Maternal effect senescence and caloric restriction interact to affect fitness through changes in life history timing

Environmental factors and individual attributes, and their interactions, impact survival, growth and reproduction of an individual throughout its life. In the clonal rotifer Brachionus, low food conditions delay reproduction and extend lifespan. This species also exhibits maternal effect senescence; the offspring of older mothers have lower survival and reproductive output. In this paper, we explored the population consequences of the individual-level interaction of maternal age and low food availability. We built matrix population models for both ad libitum and low food treatments, in which individuals are classified both by their age and maternal age. Low food conditions reduced population growth rate ( <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:semantics><mml:mrow><mml:mi>Δ</mml:mi> <mml:mi>λ</mml:mi> <mml:mo>=</mml:mo> <mml:mo>-</mml:mo> <mml:mn>0.0574</mml:mn></mml:mrow> </mml:semantics> </mml:math> ) and shifted the population structure to older maternal ages, but did not detectably impact individual lifetime reproductive output. We analysed hypothetical scenarios in which reduced fertility or survival led to approximately stationary populations that maintained the shape of the difference in demographic rates between the ad libitum and low food treatments. When fertility was reduced, the populations were more evenly distributed across ages and maternal ages, while the lower-survival models showed an increased concentration of individuals in the youngest ages and maternal ages. Using life table response experiment analyses, we compared populations grown under ad libitum and low food conditions in scenarios representing laboratory conditions, reduced fertility and reduced survival. In the laboratory scenario, the reduction in population growth rate under low food conditions is primarily due to decreased fertility in early life. In the lower-fertility scenario, contributions from differences in fertility and survival are more similar, and show trade-offs across both ages and maternal ages. In the lower-survival scenario, the contributions from decreased fertility in early life again dominate the difference in <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:semantics><mml:mrow><mml:mi>λ</mml:mi></mml:mrow> </mml:semantics> </mml:math> . These results demonstrate that processes that potentially benefit individuals (e.g. lifespan extension) may actually reduce fitness and population growth because of links with other demographic changes (e.g. delayed reproduction). Because the interactions of maternal age and low food availability depend on the population structure, the fitness consequences of an environmental change can only be fully understood through analysis that takes into account the entire life cycle.

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Journal
Journal of Animal Ecology
Published
2024-11-26
DOI
https://doi.org/10.1111/1365-2656.14220
Citations
1
Primary Topic
Physiological and biochemical adaptations
Type
article
Field-Weighted Citation Impact
0.46

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article

Maternal effect senescence and caloric restriction interact to affect fitness through changes in life history timing

Christina M. Hernández, Alyssa Liguori, Silke F. van Daalen, Kristin E. Gribble et al.
1 citations
Journal of Animal Ecology
Physiological and biochemical adaptations
0.46
article

Maternal effect senescence and caloric restriction interact to affect fitness through changes in life history timing

Christina M. Hernández, Alyssa Liguori, Silke F. van Daalen, Kristin E. Gribble, Michael G. Neubert, Hal Caswell
article en
1 citations

Abstract

Environmental factors and individual attributes, and their interactions, impact survival, growth and reproduction of an individual throughout its life. In the clonal rotifer Brachionus, low food conditions delay reproduction and extend lifespan. This species also exhibits maternal effect senescence; the offspring of older mothers have lower survival and reproductive output. In this paper, we explored the population consequences of the individual-level interaction of maternal age and low food availability. We built matrix population models for both ad libitum and low food treatments, in which individuals are classified both by their age and maternal age. Low food conditions reduced population growth rate ( <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:semantics><mml:mrow><mml:mi>Δ</mml:mi> <mml:mi>λ</mml:mi> <mml:mo>=</mml:mo> <mml:mo>-</mml:mo> <mml:mn>0.0574</mml:mn></mml:mrow> </mml:semantics> </mml:math> ) and shifted the population structure to older maternal ages, but did not detectably impact individual lifetime reproductive output. We analysed hypothetical scenarios in which reduced fertility or survival led to approximately stationary populations that maintained the shape of the difference in demographic rates between the ad libitum and low food treatments. When fertility was reduced, the populations were more evenly distributed across ages and maternal ages, while the lower-survival models showed an increased concentration of individuals in the youngest ages and maternal ages. Using life table response experiment analyses, we compared populations grown under ad libitum and low food conditions in scenarios representing laboratory conditions, reduced fertility and reduced survival. In the laboratory scenario, the reduction in population growth rate under low food conditions is primarily due to decreased fertility in early life. In the lower-fertility scenario, contributions from differences in fertility and survival are more similar, and show trade-offs across both ages and maternal ages. In the lower-survival scenario, the contributions from decreased fertility in early life again dominate the difference in <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:semantics><mml:mrow><mml:mi>λ</mml:mi></mml:mrow> </mml:semantics> </mml:math> . These results demonstrate that processes that potentially benefit individuals (e.g. lifespan extension) may actually reduce fitness and population growth because of links with other demographic changes (e.g. delayed reproduction). Because the interactions of maternal age and low food availability depend on the population structure, the fitness consequences of an environmental change can only be fully understood through analysis that takes into account the entire life cycle.

Journal of Animal EcologyVol. 94(1)
Marine Biological Laboratory (US), Cornell University (US), Woods Hole Oceanographic Institution (US), University of Amsterdam (NL)
Doherty Foundation, National Institutes of Health, Horizon 2020 Framework Programme, Division of Integrative Organismal Systems, Division of Environmental Biology, H2020 European Research Council
Zero hunger
Openalex Percentile: Top 28%
Physiological and biochemical adaptations
0.46
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