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.