The origins of human ageing.

The origins of human ageing are to be found in the origins and evolution of senescence as a general feature in the life histories of higher animals. Ageing is an intriguing problem in evolutionary biology because a trait that limits the duration of life, including the fertile period, has a negative impact on Darwinian fitness. Current theory suggests that senescence occurs because the force of natural selection declines with age and because longevity is only acquired at some metabolic cost. In effect, organisms may trade late survival for enhanced reproductive investments in earlier life. The comparative study of ageing supports the general evolutionary theory and reveals that human senescence, while broadly similar to senescence in other mammalian species, has distinct features, such as menopause, that may derive from the interplay of biological and social evolution.     

The evolution of plant life span: facts and hypotheses

There are two different views on the evolution of life forms in Cormophyta: from woody plants to herbaceous ones or in opposite direction - from herbs to trees. In accordance with these views it is supposed that life span in plants changed in the course of evolution from many years (perennials) to few years (annuals, biennials), or went in reverse - from few years to many years. The author discusses the problems of senescence and longevity in Cormophyta in the context of various hypotheses of ageing (programmed death theory, mutation accumulation, antagonistic pleiotropy, disposable soma, genes of ageing, genes of longevity). Special attention is given to bio-morphological aspects of longevity and cases of non-ageing plants ("negative senescence", "potential immortality"). It is proposed to distinguish seven models of simple ontogenesis in Cormophyta that can exemplify the diversity of mechanisms of ageing and longevity. The evolution of life span in plants is considered as an indirect result of natural selection of other characteristics of organisms or as a consequence of fixation of modifications (episelectional evolution). It seems that short life span could emerge several times during evolution of one group of plants, thus favoring its adaptive radiation.     

Sex differences in ageing in natural populations of vertebrates

In many long-lived vertebrates (including humans), adult males have shorter lifespans than adult females, partly as a result of higher annual rates of mortality in males and partly owing to sex differences in the rate of ageing. A probable explanation of the evolution of sex differences in ageing is that, in polygynous species, intense intrasexual competition between males restricts the number of seasons for which individual males are able to breed successfully, weakening selection pressures favouring adult longevity in males relative to females. If this is the case, sex differences in adult longevity and in the onset and rate of senescence should be greater in polygynous species than in monogamous ones and their magnitude should be related to the duration of effective breeding males compared with females. Here, we use data from longitudinal studies of vertebrates to show that reduced longevity in adult males (relative to females) is commonly associated with a more rapid decline in male than female survival with increasing age and is largely confined to polygynous species. The magnitude of sex differences in adult longevity in different species is consistently related to the magnitude of sex differences in the duration of effective breeding, calculated across surviving adults. Our results are consistent with the suggestion that sex differences in senescence in polygynous species are a consequence of weaker selection for longevity in males than females.     

DNA damage, cellular senescence and organismal ageing: causal or correlative?

Cellular senescence has long been used as a cellular model for understanding mechanisms underlying the ageing process. Compelling evidence obtained in recent years demonstrate that DNA damage is a common mediator for both replicative senescence, which is triggered by telomere shortening, and premature cellular senescence induced by various stressors such as oncogenic stress and oxidative stress. Extensive observations suggest that DNA damage accumulates with age and that this may be due to an increase in production of reactive oxygen species (ROS) and a decline in DNA repair capacity with age. Mutation or disrupted expression of genes that increase DNA damage often result in premature ageing. In contrast, interventions that enhance resistance to oxidative stress and attenuate DNA damage contribute towards longevity. This evidence suggests that genomic instability plays a causative role in the ageing process. However, conflicting findings exist which indicate that ROS production and oxidative damage levels of macromolecules including DNA do not always correlate with lifespan in model animals. Here we review the recent advances in addressing the role of DNA damage in cellular senescence and organismal ageing.     

An extraordinary life span estimate for the clown anemonefish Amphiprion percula

A population of the clown anemonefish Amphiprion percula was studied for 1 year, in Madang Lagoon, Papua New Guinea. From this study, data on mortality events and social structure were used to construct a stage-structured matrix model and estimate the average age at death (life expectancy) of various classes of individuals. Based on this model, it is estimated that the life expectancy of female A. percula , the oldest individuals in the population, is 30 years. This estimate is two times greater than the longevity estimated for any other coral reef damselfish and six times greater than the longevity expected for a fish of that size. The result complements the growing body of evidence, from widespread taxa, that organisms subject to low levels of extrinsic mortality show retarded senescence and increased longevity. It is suggested that fishes would be an excellent group for a broad scale comparative test of the predictions of the evolutionary theory of ageing.     

