Longitudinal analysis of Plantago: Age-by-environment interactions reveal aging

Department of Biology, University of Virginia, Charlottesville, Virginia 22904-4328, USA.
Ecology (Impact Factor: 4.66). 07/2009; 90(6):1427-33. DOI: 10.1890/08-0981.1
Source: PubMed


We know very little about aging (senescence) in natural populations, and even less about plant aging. Demographic aging is identified by an increasing rate of mortality following reproductive maturity. In natural populations, quantifying aging is often confounded because changes in mortality may be influenced by both short- and long-term environmental fluctuations as well as age-dependent changes in performance. Plants can be easily marked and monitored longitudinally in natural populations yet the age-dependent dynamics of mortality are not known. This study was designed to determine whether a plant species, Plantago lanceolata, shows demographic aging in its natural environment. A large, multiple-cohort design was used to separate age-independent and age-dependent processes. Seven years of results show environmental influences on mortality as evidenced by synchronous changes in mortality across four cohorts over time. Age-dependent mortality was found through an age-by-environment interaction when the oldest cohorts had significantly higher mortality relative to the younger cohorts during times of stress. Neither size nor quantity of reproduction could explain this variation in mortality across cohorts. These results demonstrate demographic senescence in a natural population of plants.

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Available from: Caroline E Ridley, Nov 03, 2014
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    • "Recent studies on Daphnia and a broad range of other organisms have shown that variation in the response to dietary restriction might be more common than previously thought, based on responses to resveratrol (Kim et al. 2014). Age-dependent mortality of Daphnia is affected by an age-by-environment interaction during times of stress (Roach et al. 2009). "
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    ABSTRACT: Invertebrate model systems, such as nematodes and fruit flies, have provided valuable information about the genetics and cellular biology involved in aging. However, limitations of these simple, genetically tractable organisms suggest the need for other model systems, some of them invertebrate, to facilitate further advances in the understanding of mechanisms of aging and longevity in mammals, including humans. This paper introduces 10 review articles about the use of invertebrate model systems for the study of aging by authors who participated in an ‘NIA-NIH symposium on aging in invertebrate model systems’ at the 2013 International Congress for Invertebrate Reproduction and Development. In contrast to the highly derived characteristics of nematodes and fruit flies as members of the superphylum Ecdysozoa, cnidarians, such as Hydra, are more ‘basal’ organisms that have a greater number of genetic orthologs in common with humans. Moreover, some other new model systems, such as the urochordate Botryllus schlosseri, the tunicate Ciona, and the sea urchins (Echinodermata) are members of the Deuterostomia, the same superphylum that includes all vertebrates, and thus have mechanisms that are likely to be more closely related to those occurring in humans. Additional characteristics of these new model systems, such as the recent development of new molecular and genetic tools and a more similar pattern to humans of regeneration and stem cell function suggest that these new model systems may have unique advantages for the study of mechanisms of aging and longevity.
    Invertebrate Reproduction and Development 01/2015; 59(sup1). DOI:10.1080/07924259.2014.970002 · 0.61 Impact Factor
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    • "Rather, our null hypothesis predicts that any differences in trait value (e.g., seed size) between fl oral positions will display common patterns of lower investment at distal relative to basal fl oral positions. This null hypothesis follows other tests of reproductive effort in iteroparous organisms (e.g., Kliber and Eckert, 2004 ; Zeng et al., 2009 ), including a congener of the model system used in the present study ( Caruso, 2006 ), and is statistical rather than concerned with the proportion of variation in traits that is attributable to specifi c constraints ( Cole, 1954 ; Charnov and Schaffer, 1973 ; Young, 1981 ; Orzack and Tuljapurkar, 1989 ). Models explaining the adaptive value of semelparous reproduction generally compare the cumulative fi tness of an annual semelparous strategy with a perennial iteroparous strategy. For annual semelparous organisms, where survival to the next year (or other reproductive " cycle " ) is low, completing growth and reproduction within a single year is expected to maximize reproductive success ( Clutton-Brock, 1984 ; Charlesworth, 1994 ; Kaitala et al., 2002 ; Zeineddine and Jansen, 2009 ). "
