction via ramets will ensure genet survival and retard genet senescence [44]. Interestingly, during plant evolution, while all early vascular plants were clonal, clonality was lost in some clades only after the appearance of erect and arborescent forms, e.g. Lepidodendron [45]. Similarly, while all extant pteridophytes are relatively small and clonal, their now extinct large and non-clonal relatives gave rise to the mostly large and non-clonal gymnosperms [45]. As mentioned earlier, trees generally lack clonality, and their reproduction is not limited by small body size. Trees have relatively long-lived meristematic lines while small non-woody plants employ clonality to achieve reproductive economy. Thus according to Aarssen [42], some plants may sacrifice the size of a ramet in order to produce ramets in larger numbers via clonality with reductions in the longevity of each individual ramet, while others trade off clonality to achieve tallness (as happens in trees) in which case they can escape local competition and send their gametes and zygotes to far distances through wind or biotic pollination and seed dispersal. This reproductive process also occurs for longer periods of time in tall trees compared to smaller clonal plants. Separation between germline and soma Williams [12] asserted that senescence could only occur in organisms where there is separation between germline and soma. The unity of germline and soma was therefore considered to be a barrier to the evolution of senescence in unicellular organisms such as bacteria in which germline and


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soma were considered indistinguishable. Recently, however, senescence has been shown to occur in bacteria which undergo either asymmetrical [46] or symmetrical division [47]. In these cases, the older cell retains the old pole and only the newly synthesized components enter the daughter cell [47]. Consequently, even in unicellular organisms there may be separation between germline and soma [19] which is also perhaps indicated by the presence of two types of nuclei, the germline micronucleus and the somatic macronucleus, in amoebae such as Paramoecium [48]. Similarly, the budding of smaller yeast daughter cells from older and larger mother cells which show signs of ageing [49] may also constitute a germline–soma distinction [19]. Other authors have also questioned whether the separation between germline and soma is necessary for the evolution of senescence [50, 51], pointing out additionally the consequences of this point of view for differences between senescence in ramets and genets [52]. The amount of clonal reproduction in an organism can also affect the evolution of senescence since clonal reproduction tends to retard but does not preclude senescence [53, 54]. Therefore, even “immortal” Hydra [55] may show senescence [56], as does the asexually reproducing marine oligochaete Paranais litoralis [50]. Similary zooid senesence in the marine bryozoan Electra pilosa has also been observed [57]. Yet, the evolutionary theory of senescence does not offer clear predictions for the presence of colony-level senescence in clonal organisms [50], and further exploration of this interesting subject area is warranted. The physiological integration between ramets may also affect the evolution of senescence at the level of the genet [52]. If an individual plant is structurally and functionally a single-rooted integrated physiological unit (IPU) and does not produce asexual ramets to which it is attached, then this IPU will undergo senescence since it will continue to grow and may even reach a size level that is beyond its physiological optimum; at this point the genet will begin to senesce. This may be what occurs in the iteroparous sea beet Beta vulgaris ssp. maritime, which never produces ramets, exists as a single IPU, and in which ageing effects have been observed [58]. According to this view, if the genet is physically connected to ramets, and retains this connectivity, senescence in the genets will set in. However, if the ramets produced by the genets are physically separated from the genet by fragmentation, then while the individual fragments or ramets may undergo senescence, there will be limited evolution of senescence in the genet as long as new ramets are produced by clonal growth. Thus ramets will senesce but the genet may escape senescence. Therefore, with respect to plants, the critical distinction is not between germline and soma or even between clonal and non-clonal plants but between plants in which the genet is a single-rooted

