Growing more positive with age: The relationship between reproduction and survival in aging flies

Joost van den Heuvel; Jelle Zandveld; Paul M Brakefield; Thomas B.L. Kirkwood; Daryl P. Shanley; Bas J. Zwaan

doi:10.1016/j.exger.2017.01.016

Growing more positive with age: The relationship between reproduction and survival in aging flies

Joost van den Heuvel^*, Jelle Zandveld, Paul M Brakefield, Thomas B.L. Kirkwood, Daryl P. Shanley, Bas J. Zwaan

^*Corresponding author for this work

Molecular Aging Program

2 Citations (Scopus)

Abstract

Populations of laboratory animals that are selected for increased lifespan often show negative correlated responses in early fecundity. However, late fecundity and/or total lifetime fecundity can be higher in the populations selected for increased lifespan. This has been interpreted by some as being at odds with the disposable soma theory, which predicts decreased lifespan to increase total reproductive output. Alternatively, the Y–model explores the effects of variation in resource allocation and acquisition on life histories. In this model, a negative relationship between lifespan and reproduction can be viewed as variation in allocation, whereas a positive relationship is the result of variation in acquisition. However, a frequently neglected complication of the Y-model is that older individuals often show a decline in resource acquisition. Therefore, differential allocation to maintenance and survival might affect this decline in late-life acquisition which will affect resource availability across the whole lifespan. In this paper we show that a model which incorporates the ideas of the Y-model, the disposable soma theory, and an age-related decrease in resource acquisition, i.e. feeding senescence, can explain how the relationship between fecundity and lifespan changes with age. Furthermore, by modeling environments with contrasting extrinsic mortality rates, we explored how the outcome of the model depended on the relative importance of early and late-life reproduction. In high mortality environments a relatively higher early fecundity, lower late fecundity, and lower lifespans were more optimal, whereas the opposite was true for low mortality environments. We applied predictions from the model to a cohort of individually-housed female Drosophila melanogaster flies for which we measured age specific fecundity and lifespan. Early fecundity was negatively associated with lifespan, while late fecundity related positively with lifespan in the same cohort. This verified that the mechanism of feeding senescence could explain patterns for age specific relationships between lifespan and fecundity.

Original language	English
Journal	Experimental Gerontology
Volume	90
Pages (from-to)	34-42
Number of pages	9
ISSN	0531-5565
DOIs	https://doi.org/10.1016/j.exger.2017.01.016
Publication status	Published - Apr 2017

Keywords

Disposable soma theory
Dynamic programming
Energy allocation Y-model
Lifespan
Reproduction
Trade-off

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10.1016/j.exger.2017.01.016

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@article{c098b8046e174a818826b9a1c944bfc4,

title = "Growing more positive with age: The relationship between reproduction and survival in aging flies",

abstract = "Populations of laboratory animals that are selected for increased lifespan often show negative correlated responses in early fecundity. However, late fecundity and/or total lifetime fecundity can be higher in the populations selected for increased lifespan. This has been interpreted by some as being at odds with the disposable soma theory, which predicts decreased lifespan to increase total reproductive output. Alternatively, the Y–model explores the effects of variation in resource allocation and acquisition on life histories. In this model, a negative relationship between lifespan and reproduction can be viewed as variation in allocation, whereas a positive relationship is the result of variation in acquisition. However, a frequently neglected complication of the Y-model is that older individuals often show a decline in resource acquisition. Therefore, differential allocation to maintenance and survival might affect this decline in late-life acquisition which will affect resource availability across the whole lifespan. In this paper we show that a model which incorporates the ideas of the Y-model, the disposable soma theory, and an age-related decrease in resource acquisition, i.e. feeding senescence, can explain how the relationship between fecundity and lifespan changes with age. Furthermore, by modeling environments with contrasting extrinsic mortality rates, we explored how the outcome of the model depended on the relative importance of early and late-life reproduction. In high mortality environments a relatively higher early fecundity, lower late fecundity, and lower lifespans were more optimal, whereas the opposite was true for low mortality environments. We applied predictions from the model to a cohort of individually-housed female Drosophila melanogaster flies for which we measured age specific fecundity and lifespan. Early fecundity was negatively associated with lifespan, while late fecundity related positively with lifespan in the same cohort. This verified that the mechanism of feeding senescence could explain patterns for age specific relationships between lifespan and fecundity.",

keywords = "Disposable soma theory, Dynamic programming, Energy allocation Y-model, Lifespan, Reproduction, Trade-off",

author = "{van den Heuvel}, Joost and Jelle Zandveld and Brakefield, {Paul M} and Kirkwood, {Thomas B.L.} and Shanley, {Daryl P.} and Zwaan, {Bas J.}",

year = "2017",

month = apr,

doi = "10.1016/j.exger.2017.01.016",

language = "English",

volume = "90",

pages = "34--42",

journal = "Experimental Gerontology",

issn = "0531-5565",

publisher = "Elsevier",

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TY - JOUR

T1 - Growing more positive with age

T2 - The relationship between reproduction and survival in aging flies

AU - van den Heuvel, Joost

AU - Zandveld, Jelle

AU - Brakefield, Paul M

AU - Kirkwood, Thomas B.L.

