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Experimental Evolution of Life-history: Testing the Evolutionary Theories of Ageing
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. (Ageing Research Group)ORCID iD: 0000-0001-9284-3459
2014 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Ageing reduces fitness, but how ageing evolves is still unclear. Evolutionary theory of ageing hinges on the fundamental principal that the force of natural selection declines with age. This principle has yielded two important predictions: 1) the evolution of faster ageing in populations under high rate of extrinsic mortality; and 2) the evolution of faster ageing in a sex that experiences higher rates of extrinsic mortality. However, an emerging new theory argues that when the extrinsic mortality is not random but instead selects on traits showing positive genetic correlation with lifespan, increased mortality should lead to the evolution of increased lifespan. Such condition-dependent mortality is also expected to increase the robustness in the population, resulting in increased deceleration of mortality in late-life. Similarly, high sex-specific mortality can result in increased sex-specific selection on traits that have positive pleiotropic effects on lifespan in the affected sex. This thesis is based on two experimental evolution studies in Caenorhabditis remanei. The first experiment was designed to disentangle the effects of the rate (high or low) and the source (random or condition-dependent) of mortality on the evolution of lifespan and ageing. Reduced lifespan evolved under high rate of random mortality, whereas high condition-dependent mortality, imposed by heat-shock, led to the evolution of increased lifespan (Paper I). However, while female reproduction increased under condition-dependent mortality, male reproduction suffered, suggesting a role for sexual antagonism in maintaining genetic variation for fitness (Paper II). Besides, long lifespan and high fecundity evolved at a cost of slow juvenile growth rate in females (Paper III). Moreover, high condition-dependent mortality led to the evolution of lower rate of intrinsic mortality in late-life (Paper IV). The second experiment showed that evolution of sexual dimorphism in lifespan is driven by the factors that cause sex-specific mortality and cannot be predicted from differences in mortality rate alone. Specifically, high condition-dependent mortality renders males less prone to ageing than females despite higher rates of male mortality (Paper V). The strength of this thesis is the reconfirmation of the earlier findings combined with support for the new theory. Rather than further complicating the matter, the inclusion of the new ideas should help explain some empirical results that are inconsistent with the classic theory, as well as provide a more comprehensive picture of ageing evolution.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2014. , 43 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1178
Keyword [en]
senescence, ageing, longevity, mortality, experimental evolution, Caenorhabditis remanei
National Category
Natural Sciences
Research subject
Biology
Identifiers
URN: urn:nbn:se:uu:diva-231948ISBN: 978-91-554-9034-8 (print)OAI: oai:DiVA.org:uu-231948DiVA: diva2:746053
Public defence
2014-10-28, Friessalen, EBC, Norbyvägen 14, Uppsala, 14:00 (English)
Opponent
Supervisors
Available from: 2014-10-06 Created: 2014-09-11 Last updated: 2015-01-23
List of papers
1. Longer life span evolves under high rates of condition-dependent mortality
Open this publication in new window or tab >>Longer life span evolves under high rates of condition-dependent mortality
2012 (English)In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 22, no 22, 2140-2143 p.Article in journal (Refereed) Published
Abstract [en]

Aging affects nearly all organisms, but how aging evolves is still unclear [1-5]. The central prediction of classic theory is that high extrinsic mortality leads to accelerated aging and shorter intrinsic life span [6, 7]. However, this prediction considers mortality as a random process, whereas mortality in nature is likely to be condition dependent. Therefore, the novel theory maintains that condition dependence may dramatically alter, and even reverse, the classic pattern [2-4]. We present experimental evidence for the evolution of longer life span under high condition-dependent mortality. We employed an experimental evolution design, using a nematode, Caenorhabditis remanei, that allowed us to disentangle the effects of mortality rate (high versus low) and mortality source (random versus condition dependent). We observed the evolution of shorter life span under high random mortality, confirming the classic prediction. In contrast, high condition-dependent mortality led to the evolution of longer life span, supporting a key role of condition dependence in the evolution of aging. This life-span extension was not the result of a trade-off with reproduction. By simultaneously corroborating the classic results [8-10] and providing the first experimental evidence for the novel theory [2-4], our study resolves apparent contradictions in the study of aging and challenges the traditional paradigm by demonstrating that condition-environment interactions dictate the evolutionary trajectory of aging.

National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-188135 (URN)10.1016/j.cub.2012.09.021 (DOI)000311523800022 ()
Available from: 2012-12-12 Created: 2012-12-12 Last updated: 2017-12-07Bibliographically approved
2. Evolution of male reproductive ageing under differential risks and causes of death
Open this publication in new window or tab >>Evolution of male reproductive ageing under differential risks and causes of death
(English)Manuscript (preprint) (Other academic)
National Category
Biological Sciences
Research subject
Biology
Identifiers
urn:nbn:se:uu:diva-232062 (URN)
Available from: 2014-09-12 Created: 2014-09-12 Last updated: 2015-01-23
3. Slow development as an evolutionary cost of long life
Open this publication in new window or tab >>Slow development as an evolutionary cost of long life
Show others...
2017 (English)In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 31, no 6, 1252-1261 p.Article in journal (Refereed) Published
Abstract [en]

