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Age-specific trade-offs in life-history evolution
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.ORCID iD: 0000-0003-3356-7284
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Trade-offs prevent selection from driving all fitness-enhancing traits towards values that would maximize fitness. Life-history trade-offs, such as the one between survival and reproduction are well-studied, yet trade-offs can also involve behavioural or cognitive traits. Because males and females have different routes to successful reproduction, the optimal resolution of life-history trade-offs can differ between the sexes. However, shared genome can constrain the evolution of sex-specific adaptations. In this thesis, I explore the links between sex-specific life histories, cognition and behaviour. I start by linking sex differences in life histories to sex differences in learning performance in the outcrossing nematode Caenorhabditis remanei (Paper I). I report that age-related learning differs between the sexes and that it corresponds to sexual dimorphism in life history. Then, I use experimental evolution to select for learning performance to study the patterns of genetic correlations between learning and life-history traits in both sexes (Paper II). The results demonstrate the correlated evolution of sexual dimorphism in life history indicating sex-specific fitness costs and benefits of learning. In Paper III I use the fruit fly Drosophila melanogaster to ask about the extent to which cognitive and demographic aging are independent. The results reveal that selection for late-life reproduction alone bears no effect on late-life learning and that joint selection on late-life learning and reproduction does not yield lifespan benefits. The selection might have affected, however, female age-specific reproductive effort. Motivated by the questions on aging I proceed to ask why a potent lifespan extending drug – rapamycin affects sexes differently (Paper IV). I take a closer look at the trade-off between growth, lifespan and reproduction and propose that the sex experiencing a stronger relationship between size and fitness pays a higher cost of lifespan extension. Finally, I focus on another sex-specific trait – dispersal (Paper V). I conduct experimental evolution to uncover a negative genetic correlation between dispersal and reproduction and show sex-specific genetic variation for dispersal. In summary, my thesis unravels the complex pattern of interdependence between life-history, behavioural and cognitive traits, where sex emerges as an important factor that can maintain genetic variation for trade-offs.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2017. , 48 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1555
Keyword [en]
life history, trade-off, learning, aging, sex differences, dispersal, Caenorhabditis, Drosophila
National Category
Biological Sciences
Research subject
Biology with specialization in Animal Ecology
Identifiers
URN: urn:nbn:se:uu:diva-329035ISBN: 978-91-513-0067-2 (print)OAI: oai:DiVA.org:uu-329035DiVA: diva2:1139517
Public defence
2017-10-27, Zootissalen, Villavägen 9, Uppsala, 13:00 (English)
Opponent
Supervisors
Available from: 2017-10-04 Created: 2017-09-07 Last updated: 2017-10-18
List of papers
1. Sex differences in cognitive ageing: Testing predictions derived from life-history theory in a dioecious nematode
Open this publication in new window or tab >>Sex differences in cognitive ageing: Testing predictions derived from life-history theory in a dioecious nematode
2013 (English)In: Experimental Gerontology, ISSN 0531-5565, E-ISSN 1873-6815, Vol. 48, no 12, 1469-1472 p.Article in journal (Refereed) Published
Abstract [en]

Life-history theory maintains that organisms allocate limited resources to different traits to maximize fitness. Learning ability and memory are costly and known to trade-off with longevity in invertebrates. However, since the relationship between longevity and fitness often differs between the sexes, it is likely that sexes will differentially resolve the trade-off between learning and longevity. We used an established associative learning paradigm in the dioecious nematode Caenorhabditis remanei, which is sexually dimorphic for lifespan, to study age-related learning ability in males and females. In particular, we tested the hypothesis that females (the shorter-lived sex) show higher learning ability than males early in life but senesce faster. Indeed, young females outperformed young males in learning a novel association between an odour (butanone) and food (bacteria). However, while learning ability and offspring production declined rapidly with age in females, males maintained high levels of these traits until mid-age. These results not only demonstrate sexual dimorphismin age-related learning ability but also suggest that it conforms to predictions derived from the life-history theory.

Keyword
Ageing, Caenorhabditis, Learning, Life-history, Sex differences, Trade-off
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-213468 (URN)10.1016/j.exger.2013.09.008 (DOI)000327489800012 ()
Available from: 2013-12-30 Created: 2013-12-23 Last updated: 2017-12-06Bibliographically approved
2. Selection on learning performance results in the correlated evolution of sexual dimorphism in life history
Open this publication in new window or tab >>Selection on learning performance results in the correlated evolution of sexual dimorphism in life history
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2016 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 70, no 2, 342-357 p.Article in journal (Refereed) Published
Abstract [en]

The evolution of learning can be constrained by trade-offs. As male and female life histories often diverge, the relationship between learning and fitness may differ between the sexes. However, because sexes share much of their genome, intersexual genetic correlations can prevent males and females from reaching their sex-specific optima resulting in intralocus sexual conflict (IaSC). To investigate if IaSC constraints sex-specific evolution of learning, we selected Caenorhabditis remanei nematode females for increased or decreased olfactory learning performance and measured learning, life span (in mated and virgin worms), reproduction, and locomotory activity in both sexes. Males from downward-selected female lines had higher locomotory activity and longer virgin life span but sired fewer progeny than males from upward-selected female lines. In contrast, we found no effect of selection on female reproduction and downward-selected females showed higher locomotory activity but lived shorter as virgins than upward-selected females. Strikingly, selection on learning performance led to the reversal of sexual dimorphism in virgin life span. We thus show sex-specific trade-offs between learning, reproduction, and life span. Our results support the hypothesis that selection on learning performance can shape the evolution of sexually dimorphic life histories via sex-specific genetic correlations.

