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      Early reproductive investment, senescence and lifetime reproductive success in female Asian elephants

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          Abstract

          The evolutionary theory of senescence posits that as the probability of extrinsic mortality increases with age, selection should favour early-life over late-life reproduction. Studies on natural vertebrate populations show early reproduction may impair later-life performance, but the consequences for lifetime fitness have rarely been determined, and little is known of whether similar patterns apply to mammals which typically live for several decades. We used a longitudinal dataset on Asian elephants ( Elephas maximus) to investigate associations between early-life reproduction and female age-specific survival, fecundity and offspring survival to independence, as well as lifetime breeding success (lifetime number of calves produced). Females showed low fecundity following sexual maturity, followed by a rapid increase to a peak at age 19 and a subsequent decline. High early life reproductive output (before the peak of performance) was positively associated with subsequent age-specific fecundity and offspring survival, but significantly impaired a female's own later-life survival. Despite the negative effects of early reproduction on late-life survival, early reproduction is under positive selection through a positive association with lifetime breeding success. Our results suggest a trade-off between early reproduction and later survival which is maintained by strong selection for high early fecundity, and thus support the prediction from life history theory that high investment in reproductive success in early life is favoured by selection through lifetime fitness despite costs to later-life survival. That maternal survival in elephants depends on previous reproductive investment also has implications for the success of (semi-)captive breeding programmes of this endangered species.

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          Most cited references63

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          PLEIOTROPY, NATURAL SELECTION, AND THE EVOLUTION OF SENESCENCE

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            Age-dependent traits: a new statistical model to separate within- and between-individual effects.

            Evolutionary questions regarding aging address patterns of within-individual change in traits during a lifetime. However, most studies report associations between age and, for example, reproduction based on cross-sectional comparisons, which may be confounded with progressive changes in phenotypic population composition. Unbiased estimation of patterns of age-dependent reproduction (or other traits) requires disentanglement of within-individual change (improvement, senescence) and between-individual change (selective appearance and disappearance). We introduce a new statistical model that allows patterns of variance and covariance to differ between levels of aggregation. Our approach is simpler than alternative methods and can quantify the relative contributions of within- and between-individual changes in one framework. We illustrate our model using data on a long-lived bird species, the oystercatcher (Haematopus ostralegus). We show that for different reproductive traits (timing of breeding and egg size), either within-individual improvement or selective appearance can result in a positive association between age and reproductive traits at the population level. Potential applications of our methodology are manifold because within- and between-individual patterns are likely to differ in many biological situations.
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              Evolution of ageing.

              T Kirkwood (1977)
              An evolutionary view of ageing suggests that mortality may be due to an energy-saving strategy of reduced error regulation in somatic cells. This supports Orgel's 'error catastrophe' hypothesis and offers a new basis for the study of normal and abnormal ageing syndromes and of apparently immortal transformed cell lines.
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                Author and article information

                Journal
                J Evol Biol
                J. Evol. Biol
                jeb
                Journal of Evolutionary Biology
                BlackWell Publishing Ltd (Oxford, UK )
                1010-061X
                1420-9101
                April 2014
                03 March 2014
                : 27
                : 4
                : 772-783
                Affiliations
                [* ]Department of Animal and Plant Sciences, University of Sheffield Sheffield, UK
                []Section of Ecology, Department of Biology, University of Turku Turku, Finland
                Author notes
                Correspondence: Adam D. Hayward, Department of Animal and Plant Sciences, Alfred Denny Building, University of Sheffield, Western Bank, Sheffield S10 2TN, UK. Tel.: +44 (0)1142220073; fax: +44 (0)1142220002; e-mail: a.hayward@ 123456sheffield.ac.uk
                1 These authors contributed equally.
                Article
                10.1111/jeb.12350
                4237172
                24580655
                0ed71c3c-deea-45e9-b725-d9dcea00c469
                © 2014 The Authors. Journal of Evolutionary Biology published by John Wiley & Sons Ltd on behalf of European Society for Evolutionary Biology

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 19 December 2013
                : 20 January 2014
                : 25 January 2014
                Categories
                Research Papers

                Evolutionary Biology
                ageing,antagonistic pleiotropy,disposable soma,reproductive costs, senescence,trade-off

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