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IPU and one in which it is physically connected to its clones [52]. From this perspective, senescence will evolve in clonal plants that are physiologically integrated rather than in those that fragment. The unity of the germline and soma therefore appears to be a necessary but not sufficient condition to prevent the evolution of senescence in plants and clonal animals [52]. Ageing in trees It therefore appears that despite indeterminate growth and great longevity in plants, especially in trees, they do exhibit senescence. What are the correlates of this senescence and how may ageing be explained in trees? Plants can only live as long as they continue to grow. This is because plants are autotrophs and continually require to produce new photosynthetic units (leaves) as well as nutrient-gathering units (roots) in order to grow. New leaves often require new branches in the growth process. Thus plant growth and plant size are likely to have strong relationships with plant age. In trees, several factors may govern reduced growth with age [59]. a) Respiration/Photosynthesis Ratios: As trees grow, there is an increase in non-productive relative to productive tissue [60, 61]. Increasing respiration relative to photosynthesis results in slower growth. b) Hydraulic Limitation: Increasing tree height results in increasing length and corresponding decreasing conductance of water-conducting xylem tissue. This has led to the hydraulic limitation hypothesis of tree growth and tree height [62, 63], which although applicable to many trees, may not be universal [64]. c) Nutrient Limitation: This hypothesis refers to self-limitation of tree growth by locking up nutrients in tree biomass, and thus making nutrients unavailable for further growth [65]. Individual trees may only be released from such limitation if there is continuous nutrient flux into the system or by nutrient resorption from senescing tissues such as leaves. d) Genetically Programmed Senescence: According to this hypothesis, there is programmed senescence leading to decreased growth potential of meristems. Whereas this type of senescence brought about by DNA methylation and changes in gene expression has been shown in transitions from juvenile to adult stages in plants [66, 67], it has not been clearly demonstrated in trees after they have acquired adult reproductive status. Hence the evidence for this process is still equivocal [59]. The effect of size must also be uncoupled from that of age while examining senescence in trees [68]. Experiments in which meristems from the canopy of old tall trees were grafted onto young rootstocks in angiosperms and gymnosperms showed that there was no reduction in growth


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potential of these meristems, while the meristems left in their original locations exhibited reduced vigour [68]. Therefore, factors extrinsic to the meristem such as its location can influence its growth and vigour, and thereby its senescence, rather than factors intrinsic to the meristem. To demonstrate this, young shoots grafted onto the tall crowns of Japanese cedar trees exhibited the limitations of photosynthesis and stomatal conductance inherent to their new locations, and their performance was as poor at that of the ageing crowns [69]. Even in non-clonal plants with a single terminal meristem (e.g. palms), there is a decline in reproductive output with size and height which is probably due to problems in vascular transport with increasing height [70]. Some palms may, however, have resolved the problem of a reproductive slow down by becoming clonal [71]. It appears, therefore, that senescence can occur in single-rooted genets of trees as a result of size-mediated effects. Other studies have also shown a decline in growth rates with lifespan in trees [9]. The maximum height of trees (ca. 130 m) is probably dictated by hydraulic [72] as well as biomechanical constraints [73, 74], although tallness itself is a trait subject to escalation owing to competition between plants for light [43]. Hydraulic and biomechanical constraints are also present in long-lived desert cacti [75]. The longest-lived cacti are those that can reach heights of 12–15 m and have tree-like forms (e.g. Carnegiea gigantea); such cacti regularly live for more than 100 years [40]. Most trees reach heights of only about 30–50 m; consequently their growth potentials, and thereby their longevity, would be influenced by the numerous constraints outlined above. Furthermore, since plants are immobile, their longevity is also subject to their ability to escape degradation of their supporting dead and living tissues by attacks from pests and pathogens, particularly fungi [2, 36, 76, 77]. It is therefore not surprising that most of the Methuselahs of the plant world occur in taxa which are strongly defended by terpenoid resins (e.g. conifers) and phenolic compounds [60]. Indeed these resins are so resistant to degradation that intact DNA can even be recovered from ancient organisms that have been trapped in amber [78]. It would be valuable therefore to correlate the maximum longevity of trees with their pest- and pathogen-resisting abilities; e.g. the great longevity of some white cedar Thuja occidentalis populations is probably also due to their decay-resistant properties [36]. The Methuselahs of the plant tree world also appear to inhabit extreme environments such as deserts or arid mountains. Is longevity then an inevitable outcome of adaptations for survival in such harsh environments? It might also be worth investigating bonsai plants and short-statured plants of the Mediterranean which are probably very old and in which height is not a correlate of their longevity [79].

