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Condition-dependence in life history evolution
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.ORCID iD: 0000-0001-7876-5685
2018 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Ageing is the progressive physiological deterioration that appears with increasing age and eventually leads to a decline in survival and reproduction. This physiological process is omnipresent across the tree of life, but the expected trajectory can widely vary between and within species. Classic theories predict that the evolution of senescence is strongly influenced by the level of extrinsic mortality. Furthermore, variation in early-life developmental environments can shape individual condition and thus lead to alternative life-history strategies. The interplay between early-life environment and individual condition might therefore predict the trajectory of ageing and is of importance when studying life history evolution. In this thesis, I focus on condition dependent life-history strategies and how this can translate in differential ageing patterns. Moreover, I specifically investigate the influence of early-life environment on key life history traits (i.e. survival and reproduction) and how this might eventually carry-over to future generations via nongenetic inheritance. First, I used an experimental approach involving lab populations of the nematode Caenorhabditis remanei to show that males, but not females, pay the cost for the evolution of increased lifespan (Paper I). Second, I used an empirical dataset based on 25 years of observations, to investigate the long-term effects of early-life environment on reproduction and survival (Paper II). Reproductive success of low-condition females in natural populations of collared flycatchers (Ficedula albicollis) peaks later in life, when high-condition females are already in steep reproductive decline and suffer from high mortality rates. Third, I used the neriid fly Telostylinus angusticollis in an experimental environment, to test whether condition-dependent investment in secondary sexual traits affects the life-history strategies of males (Paper III). High-condition males developed and aged faster than low-condition males, but interaction with rival males did not affect male reproductive ageing. Finally, continuing the T. angusticollis experiment, I also found that parental diet interacts with parental sex and offspring sex, ultimately affecting offspring life-histories. Parental effects can thus play an important role in shaping between-individual variation in reproductive and actuarial senescence (Paper IV). Overall, in this thesis I have explored the interaction between environment, condition and ageing in both experimental and natural settings.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2018. , p. 73
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1662
Keywords [en]
Ageing, senescence, nongenetic inheritance, sex differences, condition-dependence, life history, trade-off, Ficedula albicollis, Caenorhabditis remanei, Telostylinus angusticollis
National Category
Evolutionary Biology
Research subject
Biology with specialization in Animal Ecology
Identifiers
URN: urn:nbn:se:uu:diva-347848ISBN: 978-91-513-0314-7 (print)OAI: oai:DiVA.org:uu-347848DiVA, id: diva2:1196034
Public defence
2018-05-25, Zootissalen, Villavägen 9, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2018-05-04 Created: 2018-04-09 Last updated: 2018-05-07
List of papers
1. Evolution of male age-specific reproduction under differential risks and causes of death: males pay the cost of high female fitness
Open this publication in new window or tab >>Evolution of male age-specific reproduction under differential risks and causes of death: males pay the cost of high female fitness
2016 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 29, no 4, p. 848-856Article in journal (Refereed) Published
Abstract [en]

Classic theories of ageing evolution predict that increased extrinsic mortality due to an environmental hazard selects for increased early reproduction, rapid ageing and short intrinsic lifespan. Conversely, emerging theory maintains that when ageing increases susceptibility to an environmental hazard, increased mortality due to this hazard can select against ageing in physiological condition and prolong intrinsic lifespan. However, evolution of slow ageing under high-condition-dependent mortality is expected to result from reallocation of resources to different traits and such reallocation may be hampered by sex-specific trade-offs. Because same life-history trait values often have different fitness consequences in males and females, sexually antagonistic selection can preserve genetic variance for lifespan and ageing. We previously showed that increased condition-dependent mortality caused by heat shock leads to evolution of long-life, decelerated late-life mortality in both sexes and increased female fecundity in the nematode, Caenorhabditis remanei. Here, we used these cryopreserved lines to show that males evolving under heat shock suffered from reduced early-life and net reproduction, while mortality rate had no effect. Our results suggest that heat-shock resistance and associated long-life trade-off with male, but not female, reproduction and therefore sexually antagonistic selection contributes to maintenance of genetic variation for lifespan and fitness in this population.

