Introduction
Across the natural world, it is commonly observed that as individuals
get older, they are more likely to die and invest less in their
offspring (Nussey et al. 2013; Hoekstra et al. 2019;
Zajitschek et al. 2019). Broad patterns of senescence have been
well described for a wide range of taxa (Nussey et al. 2013;
Hoekstra et al. 2019; Zajitschek et al. 2019), and
extensive variation in the onset and rate of ageing, both within and
across populations, has also been observed (Holand et al. 2016;
Rodríguez-Muñoz et al. 2019; Cayuela et al. 2020). The
drivers of senescence and the causes of variation in the timing and
intensity of the ageing process are only just beginning to be determined
(Gaillard & Lemaître 2019).
Life-history theory predicts that senescence is driven by trade-offs
between reproduction and other physiological processes (Kirkwood 1977;
Boggs 2009; Baudisch & Vaupel 2012; Davison et al. 2014). A
central argument to this theory is that resources are limited and must
be allocated either to reproduction or somatic maintenance (Partridge
1987; Boggs 2009). Reproductive senescence could also, however, occur
through physiological damage incurred directly from reproduction, or be
adaptive to prolong survival (McNamara et al. 2009).
Controlled experiments are useful for quantifying patterns of senescence
and identifying causal factors. Experiments where the age at which
females are mated and their access to resources can be varied contribute
to tests of whether reproduction causes senescence, either directly or
by resource allocation trade-offs. In testing various senescence
hypotheses, insects are useful organisms as they have relatively short
generation times, can be reared in large numbers, and access to mates
and resources can be easily manipulated.
By varying the age at which females were mated, experiments with
Lepidoptera have shown that delayed mating reduces fecundity but extends
longevity (Unnithan & Paye 1991; Jiménez-Pérez & Wang 2009). However,
virgin females still produce eggs, and in these studies, females of the
same age but mated at different times were not compared. The effects of
reproduction on reproductive senescence cannot therefore be fully
evaluated using these data.
By manipulating nutrition, researchers have shown that, generally,
females with access to fewer resources have lower overall reproductive
output but longer lifespan (De Sousza Santos & Begon 1987; Ernsting &
Isaaks 1991; Kaitala 1991; Chippindale et al. 1993; Tatar &
Carey 1995; Curtis Creighton et al. 2009). These studies support
the theory that senescence is caused, at least in part, by either direct
or indirect costs of reproduction. To our knowledge, no studies have
compared reproductive output of females of the same age, but mated at
different ages, in the same experiment as females under nutritional
stress, to compare directly the contributions of reproductive history
and resource availability on reproductive senescence.
Here, we present a study on senescence in tsetse flies (Glossinaspecies), where we quantify the effects of maternal age on offspring
quality, under nutritional stress, delayed mating and control (standard
insectary) conditions. Tsetse are vectors of human and animal
trypanosomiasis in Africa. They have an unusual reproductive ecology,
giving birth to a single live larva weighing the same as the mother
(Hargrove & Muzari 2015), approximately every nine days and living for
up to 200 days (Hargrove 2004). With immature stages that receive only
energy and nutrients from the mother and a relatively long adult
lifespan for their small size, tsetse present an alternative model
system to study reproductive and survival senescence.
Evidence for age-related changes in maternal investment in field and
laboratory tsetse is, to date, mixed (Jordan et al. 1969; Langley
& Clutton-Brock 1998; McIntyre & Gooding 1998). Key limitations to
existing studies are that flies were kept only under optimal laboratory
conditions, not tracked individually and frequently grouped across ages.
In this study, we used a novel method of housing tsetse females to
track, for individual mothers, how senescence patterns vary if we
alleviate the costs of reproduction or impose nutritional stress. We
manipulated nutritional stress by feeding adult females on highvs low quality diets and changed reproduction stress by delaying
the age at which females were mated. In each treatment we measured
maternal mortality, reproductive output and offspring survival. We
hypothesised that offspring from older mothers would be of lower quality
and would have lower starvation tolerance. If reproduction contributes
to senescence, either directly by physiological damage or by resource
allocation trade-offs, we hypothesised that: i) mothers mated later
would experience senescence later, and potentially slower senescence;
and ii) nutritionally stressed mothers would have an earlier, and
potentially steeper decline in senescence. Alternatively, if senescence
occurs through physiological damage during reproduction, nutritionally
stressed mothers may senescence more slowly, due to an overall lower
reproductive output.