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Adaptive iteration, vascular modularity and somatic genetic mosaicism In evolutionary time, some plants have overcome various limitations to growth, and thereby to longevity, by the process of adaptive reiteration [80]. This is a type of epicormic branching which occurs from dormant buds on the trunk or branches of woody trees, not in response to injury or trauma such as defoliation or damage to the apical bud, but as an adaptive response to changing light, nutrient, water and stomatal conductance levels [59]. Adaptive reiteration is believed to free plants from light limitation by initiating new shoots in more illuminated parts of the crown, and to solve hydraulic limitations by initiating these new shoots where hydraulic conductance and water-use efficiency is higher, as well as by redirecting nutrients from senescing tissues by the formation of strong and vigorous nutrient sinks [59]. In ancient 450-year old Pinus menziesii trees, non-epicormic branches in the middle portion of the crown have 148 growth rings on average while epicormic branches in the lower crown are younger with only 94 growth rings [81]. Thus individual trees consist of a mosaic of modules of different ages, and adaptive reiteration can be a very important response leading to the extension of longevity in such trees. The phenomenon of epicormic branching occurs in angiosperms and gymnosperms in which it increases with tree height [82]. The vascular modularity of plants [83] also confers a survival advantage since it allows the localization of trauma or damage to the hydraulic system and consequently avoids systemic failure [2]. Sectoral hydraulics may have contributed to the longevity of many tree species [36]. Similarly, the ability to resprout after damage such as fire [84] is another mechanism that endows greater survival ability on plants [2]. Furthermore, since plants are somatic genetic mosaics, intraindividual selection can purge mutational load from somatic mutations and allow only the more adapted meristematic modules to survive [2, 85, 86]. Genetic heterogeneity within organisms can be beneficial for survival, and thereby contribute to longevity, especially in modular organisms [87]. Biomechanical and physical constraints on longevity Biomechanical constraints on longevity especially in taxa with indeterminate growth could also be important. While trees have great longevity coupled with woodiness, genes for making the vascular cambium of woody plants are also present in non-woody Arabidopsis [88]. This may


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explain why woodiness and the tree habit could evolve in many plant lineages [89], resulting in the appearance of long-lived taxa across the plant kingdom. The large size of trees is probably facilitated by the cellulosic properties of wood just as the longevity of corals is possibly a result of a calcium carbonate skeleton which can protect it from biomechanical stresses [36]. Indeed, colonies of proteinaceous deep-sea corals may live for four thousand years [90]. Similarly, a “redwood” of the coral reef is the giant barrel sponge Xestospongia muta which in Carribean reefs may live for up to 2300 years [91]. Yet, even in these environments, physical constraints can limit growth and thereby longevity; e.g. the constraint of flow-induced energy intakes limited the maximum size of intertidal sea anemones [92], and turbidity–light gradients in the oceans affected the photosynthetic abilities of zooxanthellae and correspondingly coral growth [93]. Importantly, however, partial colony mortality, colony fission and fusion may also confuse any straightforward relationship between size and age in reef corals [94] and associated colonial organisms. Examination of relationships between size and age in such colonial organisms is, therefore, fraught with difficulties. Protected environments, effects of ROS, and telomerase activity Long-lived animals and plants can provide important insights into the mechanisms and environments influencing the evolution of the ageing process [95]. An ocean mollusc, the Arctic quahog (Arctica islandica), can live for 400 years [96, 97], and a species of deep-sea oyster for over 500 years [98]. The imperceptible ageing of the ocean quahog is apparently due to its great antioxidant capacities [99]. Among mammals, bats have the longest lifespan for their body size [100] and in some long-lived bat species this is correlated with resistance to protein oxidation coupled with enhanced protein homeostasis abilities [101]. The eusocial naked mole rat Heterocephalus glaber lives in captivity for more than 28 years, almost 9 times longer than mice of similar sizes [102]. Surprisingly, these mole rats produce similar amounts of reactive oxygen species (ROS) compared to shorter-lived rodent species and have similar repertoires of antioxidants as these species; however, some biochemical parameters such as glucose tolerance, glycated haemoglobin, and antioxidant activity remain unchanged with age in H. glaber while those of laboratory mice and rats decline [102]. The mechanisms for such biochemical prowess remain unknown. Naked mole rats also live in underground burrow systems and may be exposed to less adult predation pressure resulting in greater longevities. Similarly, volant