AU - Shanley, Daryl P.

AU - Zwaan, Bas J.

PY - 2017/4

Y1 - 2017/4

N2 - Populations of laboratory animals that are selected for increased lifespan often show negative correlated responses in early fecundity. However, late fecundity and/or total lifetime fecundity can be higher in the populations selected for increased lifespan. This has been interpreted by some as being at odds with the disposable soma theory, which predicts decreased lifespan to increase total reproductive output. Alternatively, the Y–model explores the effects of variation in resource allocation and acquisition on life histories. In this model, a negative relationship between lifespan and reproduction can be viewed as variation in allocation, whereas a positive relationship is the result of variation in acquisition. However, a frequently neglected complication of the Y-model is that older individuals often show a decline in resource acquisition. Therefore, differential allocation to maintenance and survival might affect this decline in late-life acquisition which will affect resource availability across the whole lifespan. In this paper we show that a model which incorporates the ideas of the Y-model, the disposable soma theory, and an age-related decrease in resource acquisition, i.e. feeding senescence, can explain how the relationship between fecundity and lifespan changes with age. Furthermore, by modeling environments with contrasting extrinsic mortality rates, we explored how the outcome of the model depended on the relative importance of early and late-life reproduction. In high mortality environments a relatively higher early fecundity, lower late fecundity, and lower lifespans were more optimal, whereas the opposite was true for low mortality environments. We applied predictions from the model to a cohort of individually-housed female Drosophila melanogaster flies for which we measured age specific fecundity and lifespan. Early fecundity was negatively associated with lifespan, while late fecundity related positively with lifespan in the same cohort. This verified that the mechanism of feeding senescence could explain patterns for age specific relationships between lifespan and fecundity.

AB - Populations of laboratory animals that are selected for increased lifespan often show negative correlated responses in early fecundity. However, late fecundity and/or total lifetime fecundity can be higher in the populations selected for increased lifespan. This has been interpreted by some as being at odds with the disposable soma theory, which predicts decreased lifespan to increase total reproductive output. Alternatively, the Y–model explores the effects of variation in resource allocation and acquisition on life histories. In this model, a negative relationship between lifespan and reproduction can be viewed as variation in allocation, whereas a positive relationship is the result of variation in acquisition. However, a frequently neglected complication of the Y-model is that older individuals often show a decline in resource acquisition. Therefore, differential allocation to maintenance and survival might affect this decline in late-life acquisition which will affect resource availability across the whole lifespan. In this paper we show that a model which incorporates the ideas of the Y-model, the disposable soma theory, and an age-related decrease in resource acquisition, i.e. feeding senescence, can explain how the relationship between fecundity and lifespan changes with age. Furthermore, by modeling environments with contrasting extrinsic mortality rates, we explored how the outcome of the model depended on the relative importance of early and late-life reproduction. In high mortality environments a relatively higher early fecundity, lower late fecundity, and lower lifespans were more optimal, whereas the opposite was true for low mortality environments. We applied predictions from the model to a cohort of individually-housed female Drosophila melanogaster flies for which we measured age specific fecundity and lifespan. Early fecundity was negatively associated with lifespan, while late fecundity related positively with lifespan in the same cohort. This verified that the mechanism of feeding senescence could explain patterns for age specific relationships between lifespan and fecundity.

KW - Disposable soma theory

KW - Dynamic programming

KW - Energy allocation Y-model

KW - Lifespan

KW - Reproduction

KW - Trade-off

U2 - 10.1016/j.exger.2017.01.016

DO - 10.1016/j.exger.2017.01.016

M3 - Journal article

C2 - 28122252

AN - SCOPUS:85011025978

SN - 0531-5565

VL - 90

SP - 34

EP - 42

JO - Experimental Gerontology

JF - Experimental Gerontology

ER -

Growing more positive with age: The relationship between reproduction and survival in aging flies

Abstract

Keywords

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