Life-history theory predicts a trade-off between early-life fitness and life span. While the focus traditionally has been on the fecundity-life span trade-off, there are strong reasons to expect trade-offs with growth rate and/or development time. We investigated the roles of growth rate and development time in the evolution of life span in two independent selection experiments in the outcrossing nematode Caenorhabditis remanei. First, we found that selection under heat-shock leads to the evolution of increased life span without fecundity costs, but at the cost of slower development. Thereafter, the putative evolutionary links between development time, growth rate, fecundity, heat-shock resistance and life span were independently assessed in the second experiment by directly selecting for fast or slow development. This experiment confirmed our initial findings, since selection for slow development resulted in the evolution of long life span and increased heat-shock resistance. Because there were no consistent trade-offs with growth rate or fecundity, our results highlight the key role of development rate - differentiation of the somatic cells per unit of time - in the evolution of life span. Since development time is under strong selection in nature, reduced somatic maintenance resulting in shorter life span may be a widespread cost of rapid development.

Keyword
antagonistic pleiotropy, development time, growth, life span, stress resistance, trade-off
National Category
Ecology Zoology
Research subject
Biology
Identifiers
urn:nbn:se:uu:diva-232066 (URN)10.1111/1365-2435.12840 (DOI)000402642900009 ()
Funder
Swedish Research Council, 623-2012-6366EU, European Research Council
Available from: 2014-09-12 Created: 2014-09-12 Last updated: 2017-08-21Bibliographically approved
4. Why ageing stops: heterogeneity explains late-life mortality deceleration in nematodes
Open this publication in new window or tab >>Why ageing stops: heterogeneity explains late-life mortality deceleration in nematodes
2013 (English)In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 9, no 5, 20130217- p.Article in journal (Refereed) Published
Abstract [en]

While ageing is commonly associated with exponential increase in mortality with age, mortality rates paradoxically decelerate late in life resulting in distinct mortality plateaus. Late-life mortality plateaus have been discovered in a broad variety of taxa, including humans, but their origin is hotly debated. One hypothesis argues that deceleration occurs because the individual probability of death stops increasing at very old ages, predicting the evolution of earlier onset of mortality plateaus under increased rate of extrinsic mortality. By contrast, heterogeneity theory suggests that mortality deceleration arises from individual differences in intrinsic lifelong robustness and predicts that variation in robustness between populations will result in differences in mortality deceleration. We used experimental evolution to directly test these predictions by independently manipulating extrinsic mortality rate (high or low) and mortality source (random death or condition-dependent) to create replicate populations of nematodes, Caenorhabditis remanei that differ in the strength of selection in late-life and in the level of lifelong robustness. Late-life mortality deceleration evolved in response to differences in mortality source when mortality rate was held constant, while there was no consistent response to differences in mortality rate. These results provide direct experimental support for the heterogeneity theory of late-life mortality deceleration.

Keyword
ageing, heterogeneity, mortality plateau, nematodes, robustness, stress
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-219215 (URN)10.1098/rsbl.2013.0217 (DOI)000330289600020 ()
Available from: 2014-02-25 Created: 2014-02-24 Last updated: 2017-12-05Bibliographically approved
5. Condition dependence of male mortality drives the evolution of sex differences in longevity
Open this publication in new window or tab >>Condition dependence of male mortality drives the evolution of sex differences in longevity
2014 (English)In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 24, no 20, 2423-2427 p.Article in journal (Refereed) Published
Abstract [en]

Males and females age at different rates and have different life expectancies across the animal kingdom, but what causes the longevity "gender gaps" remains one of the most fiercely debated puzzles among biologists and demographers [1-7]. Classic theory predicts that the sex experiencing higher rate of extrinsic mortality evolves faster aging and reduced longevity [1]. However, condition dependence of mortality [8, 9] can counter this effect by selecting against senescence in whole-organism performance [5, 10]. Contrary to the prevailing view but in line with an emerging new theory [7-9, 11], we show that the evolution of sex difference in longevity depends on the factors that cause sex-specific mortality and cannot be predicted from the mortality rate alone. Experimental evolution in an obligately sexual roundworm, Caenorhabditis remanei, in which males live longer than females, reveals that sexual dimorphism in longevity erodes rapidly when the extrinsic mortality in males is increased at random. We thus experimentally demonstrate evolution of the sexual monomorphism in longevity in a sexually dimorphic organism. Strikingly, when extrinsic mortalityis increased in a way that favors survival of fast-moving individuals, males evolve increased longevities, thereby widening the gender gap. Thus,sex-specific selection on whole-organism performance in males renders them less prone to the ravages of old age than females, despite higher rates of extrinsic mortality. Our results reconcile previous research with recent theoretical breakthroughs [8, 9] by showing that sexual dimorphism inlongevity evolves rapidly and predictably as a result of the sex-specific interactions between environmental hazard and organism's condition.

National Category
Cell Biology
Research subject
Biology
Identifiers
urn:nbn:se:uu:diva-232068 (URN)10.1016/j.cub.2014.08.055 (DOI)000343959000023 ()25308078 (PubMedID)
Available from: 2014-09-12 Created: 2014-09-12 Last updated: 2017-12-05Bibliographically approved

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