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organisms such as birds, bats, and flying squirrels which can fly away from predators, as well as animals such as tortoises and bivalves which have thick anti-predator body armour are believed to have lower adult extrinsic mortality and have therefore evolved longer lifespans [12, 103, 104, 105]. Enhanced longevity and lower senescence coupled with lower extrinsic adult mortality seem to have evolved even in tiny Daphnia, since water fleas from low-mortality risk pond habitats exhibited lower amounts of senescence than those from high-risk areas [106]. It is similarly predicted that the unusually long lifespan of rodents such as the African porcupine Hystrix brachyura (greater than 27 years) is probably facilitated by its quills which are efficient anti-predator armaments [105]. From this same perspective, a comparison of chemically protected versus non-protected fish, reptiles and amphibians, showed that, after correcting for body size, the former had longer maximum lifespans than the latter species [107]. Similarly, clown anemonefish Amphiprion percula protected by anemones have lifespans six times greater than the longevity expected for their size [108]. Protection against extrinsic mortality may also induce plasticity in ageing as demonstrated by intraspecific differences in the parasitic nematode Strongyloides ratti. Those nematodes inhabiting the intestinal mucosa of rats can live for 400 days and reproduce by mitotic parthenogenesis, as opposed to the free-living soil-dwelling generations that live for only 5 days [109]. Similarly workers of the weaver ant Oecophylla smaragdina that conduct risky foraging outside the nest (major workers) have higher rates of ageing than those that perform activities within the nest (minor workers) and that rarely venture outside the protected confines of their arboreal leaf nests [110]. Deep-sea environments also seem to select for long-lived organisms, e.g. scorpaenid fish [111]. Deep-sea environments have lower oxygen concentrations; consequently deep-sea organisms probably have less exposure to environmentally-generated ROS compared to surface or shallow marine organisms. Therefore, while ROS-scavenging antioxidants are needed to a greater extent in shallower water, the selection pressure for these compounds is lower in deep-sea creatures. It is therefore extremely interesting that bioluminescence has evolved to a considerable extent in deep-sea creatures. Coelenterazine, the type of luciferin present in many marine bioluminescent groups, is a powerful antioxidant with efficient ROS-scavenging capabilities [112]. It has been suggested that when ROS scavenging was no longer so critical in the deep-sea, ROS detoxification was diverted into a communication tool by deep-sea dwellers in the dark depths of the ocean resulting in deep-sea bioluminescence [112]. Furthermore, coelenterazine is found in all tissues and not just in the bioluminescent organs [112]. While all reasons for the greater longevity of deep-sea fishes are not


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yet known, and their low metabolic rates may also be involved in this phenomenon [113], there are many exciting possibilities for research in this area [111]. In the rainbow trout (Oncorhynchus mykiss) which does not age perceptibly, high telomerase activity has been found in all analysed organs [114], as was also found for long-lived lobsters [115], both organisms with indeterminate growth. Newer studies using non-conventional model organisms are being conducted to test the proximal mechanistic theories of senescence that were mentioned before. For example, the free radical theory of ageing was tested using long-lived and short-lived colubrid snakes and it was found that longer-lived species had lower free radical production than shorter-lived ones [116]. Within the same garter snake species Thamnophis elegans, long-lived ecotypes in areas of low extrinsic mortality had more efficient mitochondria and more efficient antioxidant capacities compared to shorter-lived ecotypes living in areas with higher extrinsic mortality [117]. The evidence for these proximal theories has also been recently reviewed for birds [118] and will not be dealt with here in any detail. Dormancy and diapause Dormancy and diapause can be important bet-hedging strategies [119, 120] prolonging life in a variety of organisms ranging from desert annual plants [121], through sponges [122], many arthropods [123], and vertebrates including fish and amphibians [124]. In plants, many types of seed dormancy mechanisms exist and there is also a general positive relationship between ratios of embryo to seed volumes and seed dormancy [125]. Here too, plants exhibit exceptional longevity. A 1288-year old seed of the sacred lotus Nelumbo nucifera was germinated from an ancient lake in China, and plants were successfully grown from lotus seeds that were at least 332 years old [126]. While the preservation of such seeds in anoxic highly reducing clay lake sediments must have also contributed to their longevity, such ancient seeds were also found to be functionally and enzymatically robust, especially in L-isoaspartyl methyltransferase activity [126]. Dormancy can be an evolutionary stable strategy when there is intense competition for space in the above-ground environment and when survival in the soil seed bank is high [127]. In such cases, sexually produced offspring can inherit the limited above-ground space after parental mortality. Density dependence and severe competition for space has been shown theoretically to result in greater adult longevity [128]; this may also explain greater juvenile (seed) longevity. Periods of dormancy with very slow growth or prolonged