Ageing in a eusocial insect: molecular and physiological characteristics of life span plasticity in the honey bee

Commonly held views assume that ageing, or senescence, represents an inevitable, passive, and random decline in function that is strongly linked to chronological age. In recent years, genetic intervention of life span regulating pathways, for example, in Drosophila as well as case studies in non-classical animal models, have provided compelling evidence to challenge these views.Rather than comprehensively revisiting studies on the established genetic model systems of ageing, we here focus on an alternative model organism with a wild type (unselected genotype) characterized by a unique diversity in longevity - the honey bee.Honey bee (Apis mellifera) life span varies from a few weeks to more than 2 years. This plasticity is largely controlled by environmental factors. Thereby, although individuals are closely related genetically, distinct life histories can emerge as a function of social environmental change.Another remarkable feature of the honey bee is the occurrence of reverted behavioural ontogeny in the worker (female helper) caste. This behavioural peculiarity is associated with alterations in somatic maintenance functions that are indicative of reverted senescence. Thus, although intraspecific variation in organismal life span is not uncommon, the honey bee holds great promise for gaining insights into regulatory pathways that can shape the time-course of ageing by delaying, halting or even reversing processes of senescence. These aspects provide the setting of our review.We will highlight comparative findings from Drosophila melanogaster and Caenorhabditis elegans in particular, and focus on knowledge spanning from molecular- to behavioural-senescence to elucidate how the honey bee can contribute to novel insights into regulatory mechanisms that underlie plasticity and robustness or irreversibility in ageing.     

The mitochondrial genomes of Cambaroides similis and Procambarus clarkii (Decapoda: Astacidea: Cambaridae): the phylogenetic implications for Reptantia

Kim, S., Park, M.‐H., Jung, J.‐H., Ahn, D.‐H., Sultana, T., Kim, S., Park, J.‐K., Choi, H.‐G. & Min, G.‐S. (2012). The mitochondrial genomes of Cambaroides similis and Procambarus clarkii (Decapoda: Astacidea: Cambaridae): the phylogenetic implications for Reptantia. —Zoologica Scripta, 41, 281–292. We determined the complete mitochondrial (mt) genome sequences of two northern hemisphere freshwater crayfish species, Cambaroides similis and Procambarus clarkii (Decapoda: Astacidea: Cambaridae). These species have an identical gene order with typical metazoan mt genome compositions. However, their gene arrangement was very distinctive compared with the pan‐crustacean ground pattern because of the presence of a long inverted block, which included 19 coding genes and a control region (CR). Because the CR was inverted, their nucleotide frequencies showed a reversed strand‐specific bias compared with the other decapods. Based on a comparative analysis of mt genome arrangements between southern and northern hemisphere crayfish and their putative close marine relative (Homarus americanus, a true clawed lobster), we postulated that the ancestor of freshwater crayfish had a typical pan‐crustacean mtDNA gene order, similar to its marine relatives. Based on this assumption, we traced the most parsimonious gene rearrangement scenario of the northern hemisphere crayfish. In a phylogenetic study on the infraordinal relationships in reptan decapods, the lineage Lineata [Thalassinidea (Brachyura, Anomura)] was well supported, while the infraorder positions of Achelata and Astacidea remained unidentified.     

Proprioceptors of the thoracic limbs of Squilla mantis (Crustacea,Stomatopoda)

Summary The distribution and morphology of the internal proprioceptive organs in the thoracic appendages of the stomatopod crustacean, Squilla mantis, are described. Five distinct types of proprioceptor are recognised; connective chordotonal organ, myochordotonal organ, cuticular stress detector, multiterminal stretch receptor and apodeme stretch receptor. The connective chordotonal organs and multiterminal receptors exhibit a wide variety of structural and functional complexity. The stomatopods resemble the decapods in that the basic proprioceptive unit of the thoracic appendages appears to be the connective chordotonal organ, but differs in the higher occurrence of multiterminal stretch receptors. As described for decapods, the pereiopods of stomatopods possess the largest number and greatest variety of proprioceptors, suggesting that locomotion exerts greater selective pressure on proprioceptor development than do the other thoracic limb functions, including the raptorial strike.     

Evolution and ageing

Did senescence evolve as a direct result of natural selection in order to limit the life-span or did increases in longevity evolve in the face of random events that ordinarily limit the life-span? The adaptive hypothesis is that senescence is a programmed process which appeared in evolution because a limited life-span has selective advantages for certain species. Non-adaptive theorists hold that evolution has acted to lengthen the life-span and maximize reproduction and that senescence is only an evolutionary by-product since natural selection does not act directly on postreproductive events. The assumptions and arguments underlying these hypotheses are examined critically in the light of experimental evidence. While theoretical study of the evolution of ageing may advance our understanding of the nature of ageing itself, it is likely that further clarification of the relationship between evolution and ageing will depend on experimental approaches that are now becoming possible.     