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    ABSTRACT: Premise of the study: Life-history theory predicts a trade-off between current and future reproduction for iteroparous organisms-as individuals age, the expected value of future reproduction declines, and thus reproductive effort is expected to be higher in later clutches than in earlier. In contrast, models explaining the evolution of semelparity treat semelparous reproduction as instantaneous, with no scope for intraindividual variation. However, semelparous reproduction is also extended, but over shorter time scales; whether there are similar age-or stage-specific changes in reproductive effort within a semelparous episode is unclear. In this study, we assessed whether semelparous individuals increase reproductive effort as residual reproductive value declines by comparing the reproductive phenotype of flowers at five different floral positions along a main inflorescence. Methods: Using the herbaceous monocarp Lobelia inflata, we conducted a longitudinal study of 409 individuals including both laboratory and field populations over three seasons. We recorded six reproductive traits-including the length of three phenological intervals as well as fruit size, seed size, and seed number-for all plants across floral positions produced throughout the reproductive episode. Key results: We found that while the rate of flower initiation did not change, flowers at distal (late) floral positions developed more quickly and contained larger seed than flowers at basal (early) floral positions did. Conclusions: Our results were consistent with the hypothesis that, like iteroparous organisms, L. inflata increases reproductive effort in response to low residual reproductive value.
    American Journal of Botany 08/2014; 101(8):1323-1331. DOI:10.3732/ajb.1400283 · 2.60 Impact Factor
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    • "Indeed, it is difficult to distinguish death caused by intrinsic vs. extrinsic causes because senescence itself makes old individuals more susceptible to external forces of mortality (Mueller-Dombois 1987), even under controlled conditions. Whereas some authors have stated that making this distinction is virtually impossible (Kirkwood & Austad 2000), labour-intensive approaches such as the multi-cohort study on Plantago lanceolata (Roach 2009; Shefferson & Roach 2012, 2013) have been successful at disentangling not only intrinsic and extrinsic factors of mortality, but also the role of genetics. New statistical approaches using Bayesian and multivariate techniques may also facilitate research on this topic (Colchero, Jones & Rebke 2012; Holzwarth et al. 2013). "
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    ABSTRACT: 1. Senescence, the physiological decline that results in decreasing survival and/or reproduction with age, remains one of the most perplexing topics in biology. Most theories explaining the evolution of senescence (i.e. antagonistic pleiotropy, accumulation of mutations, disposable soma) were developed decades ago. Even though these theories have implicitly focused on unitary animals, they have also been used as the foundation from which the universality of senescence across the tree of life is assumed.2. Surprisingly, little is known about the general patterns, causes and consequences of whole-individual senescence in the plant kingdom. There are important differences between plants and most animals, including modular architecture, the absence of early determination of cell lines between the soma and gametes, and cellular division that does not always shorten telomere length. These characteristics violate the basic assumptions of the classical theories of senescence and therefore call the generality of senescence theories into question.3. This Special Feature contributes to the field of whole-individual plant senescence with five research articles addressing topics ranging from physiology to demographic modelling and comparative analyses. These articles critically examine the basic assumptions of senescence theories such as age-specific gene action, the evolution of senescence regardless of the organism's architecture and environmental filtering, and the role of abiotic agents on mortality trajectories.4. Synthesis. Understanding the conditions under which senescence has evolved is of general importance across biology, ecology, evolution, conservation biology, medicine, gerontology, law and social sciences. The question ‘why is senescence universal or why is it not?’ naturally calls for an evolutionary perspective. Senescence is a puzzling phenomenon, and new insights will be gained by uniting methods, theories and observations from formal demography, animal demography and plant population ecology. Plants are more amenable than animals to experiments investigating senescence, and there is a wealth of published plant demographic data that enable interpretation of experimental results in the context of their full life cycles. It is time to make plants count in the field of senescence.
    Journal of Ecology 05/2013; 101(3):545-554. DOI:10.1111/1365-2745.12089 · 5.52 Impact Factor
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