Factors driving eusocial insect caste lifespan differences
As aging is linked to increased mortality and decreased reproductive
success, the evolutionary theory of aging explains aging as a
non-adaptive outcome of individual’s declining ability to maintain
fitness at older ages, which leads to the accumulation of harmful
mutations in old age (Haldane 1941; Medawar 1952; Flatt T and Partridge
L 2018). Based on natural selection, theories of evolution attempt to
explain how organisms achieve maximal genetic contribution to the future
genetic pool. However, fitness maximization is limited by certain
evolutionary constraints, such as multiple life-history trade-offs
(Williams 1957; Stearns 1989). The trade-offs act as negative
correlations between the fitness components when an improvement in one
component is associated with a decrement in another, based on the
competitive allocation of limited resources (Fabian and Flatt 2014).
According to the disposable soma theory of aging, one of the major
trade-offs is the cost of reproduction, which is the phenomenon by which
an increased rate of reproduction reduces soma maintenance and,
consequently, longevity (Reznick 1985; Harshman and Zera 2006).
Insect species differ greatly in terms of fecundity and lifespan;
lifetime fecundity in insects ranges from less than ten to several
million eggs, while adult lifespan varies from days to decades. Most
non-social insect species lay tens or hundreds of eggs, and a small
fraction lay thousands (Brueland 1995). The highest lifetime fecundity
among non-social insects was reported in the Australian ghost moth,Trictena atripalpis (Hepialidae), which lays approximately 29,100
eggs (Tindale 1932). The high fecundity in non-social insect species
appears to be associated with a risky oviposition strategy and high
juvenile mortality (Brueland 1995). When compared to non-social insects,
most eusocial insect species have extremely high fecundity as a single
queen can lay hundreds of millions of eggs in a lifetime. For example,
the honeybee queen, with a lifespan of about 5 years, can lay up to
200,000 eggs per year (Bodenheimer and Nerya 1937); the queen of the
army ant Eciton burchelli , with a lifespan of up to 30 years, can
lay 100,000 eggs in three weeks (Gotwald 1995; Boswell et al. 1998); or
the queen of the termite Macrotermes subhyalinus can produce
3,600 eggs in 24 hours over her 20-year lifespan (Keller 1998; Khan et
al. 2022).
Comparative analysis between the lifespan of eusocial reproductives and
solitary insects has indicated that the evolution of eusociality is
associated with a roughly 100-fold increase in longevity between queens
and solitary females (Keller and Genoud 1997). The reproductive
individuals of many termite or ant species may live for many decades
(Keller and Genoud 1997; Keller 1998). For example, the mean average
lifespans of honeybee queens is 5.6 years, while adults of solitary
insect species exhibit lifespans of only 0.1 ± 0.2 years (Keller and
Genoud 1997; Keller 1998). As a result, it appears that the reproductive
individuals in eusocial insect colonies contradict the reversed
reproduction-longevity trade-off because they are both highly fecund and
live longer than non-reproductives within their own colonies or solitary
insect individuals.
First, it is known that variation in nutrition can have an impact on
division of labor and the development of reproductive vs
non-reproductive castes in both advanced eusocial insects with
morphologically distinct castes and social species where all individuals
are capable of mating and reproducing (totipotent at birth), and
nutritional stress can be conceptualized as a mechanism to control
reproductive potential (Smith et al. 2011; Slater et al. 2020). Further,
it has long been suspected that the lifespan disparity in eusocial
insects is associated with caste differences in extrinsic mortality risk
because workers, unlike reproductives, primarily perform risky tasks and
are subjected to a variety of stressful factors (Kramer and Schaible
2013). However, according to recent findings and supporting by the
disposable soma theory of ageing (Kirkwood 1977; Kreider et al. 2021),
when castes are exposed to antagonistic fitness effects, allocation of
limited resources by workers to queens results in accumulation of
deleterious mutational effects preferentially in workers. As a result,
it appears that extrinsic mortality may be only a minor factor in
caste-specific lifespan divergence, and that caste-specific lifespan
differences evolved as a result of antagonistic effects caused by
reproductive division of labor (Kreider et al. 2021). Furthermore,
interspecific variation in queen lifespan and fecundity is linked to
differences in alternative reproductive strategies observed in different
species, such as polygyny (colonies with multiple reproductive queens)
or monogyny (colonies with only one reproductive queen) in ants.
Comparison of different ant species revealed that monogynous queens have
a longer lifespan than that of polygynous queens, despite having their
equal morphology, colony founding mode, and extrinsic mortalities
(Keller and Genoud 1997; Schrempf et al. 2011), and that mating has a
positive effect on lifespan and the lifetime reproductive success of
queens (Schrempf et al. 2005). Finally, contrary to the common
observation that reproductive performance declines with age, sociality
in insects has been linked to a positive correlation between fecundity
and age (Keller and Genoud 1997; Lopez-Vaamonde et al. 2009; Heinze and
Schrempf 2012). This demonstrates that the social environment has a
significant impact on aging of social insects.