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development have been seen, for example, in the periodical cicadas which have larval development periods of 13 or 17 years, which are the longest larval development periods for any insect [129]. During this period, cicada nymphs feed on root xylem tissues in the relatively protected rhizosphere environment. It is possible that this prolonged juvenile development has been selected for since it increases fecundity with little simultaneous increased risk of mortality [130]. In this vein, it is also useful to consider the evolutionary and reproductive consequences of vegetative dormancy in plants which occurs when an herbaceous perennial does not sprout aboveground but lives underground as rootstock for one or more growing seasons [131]. The relationship between this type of vegetative dormancy, senescence and lifespan is recently being investigated and presents a new exciting area of research [132]. Sociality and ageing Sociality can also have an effect on ageing in animals, perhaps in a way analogous to that between attached and non-attached ramets and genets in plants and in clonal as well as colonial animals. In insects, the evolution of eusociality was associated with a 100-fold increase in lifespan [133]. In birds, however, no relationship between sociality and lifespan was detected after correcting for body size [134, 135]. The findings for eusocial insects are consistent with evolutionary theories of ageing, since their colonies are usually situated in extremely sheltered places where the mortality of queens or kings (i.e. the sole reproductives of the colony) from extrinsic causes is likely to be much lower than in non-social taxa [133]. In accordance with theory, queens of ant species that found monogynous colonies live longer than those of polygynous colonies, and this is believed to be related to the mortality risk of colony founding via polygyny compared to monogyny [133]. Similarly, termite kings and queens have greater longevity compared to reproductives of other solitary insect species, living as they do within the protected environment of their mounds [136]. In social organisms, ageing may be delayed and longevity prolonged even during post-reproductive periods if by this means care-giving and intergenerational transfers to offspring or grand-offspring can enhance the survival and in turn the reproduction of the recipients of the transfer [137, 138]. Queens of some ant species can live for 30 years [139]. Hive bees that are prevented from becoming foragers can live for many times longer than forager bees since as nurse bees restricted to the hive they are capable of transferring more investment to the next generation than as foragers [140].


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Furthermore, since the risk of mortality for hive bees is much lower than that for foragers, investment in the forager soma should be lower than that for hive bees; foragers may therefore be more expendable and have shorter lifespans in accordance with the disposable soma theory of ageing [140, 141]. In social organisms, therefore, the reproductive success, ageing and longevity of individuals rely on the structure and ecology of the social group for their explanation. Social insects, therefore, can contribute greatly to the study of ageing [142]. In the branching coral Acropora palmate, regeneration rates are higher in the younger distal parts of the colony while older basal parts show lower regeneration and therefore greater senescence [143]. Physiological integration between parts of the colony may be responsible for this phenomenon wherein older parts transfer nutrients and metabolites to the younger growing tips which serve as active growth sinks [144]. Thus proximal senescence which occurs at the base of the colonial organism may be offset by the increased growth and reproductive potential of the distal tips and this is achieved by transfer of nutrients from older to young modules [145]. Furthermore, trade-offs in stem cell allocations between requirements for tissue repair and for reproduction are important factors influencing survival and longevity in these clonal and colonial animals [146]. Thus integration of reproduction as well as tissue repair over the entire colony could be responsible for the long-lived nature of the colony, i.e. of the genet, while individual ramets (modules) may senesce [147–149]. This pattern of increased senescence at the proximal part of the colony compared to the distal part has also been observed in a variety of other organisms, e.g. hydroids [150], ascidians [151] and bryozoans [57], and appears to be a common strategy for such growth forms. While sexual selection and sexual dimorphism have been invoked to explain higher mortality rates in males compared to females in both animals (see review of this controversial subject for animals [152]) and plants [153], an examination of this topic is beyond the scope of the present paper. Longevities of interacting species Evolutionary theories of ageing concern themselves with the longevities of individuals which influence the longevity characteristics of species. When species are involved in mutualistic or parasitic interactions, which may even be symbiotic in nature, there is likely to be co-evolution of the longevities of the interactants. For example, most plants depend on the activity of mycorrhizae for successful existence, and since many plants require mycorrhizal inoculum for successful establishment, the mycorrhizal spores

