Incorporating effects of age on energy dynamics predicts nonlinear maternal allocation patterns in iteroparous animals.

Antoine M G Barreaux,Andrew D Higginson,Michael B Bonsall,Sinead English

doi:10.1098/rspb.2021.1884

Abstract

Iteroparous parents face a trade-off between allocating current resources to reproduction versus maximizing survival to produce further offspring. Parental allocation varies across age and follows a hump-shaped pattern across diverse taxa, including mammals, birds and invertebrates. This nonlinear allocation pattern lacks a general theoretical explanation, potentially because most studies focus on offspring number rather than quality and do not incorporate uncertainty or age-dependence in energy intake or costs. Here, we develop a life-history model of maternal allocation in iteroparous animals. We identify the optimal allocation strategy in response to stochasticity when energetic costs, feeding success, energy intake and environmentally driven mortality risk are age-dependent. As a case study, we use tsetse, a viviparous insect that produces one offspring per reproductive attempt and relies on an uncertain food supply of vertebrate blood. Diverse scenarios generate a hump-shaped allocation when energetic costs and energy intake increase with age and also when energy intake decreases and energetic costs increase or decrease. Feeding success and environmentally driven mortality risk have little influence on age-dependence in allocation. We conclude that ubiquitous evidence for age-dependence in these influential traits can explain the prevalence of nonlinear maternal allocation across diverse taxonomic groups.

Highlights

Maternal allocation of resources to offspring typically has a positive effect on offspring traits such as longevity and fecundity and thereby offspring fitness [1,2,3,4]
We show that this nonlinear allocation pattern emerges in diverse scenarios, and the wide-ranging empirical evidence for age effects on the traits involved can explain why nonlinear allocation is found across numerous iteroparous animals
Our model predicts that optimal maternal allocation of resources is nonlinear with age, when there is age-dependence in key drivers of energy dynamics

Summary

Introduction

Maternal allocation of resources to offspring typically has a positive effect on offspring traits such as longevity and fecundity and thereby offspring fitness [1,2,3,4]. Maternal physiological state influences this allocation trade-off, and maternal state can vary with age, as foraging efficiency may decrease [9], physiological functions decline and cellular damage accumulates [10,11,12,13], with the result that mothers can face an increased risk of death as they get older [1,14]. Maternal allocation tends to decline with age, termed reproductive senescence [10,15,16] Explanations of such senescence are based on the declining strength of natural selection with age [6], permitting the accumulation of deleterious mutations [17] or the fixation of alleles with a pleiotropic effect that favour fitness early in life but have negative effects later on [18]. Reproductive restraint in later life may be an adaptive strategy to cope with the accumulation of reproductive damage and the associated increase in mortality [20]

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