American Society of Naturalists

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“Adaptive maternal investment in the wild? Links between maternal growth trajectory and offspring size, growth, and survival in contrasting environments”

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Tim Burton, Njal Rollinson, Simon McKelvey, David C. Stewart, John D. Armstrong, and Neil B. Metcalfe (Apr 2020)

Maternal growth trajectory influences offspring growth & survival independently of variation in initial offspring size

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Slow-growing mothers produce large, slow-growing young that survive better in tough environments

Electrofishing for juvenile Atlantic salmon (<i>Salmo salar</i>) in a tributary stream of the River Conon (Scotland, UK). Researchers show that female salmon who grew at a fast rate when they were juveniles themselves, produce small young that can grow more rapidly than the larger young of slower growing mothers. This growth advantage comes at a cost: the young of fast-growing mothers have poorer prospects of survival when the density of predatory brown trout is high.<br />(Credit: Tim Burton)
Electrofishing for juvenile Atlantic salmon (Salmo salar) in a tributary stream of the River Conon (Scotland, UK). Researchers show that female salmon who grew at a fast rate when they were juveniles themselves, produce small young that can grow more rapidly than the larger young of slower growing mothers. This growth advantage comes at a cost: the young of fast-growing mothers have poorer prospects of survival when the density of predatory brown trout is high.
(Credit: Tim Burton)

Mothers often choose between producing many young that are small or fewer young that are large. In addition to this trade-off between offspring ‘quantity and quality’, recent studies have shown that mothers influence additional traits of their young, e.g. their behavior or rate of growth, and can use their own experience as juveniles to inform this decision. This is expected to occur in species where the environment experienced by mothers when they were juveniles can reliably ‘predict’ the type of environment to be faced by their developing young. Atlantic salmon may be a species where such cross-generational phenomena occur, because females home with great accuracy to spawn their eggs in nests, hidden in the gravel of the very same freshwater streams where they grew up themselves. Researchers from the University of Glasgow, University of Toronto, and Marine Scotland manipulated nutrient levels (and thus productivity) in tributary streams of the River Conon in north Scotland to investigate if female salmon who grew slowly when they were young (and thus likely experienced a unproductive nursery environment) would produce young ‘tailored’ to such conditions themselves. The young of slower-growing mothers were larger and grew more slowly than those of faster-growing mothers, irrespective of stream nutrient levels. However, the young of slow-growing mothers had higher survival prospects in streams where the density of predatory brown trout was high. Intriguingly, these links between growth trajectory of the mother and the survival of her young occurred independently of differences in the initial size of eggs from which these juveniles hatched. This suggests that female salmon may also be adjusting aspects of their young other than their size to better prepare them for the environment they will face in early life.


Abstract

Life history theory predicts that investment per offspring should correlate negatively with the quality of environment offspring are anticipated to encounter; parents may use their own experience as juveniles to predict this environment and may modulate offspring traits such as growth capacity as well as initial size. We manipulated nutrient levels in the juvenile habitat of wild Atlantic salmon Salmo salar to investigate the hypothesis that the egg size maximizing juvenile growth and survival depends on environmental quality. We also tested whether offspring traits were related to parental growth trajectory. Mothers that grew fast when young produced more, smaller offspring than mothers that had grown slowly to reach the same size. Despite their size disadvantage, offspring of faster-growing mothers grew faster than those of slow-growing mothers in all environments, counter to the expectation that they would be competitively disadvantaged. However, they had lower relative survival in environments where the density of older predatory/competitor fish was relatively high. These links between maternal (but not paternal) growth trajectory and offspring survival rate were independent of egg size, underscoring that mothers may be adjusting egg traits other than size to suit the anticipated environment faced by their offspring.