Abbreviation of larval development and extension of brood care as key features of the evolution of freshwater Decapoda

The transition from marine to freshwater habitats is one of the major steps in the evolution of life. In the decapod crustaceans, four groups have colonized fresh water at different geological times since the Triassic, the freshwater shrimps, freshwater crayfish, freshwater crabs and freshwater anomurans. Some families have even colonized terrestrial habitats via the freshwater route or directly via the sea shore. Since none of these taxa has ever reinvaded its environment of origin the Decapoda appear particularly suitable to investigate life‐history adaptations to fresh water. Evolutionary comparison of marine, freshwater and terrestrial decapods suggests that the reduction of egg number, abbreviation of larval development, extension of brood care and lecithotrophy of the first posthatching life stages are key adaptations to fresh water. Marine decapods usually have high numbers of small eggs and develop through a prolonged planktonic larval cycle, whereas the production of small numbers of large eggs, direct development and extended brood care until the juvenile stage is the rule in freshwater crayfish, primary freshwater crabs and aeglid anomurans. The amphidromous freshwater shrimp and freshwater crab species and all terrestrial decapods that invaded land via the sea shore have retained ocean‐type planktonic development. Abbreviation of larval development and extension of brood care are interpreted as adaptations to the particularly strong variations of hydrodynamic parameters, physico‐chemical factors and phytoplankton availability in freshwater habitats. These life‐history changes increase fitness of the offspring and are obviously favoured by natural selection, explaining their multiple origins in fresh water. There is no evidence for their early evolution in the marine ancestors of the extant freshwater groups and a preadaptive role for the conquest of fresh water. The costs of the shift from relative r‐ to K‐strategy in freshwater decapods are traded‐off against fecundity, future reproduction and growth of females and perhaps against size of species but not against longevity of species. Direct development and extension of brood care is associated with the reduction of dispersal and gene flow among populations, which may explain the high degree of speciation and endemism in directly developing freshwater decapods. Direct development and extended brood care also favour the evolution of social systems, which in freshwater decapods range from simple subsocial organization to eusociality. Hermaphroditism and parthenogenesis, which have evolved in some terrestrial crayfish burrowers and invasive open water crayfish, respectively, may enable populations to adapt to restrictive or new environments by spatio‐temporal alteration of their socio‐ecological characteristics. Under conditions of rapid habitat loss, environmental pollution and global warming, the reduced dispersal ability of direct developers may turn into a severe disadvantage, posing a higher threat of extinction to freshwater crayfish, primary freshwater crabs, aeglids and landlocked freshwater shrimps as compared to amphidromous freshwater shrimps and secondary freshwater crabs.     

The effect of injury on whole-plant senescence: an experiment with two root-sprouting Barbarea species

Background and Aims Senescence is the process of losing fitness when growing old, and is shaped by the trade-off between maintenance and reproduction that makes reproduction more unsure and maintenance more costly with age. In repeatedly reproducing plants, reductions in growth and fertility are signs of senescence. Disturbance, however, provides an opportunity to reset the ageing clock and consequently potentially ameliorate senescence.Methods To test the effects of disturbance on traits closely related to fitness and thus to senescence, a long-term garden experiment was established with two short-lived perennial congeners, Barbarea vulgaris and Barbarea stricta, that differ in their ability to resprout after injury. In the experiment, five damage treatments were applied to plants in four different phenophases.Key Results It was found that damage to the plant body significantly prolonged life span in B. vulgaris but decreased whole-life seed production in both species. High concentration of seed production in one growing season characterized short life spans. Both more severe damage and a more advanced phenological phase at the time of damage caused reproduction to be spread over more than one growing season and equalized per-season seed production. In terms of seed quality, average weight of a single seed decreased and seed germination rate increased with age regardless of damage.Conclusions Although disturbance is able to reset the ageing clock of plants, it is so harmful to plant fitness that resprouting serves, at best, only to alleviate slightly the signs of senescence. Thus, in terms of whole-life seed production, injured plants were not more successful than uninjured ones in the two studied species. Indeed, in these species, injury only slightly postponed or decelerated senescence and did not cause effective rejuvenation.     