Keywords
heat shock, intralocus sexual conflict, life-history trade-off, senescence, sex-specific pleiotropy
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-295550 (URN)10.1111/jeb.12833 (DOI)000373929000015 ()26801472 (PubMedID)
Available from: 2016-06-08 Created: 2016-06-08 Last updated: 2018-04-09Bibliographically approved
2. “Silver-spoon” natal conditions increase early-life fitness but accelerate reproductive ageing in a wild bird
Open this publication in new window or tab >>“Silver-spoon” natal conditions increase early-life fitness but accelerate reproductive ageing in a wild bird
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Early-life conditions can have long-lasting effects and organisms that experience a poor start in life are often expected to age at a faster rate. Alternatively, individuals raised in high-quality environments can overinvest in early-reproduction resulting in rapid ageing. Here we use long-term experimental manipulation of early-life conditions in a natural population of collared flycatchers (Ficedula albicollis), to show that females raised in a low-competition environment have higher early-life reproduction but lower late-life reproduction than females raised in high-competition environment. We experimentally created either artificially increased (high-competition) or reduced (low-competition) broods. Reproductive success of high-competition females peaked in late-life, when low-competition females were already in steep reproductive decline and suffered from higher mortality rate. Our results demonstrate that “silver spoon” effects can increase female early-life performance at the cost of faster reproductive ageing and increased late-life mortality. These findings support the evolutionary theory of ageing and show that early-life environmental conditions shape reproductive and demographic ageing in nature.

National Category
Evolutionary Biology
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-347831 (URN)
Available from: 2018-04-08 Created: 2018-04-08 Last updated: 2018-04-09
3. Ontogenetic timing as a condition-dependent life history trait: High-condition males develop quickly, peak early, and age fast
Open this publication in new window or tab >>Ontogenetic timing as a condition-dependent life history trait: High-condition males develop quickly, peak early, and age fast
Show others...
2017 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 71, no 3, p. 671-685Article in journal (Refereed) Published
Abstract [en]

Within-population variation in ageing remains poorly understood. In males, condition-dependent investment in secondary sexual traits may incur costs that limit ability to invest in somatic maintenance. Moreover, males often express morphological and behavioral secondary sexual traits simultaneously, but the relative effects on ageing of investment in these traits remain unclear. We investigated the condition dependence of male life history in the neriid fly Telostylinus angusticollis. Using a fully factorial design, we manipulated male early-life condition by varying nutrient content of the larval diet and, subsequently, manipulated opportunity for adult males to interact with rival males. We found that high-condition males developed more quickly and reached their reproductive peak earlier in life, but also experienced faster reproductive ageing and died sooner than low-condition males. By contrast, interactions with rival males reduced male lifespan but did not affect male reproductive ageing. High-condition in early life is therefore associated with rapid ageing in T. angusticollis males, even in the absence of damaging male-male interactions. Our results show that abundant resources during the juvenile phase are used to expedite growth and development and enhance early-life reproductive performance at the expense of late-life performance and survival, demonstrating a clear link between male condition and ageing.

Place, publisher, year, edition, pages
WILEY, 2017
Keywords
Condition dependence, costs of secondary sexual traits, life history, reproductive ageing, senescence, sexual selection
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-320842 (URN)10.1111/evo.13172 (DOI)000396039000012 ()28067402 (PubMedID)
Funder
Australian Research CouncilEU, European Research CouncilSwedish Research Council
Available from: 2017-04-26 Created: 2017-04-26 Last updated: 2018-04-09Bibliographically approved
4. Early-life parental diet effects on ageing depend on the sex of parents and their offspring
Open this publication in new window or tab >>Early-life parental diet effects on ageing depend on the sex of parents and their offspring
Show others...
(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-347832 (URN)
Available from: 2018-04-09 Created: 2018-04-09 Last updated: 2018-04-09

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