Keyword
Caenorhabditis, cognition, intralocus sexual conflict, olfactory learning, sex-specific life histories
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-282325 (URN)10.1111/evo.12862 (DOI)000370662500007 ()26787139 (PubMedID)
Available from: 2016-04-05 Created: 2016-04-05 Last updated: 2017-11-30Bibliographically approved
3. Experimental evolution of slowed cognitive aging in Drosophila melanogaster
Open this publication in new window or tab >>Experimental evolution of slowed cognitive aging in Drosophila melanogaster
2017 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 71, no 3, 662-670 p.Article in journal (Refereed) Published
Abstract [en]

Reproductive output and cognitive performance decline in parallel during aging, but it is unknown whether this reflects a shared genetic architecture or merely the declining force of natural selection acting independently on both traits. We used experimental evolution in Drosophila melanogaster to test for the presence of genetic variation for slowed cognitive aging, and assess its independence from that responsible for other traits' decline with age. Replicate experimental populations experienced either joint selection on learning and reproduction at old age (Old + Learning), selection on late-life reproduction alone (Old), or a standard two-week culture regime (Young). Within 20 generations, the Old + Learning populations evolved a slower decline in learning with age than both the Old and Young populations, revealing genetic variation for cognitive aging. We found little evidence for a genetic correlation between cognitive and demographic aging: although the Old + Learning populations tended to show higher late-life fecundity than Old populations, they did not live longer. Likewise, selection for late reproduction alone did not result in improved late-life learning. Our results demonstrate that Drosophila harbor genetic variation for cognitive aging that is largely independent from genetic variation for demographic aging and suggest that these two aspects of aging may not necessarily follow the same trajectories.

Place, publisher, year, edition, pages
WILEY, 2017
Keyword
Cognitive aging, Drosophila, experimental evolution, genetic architecture, learning, trade-off
National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-320841 (URN)10.1111/evo.13156 (DOI)000396039000011 ()28000915 (PubMedID)
Funder
The Royal Swedish Academy of SciencesSwedish Research CouncilEU, European Research Council
Available from: 2017-04-26 Created: 2017-04-26 Last updated: 2017-09-07Bibliographically approved
4. Sex-specific Tradeoffs With Growth and Fitness Following Life-span Extension by Rapamycin in an Outcrossing Nematode, Caenorhabditis remanei
Open this publication in new window or tab >>Sex-specific Tradeoffs With Growth and Fitness Following Life-span Extension by Rapamycin in an Outcrossing Nematode, Caenorhabditis remanei
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2016 (English)In: The journals of gerontology. Series A, Biological sciences and medical sciences, ISSN 1079-5006, E-ISSN 1758-535X, Vol. 71, no 7, 882-890 p.Article in journal (Refereed) Published
Abstract [en]

Rapamycin inhibits the nutrient-sensing TOR pathway and extends life span in a wide range of organisms. Although life-span extension usually differs between the sexes, the reason for this is poorly understood. Because TOR influences growth, rapamycin likely affects life-history traits such as growth and reproduction. Sexes have different life-history strategies, and theory predicts that they will resolve the tradeoffs between growth, reproduction, and life span differently. Specifically, in taxa with female-biased sexual size dimorphism, reduced growth may have smaller effects on male fitness. We investigated the effects of juvenile, adult, or life-long rapamycin treatment on growth, reproduction, life span, and individual fitness in the outcrossing nematode Caenorhabditis remanei. Life-long exposure to rapamycin always resulted in the strongest response, whereas postreproductive exposure did not affect life span. Although rapamycin resulted in longer life span and smaller size in males, male individual fitness was not affected. In contrast, size and fitness were negatively affected in females, whereas life span was only extended under high rapamycin concentrations. Our results support the hypothesis that rapamycin affects key life-history traits in a sex-specific manner. We argue that the fitness cost of life-span extension will be sex specific and propose that the smaller sex generally pay less while enjoying stronger life-span increase.

Keyword
Antiaging, Evolution, Longevity
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-304528 (URN)10.1093/gerona/glv174 (DOI)000381209900006 ()26472877 (PubMedID)
Funder
Swedish Research Council, C0636601, 621-2013-4828EU, European Research Council, St-G 2010 AGINGSEXDIFF 260885
Available from: 2016-10-12 Created: 2016-10-06 Last updated: 2017-11-29Bibliographically approved
5. Fitness-associated dispersal: selection for increased dispersal results in lower fitness
Open this publication in new window or tab >>Fitness-associated dispersal: selection for increased dispersal results in lower fitness
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(English)Manuscript (preprint) (Other academic)
Keyword
fitness-associated dispersal, dispersal syndromes, artificial selection, life-history theory, Caenorhabdtitis
National Category
Natural Sciences
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-329033 (URN)
Available from: 2017-09-06 Created: 2017-09-06 Last updated: 2017-09-07

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