Sociality, age at first reproduction and senescence: comparative analyses of birds

Evolutionary theories of senescence suggest that aging evolves as a consequence of early reproduction imposing later viability costs, or as a consequence of weak selection against mutations that act late in life. In addition, highly social species that live in sites that are protected from extrinsic mortality due to predation should senesce at a slower rate than solitary species. Therefore, species that start reproducing late in life should senesce at a slower rate than species that start reproducing early. In addition, social species should senesce more slowly than solitary species. Here I investigate the rate of senescence using an extensive data set on longevity records under natural field conditions to test predictions about the evolution of senescence among 271 species of birds. Longevity records increased with sampling effort and body mass, but once these confounding variables were controlled statistically, there was a strongly positive relationship between relative longevity and relative adult survival rate. Relative longevity after controlling statistically for sampling effort, body mass and adult survival rate, increased with age at first reproduction, but not with degree of breeding sociality. These findings suggest that the evolution of senescence is related to timing of first reproduction, but that the evolution of breeding sociality has played a negligible role in the evolution of senescence.     

Phylogenetic systematics of the reptantian Decapoda (Crustacea, Malacostraca)

Although the biology of the reptantian Decapoda has been much studied, the last comprehensive review of reptantian systematics was published more than 80 years ago. We have used cladistic methods to reconstruct the phylogenetic system of the reptantian Decapoda. We can show that the Reptantia represent a monophyletic taxon. The classical groups, the 'Palinura', 'Astacura' and 'Anomura' are paraphyletic assemblages. The Polychelida is the sister-group of all other reptantians. The Astacida is not closely related to the Homarida, but is part of a large monophyletic taxon which also includes the Thalassinida, Anomala and Brachyura. The Anomala and Brachyura are sister-groups and the Thalassinida is the sister-group of both of them. Based on our reconstruction of the sister-group relationships within the Reptantia, we discuss alternative hypotheses of reptantian interrelationships, the systematic position of the Reptantia within the decapods, and draw some conclusions concerning the habits and appearance of the reptantian stem species.     

Maintenance of somatic tissue regeneration with age in short‐ and long‐lived species of sea urchins

Aging in many animals is characterized by a failure to maintain tissue homeostasis and the loss of regenerative capacity. In this study, the ability to maintain tissue homeostasis and regenerative potential was investigated in sea urchins, a novel model to study longevity and negligible senescence. Sea urchins grow indeterminately, regenerate damaged appendages and reproduce throughout their lifespan and yet different species are reported to have very different life expectancies (ranging from 4 to more than 100 years). Quantitative analyses of cell proliferation and apoptosis indicated a low level of cell turnover in tissues of young and old sea urchins of species with different lifespans (Lytechinus variegatus, Strongylocentrotus purpuratus and Mesocentrotus franciscanus). The ability to regenerate damaged tissue was maintained with age as assessed by the regrowth of amputated spines and tube feet (motor and sensory appendages). Expression of genes involved in cell proliferation (pcna), telomere maintenance (tert) and multipotency (seawi and vasa) was maintained with age in somatic tissues. Immunolocalization of the Vasa protein to areas of the tube feet, spines, radial nerve, esophagus and a sub‐population of circulating coelomocytes suggests the presence of multipotent cells that may play a role in normal tissue homeostasis and the regenerative potential of external appendages. The results indicate that regenerative potential was maintained with age regardless of lifespan, contrary to the expectation that shorter lived species would invest less in maintenance and repair.     

Species with a chemical defence,but not chemical offence,live longer

Evolutionary hypotheses for ageing generally predict that delayed senescence should evolve in organisms that experience lower extrinsic mortality. Thus, one might expect species that are highly toxic or venomous (i.e. chemically protected) will have longer lifespans than related species that are not likewise protected. This remarkable relationship has been suggested to occur in amphibians and snakes. First, we show that chemical protection is highly conserved in several lineages of amphibians and snakes. Therefore, accounting for phylogenetic autocorrelation is critical when conservatively testing evolutionary hypotheses because species may possess similar longevities and defensive attributes simply through shared ancestry. Herein, we compare maximum longevity of chemically protected and nonprotected species, controlling for potential nonindependence of traits among species using recently available phylogenies. Our analyses confirm that longevity is positively correlated with body size in both groups which is consistent with life‐history theory. We also show that maximum lifespan was positively associated with chemical protection in amphibian species but not in snakes. Chemical protection is defensive in amphibians, but primarily offensive (involved in prey capture) in snakes. Thus, we find that although chemical defence in amphibians favours long life, there is no evidence that chemical offence in snakes does the same.     

