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Condition dependence of male mortality drives the evolution of sex differences in longevity
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
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. (Ageing Research Group)
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.

Place, publisher, year, edition, pages
2014. Vol. 24, no 20, 2423-2427 p.
National Category
Cell Biology
Research subject
Biology
Identifiers
URN: urn:nbn:se:uu:diva-232068DOI: 10.1016/j.cub.2014.08.055ISI: 000343959000023PubMedID: 25308078OAI: oai:DiVA.org:uu-232068DiVA: diva2:746433
Available from: 2014-09-12 Created: 2014-09-12 Last updated: 2017-12-05Bibliographically approved
In thesis
1. Experimental Evolution of Life-history: Testing the Evolutionary Theories of Ageing
Open this publication in new window or tab >>Experimental Evolution of Life-history: Testing the Evolutionary Theories of Ageing
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
senescence, ageing, longevity, mortality, experimental evolution, Caenorhabditis remanei
National Category
Natural Sciences
Research subject
Biology
Identifiers
urn:nbn:se:uu:diva-231948 (URN)978-91-554-9034-8 (ISBN)
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

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Chen, Hwei-yenMaklakov, Alexei A.

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