American Society of Naturalists

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“Parental age effects and the evolution of senescence”

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Patrick M. Barks and Robert A. Laird (May 2020)

Parental age effects on offspring quality modify predictions from classic evolutionary theory on senescence

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Parental age effects shape the evolution of ageing

An old, dying frond of common duckweed (<i>Lemna minor</i>) (right), and its final daughter (left).<br />(Credit: Patrick Barks)
An old, dying frond of common duckweed (Lemna minor) (right), and its final daughter (left).
(Credit: Patrick Barks)

Across the tree of life, individuals of many species are subject to age-related deterioration, colloquially known as ‘ageing’. At the extreme end of the ageing spectrum are organisms like Pacific salmon, mayflies, and certain species of bamboo, which rapidly deteriorate and die following a single bout of reproduction. At the opposite end are organisms whose rates of survival and reproduction remain stable or even increase throughout adulthood, like certain types of molluscs, tortoises and coniferous trees. While there exists a great deal of evolutionary theory to explain why ageing might evolve in the first place, evolutionary biologists have a limited understanding of the factors that shape variation in rates of ageing, both within and among species.

Researchers Patrick Barks and Robert Laird, working at the University of Lethbridge in Alberta, Canada, developed a mathematical model to investigate how rates of ageing may be shaped by a phenomenon known as a ‘parental age effect’, which occurs when offspring fitness consistently changes with parental age. For example, in some species, parents may gain experience or better territories as they age, leading to increases in offspring fitness with parental age. In other species, like members of the aquatic plant family known as duckweeds, parental ‘fronds’ tend to produce smaller, less-fecund offspring as they age.

By analyzing models with both real and simulated data, Barks and Laird showed that, for organisms like duckweed in which offspring fitness tends to decline with parental age, natural selection favours stronger age-related declines in parental survival and reproduction (i.e. faster ageing) than would otherwise be expected. Conversely, age-related increases in offspring quality can diminish the strength of selection for age-related deterioration.


Abstract

Most theory on the evolution of senescence implicitly assumes that all offspring are of equal quality. However, in addition to age-related declines in survival and fecundity (classically-defined senescence), many organisms exhibit age-related declines in offspring quality, a phenomenon known as a parental age effect. Theoretical work suggests that parental age effects may alter age-trajectories of selection and therefore shape the evolution of senescence; however, to date, these analyses have been limited to idealized life cycles, and models of maternal care in human populations. To gain a broader understanding of how parental age effects may shape age-trajectories of selection, we extend the classic age-structured population projection model to also account for parental age structure, and apply this model to empirical data from an aquatic plant known to exhibit parental age effects (the duckweed Lemna minor), as well as a diverse set of simulated life cycles. Our results suggest that parental age effects alter predictions from classic theory on the evolution of senescence. Age-related declines in offspring quality reduce the relative value of late-life reproduction, leading to steeper age-related declines in the force of natural selection than would otherwise be expected, and potentially favoring the evolution of more rapid rates of senescence.