Molecular genetics of crustacean feeding appendage development and diversification

Arthropods dominate our seas, land, and air and have done so for hundreds of millions of years. Among the arthropods, crustaceans present us with a rich history of morphological change, much of which is still represented among extant forms. Crustacea largely interact with their environment via their appendages; thus vast amounts of variation exist among the different appendages of a single individual and between appendages from different species. Comparative studies of crustacean appendage development present us with an important story regarding the evolution of morphology over both relatively short (a few million years) and relatively long (a few hundred million years) evolutionary time scales. Recent studies have used the genetic and molecular data from Drosophila development to try to understand the molecular basis for some of the variations seen in crustacean limbs. Here we review some of these data based on the expression patterns of the genes Ultrabithorax, abdominal - A, Sex combs reduced, and Distal-less.     

Longevity and ageing: appraising the evolutionary consequences of growing old

Senescence or ageing is an increase in mortality and/or decline in fertility with increasing age. Evolutionary theories predict that ageing or longevity evolves in response to patterns of extrinsic mortality or intrinsic damage. If ageing is viewed as the outcome of the processes of behaviour, growth and reproduction then it should be possible to predict mortality rate. Recent developments have shown that it is now possible to integrate these ecological and physiological processes and predict the shape of mortality trajectories. By drawing on the key exciting developments in the cellular, physiological and ecological process of longevity the evolutionary consequences of ageing are reviewed. In presenting these ideas an evolutionary demographic framework is used to argue how trade-offs in life-history strategies are important in the maintenance of variation in longevity within and between species. Evolutionary processes associated with longevity have an important role in explaining levels of biological diversity and speciation. In particular, the effects of life-history trait trade-offs in maintaining and promoting species diversity are explored. Such trade-offs can alleviate the effects of intense competition between species and promote species coexistence and diversification. These results have important implications for understanding a number of core ecological processes such as how species are divided among niches, how closely related species co-occur and the rules by which species assemble into food-webs. Theoretical work reveals that the proximate physiological processes are as important as the ecological factors in explaining the variation in the evolution of longevity. Possible future research challenges integrating work on the evolution and mechanisms of growing old are briefly discussed.     

Pollination-induced flower senescence: a review

Ethylene has long been implicated in the control of the senescence of many cut flower species, but the control of senescence in relation to wild species has received much less attention. The longevity of individual flowers varies greatly from species to species; in some each flower is open for just a few hours, whilst in others the flower may persist for several weeks, or even months. The functional life of the flower may be terminated by petal wilting, abscission or a colour change of all, or part, of the perianth. In some species pollination appears to reduce floral longevity whilst in others, particularly those species having short-lived flowers, the pattern of flower development and senescence appears unaffected by pollination.Examples of the various pollination-induced strategies shown by plants are presented and the role of ethylene and other potential mediators of senescence in these processes discussed.     

<Emphasis Type="Italic">Arctica islandica:</Emphasis> the longest lived non colonial animal known to science

The ocean quahog, Arctica islandica is not just the longest living bivalve, it is also the longest lived, non-colonial animal known to science. With the maximum life span potential ever increasing and currently standing in excess of 400 years the clam has recently gained interest as a potential model organism for ageing research. This review details what is known about the biology of A. islandica, it discusses observed age-associated changes and reviews previous ageing research undertaken on the species and other long-lived bivalves which may be applicable to future ageing research and discusses future directions for ageing research with A. islandica. Historically much of the research on bivalves has been targeted at their utilization as a food source, environmental sentinels and more recently the use of their shells as archives of environmental change. The result of this has been an abundance of knowledge on bivalve life strategies, and a limited amount of information on the physiological changes in the cells and tissues of bivalves during the ageing process. However, research into the mechanisms of senescence of long-lived bivalves from a biogerontological perspective has advanced only recently. The research undertaken thus far has documented age-related differences in anti-oxidant defences and accumulation of oxidative products but despite the recent attention into ageing of A. islandica it is still to be ascertained if the species experiences senescence. Future directions for ageing research using A. islandica are discussed.     

Global gradients of avian longevity support the classic evolutionary theory of ageing

Senescence, the process of physiological deterioration associated with growing old, is a shared characteristic of a wide range of animals. Yet, lifespan varies dramatically among species. To explain this variation, the evolutionary theory of ageing has been proposed more than 50 yr ago. Although the theory has been tested experimentally and through comparative analyses, there remains debate whether its fundamental prediction is empirically supported. Here, we use a comprehensive database on avian life history traits to test the evolutionary theory of ageing at a global scale. We show that pronounced geographical gradients of maximum longevity exist, that they are predicted by measures of predator diversity and only partly depend on correlated life‐history traits. The results are consistent with species‐level analyses and can be replicated across bio‐geographical regions. Our analyses suggest that stochastic predation is an important driver of the evolution of lifespan, at least in birds.