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must also have considerable longevity to match with the germinating time of their host seeds [154]. Similarly, the longevity of parasites must match that of their hosts, especially during the juvenile development stage, as occurs during the parasitism of fig wasps developing within fig inflorescences [155]. Some parasites may even be able to increase the lifespans of their vectors if by doing so they can increase their own transmission [156]. Therefore, an examination of arms races in the longevities of interacting partners [157] should emerge as a fascinating avenue for investigation. Similarly, mutualistic ants influence life-history traits including the longevity of their aphid partners from whom they derive nutrition and to whom they provide protection from predators and fungi [158]. Thus the impact of partner behaviour and/or physiology on the longevities of interactants is an area worthy of serious investigation. Regeneration in plants and animals Understanding regeneration abilities across plants and animals will also aid in an understanding of longevity [159]. This is because regeneration abilities vary greatly in these kingdoms, whether at tissue, organ or whole organism levels [159]. Somatic embryogenesis in plants in which a single somatic cell can give rise to an embryogenic-like ontogeny is quite unique [160]. A comprehensive comparison of regeneration abilities relative to longevity in clonal versus non-clonal plants and animals would provide interesting pointers to relationships with longevity. While stem cells also age [161], how stem cells in plants and in animals are able to erase epigenetic marks and to reset their ages on being elicited to develop into whole organisms are very exciting research areas. Conclusions While all the above evolutionary theories and proximate mechanism can explain general patterns of ageing, there is variation in lifespans even when genetically identical organisms are reared in constant environments [162]. Investigations of the molecular, cellular and systemic sources of such intrinsic variability will therefore provide important insights into the ageing process. A multidisciplinary and multifactorial approach to the problem of longevity is undoubtedly necessary since factors contributing to longevity are not mutually exclusive [79]. What implications do all these perspectives have for human ageing? The intergenerational transfer theory may tell us that over evolutionary time those


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human populations that invest more in their offspring and grand-offspring may be able to postpone senescence, while other theories predict that any factors that reduce extrinsic mortality in adult age and contribute to greater fecundity may also result in the evolution of longer lifespans. From the perspective of development, research that can reveal how plants undergo somatic embryogenesis from a single cell will have important implications for our understanding of how cell, tissues and organisms can forget elapsed time and reset their development clocks. In conclusion, it is important to remember that evolution of reduced ageing or enhanced longevity is a population process, while ageing is an individual phenomenon. While an individual experiences the effect of natural selection in the past, its offspring will experience the natural selection of the future. Thus past, present and future dwell within an individual, and provide a measure of its immortality. Acknowledgements I thank Vidyanand Nanjundiah for critical comments on the manuscript. I am grateful to Abdullah Olgun for inviting me to contribute to this volume and for accepting this idiosyncratic but hopefully informative review. References 1. Partridge, L., and Gems, D. 2006, Trends Ecol. Evol., 21, 334. 2. Borges, R.M., 2009, J. Biosci., 34, 605. 3. Hayflick, L. 2000, Br. J. Cancer, 83, 841. 4. Bonsall, M.B. 2006, Phil.Trans. R. Soc. B, 361, 119. 5. Kirkwood, T.B.L. and Austad, S.N. 2000, Nature, 408, 233. 6. Campisi, J., and d’Adda di Fagagna, F. 2007, Nature Rev. Mol. Cell. Biol.,

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4. living long or dying young in plants and animals

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