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

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.

Improved estimates of abortion rates in tsetse (Glossinaspp)

“…Similarly, egg lengths are significantly shorter in these age categories. These results are consistent with laboratory findings (Lord et al 2021) and with the predictions of an evolutionary model (Barreaux et al, 2022). The field results provide no support, however, for the laboratory finding that abortion rates increase among the oldest females – cf Fig.…”

“…Similarly, the theoretical prediction (Barreaux et al, 2022) that pupal size should decrease in older tsetse is not supported by field results (English et al, 2016; Hargrove et al, 2018). Barreaux et al (2022) noted the danger of relying solely on results based on laboratory flies and the current work reinforces that concern.…”

Age‐dependent changes in reproductive allocation in a facultative ectoparasite, the blowfly Lucilia sericata (Meigen) (Calliphoridae)

“…Alternatively, young individuals with high opportunity for future reproduction might allocate less to current reproduction to maximize future reproduction, and organisms may increase their investment in reproduction as they approach the end of their life (termed ‘terminal investment’) and have low prospects of future survival (Creighton et al, 2009). These various drivers of age‐dependent allocation are not mutually exclusive and can combine to form an inverse U‐shaped pattern of increase and then decline (Barreaux et al, 2022), as observed across multiple taxa (Monaghan et al, 2020).…”

Lipid metabolism dysfunction following symbiont elimination is linked to altered Kennedy pathway homeostasis

“…Following birth, the milk glands rapidly involute and lipid reserves accumulate to support a subsequent offspring (Attardo et al, 2012; Baumann et al, 2013; Benoit et al, 2018). Tsetse mothers endure this metabolically intense K-selected reproductive strategy continuously through their adulthood, ultimately birthing up to 8-12 larvae per lifetime (Barreaux et al, 2022; Michalkova et al, 2014a).…”

“…Reproduction represents an evolutionarily imperative and metabolically taxing physiological process for all animals (Flatt, 2011; Perrin and Sibly, 1993). This may be especially true for insects, which maintain a high reproductive rate, even though progeny quality declines throughout adulthood (Barreaux et al, 2022; Michalkova et al, 2014a). One such insect is the tsetse fly, Glossina spp ., which reproduces via a process called ‘adenotrophic viviparity’ (gland fed, live birth (Benoit et al, 2015)).…”