Eusociality and the Evolution of Aging in Superorganisms

Abstract

Eusocial insects-ants, bees, wasps, and termites-are being recognized as model organisms to unravel the evolutionary paradox of aging for two reasons: (1) queens (and kings, in termites) of social insects outlive similarly sized solitary insects by up to several orders of magnitude and (2) all eusocial taxa show a divergence of long queen and shorter worker life spans, despite their shared genomes and even under risk-free laboratory environments. Traditionally, these observations have been explained by invoking the classical evolutionary aging theory: well-protected inside their nests, queens are much less exposed to external hazards than foraging workers, and this provides natural selection the opportunity to favor queens that perform well at advanced ages. Although quite plausible, these verbal arguments have not been backed up by mathematical analysis. Here, for the first time, we provide quantitative models for the evolution of caste-specific aging patterns. We show that caste-specific mortality risks are in general neither sufficient nor necessary to explain the evolutionary divergence in life span between queens and workers and the extraordinary queen life spans. Reproductive monopolization and the delayed production of sexual offspring in highly social colonies lead natural selection to inherently favor queens that live much longer than workers, even when exposed to the same external hazards. Factors that reduce a colony's reproductive skew, such as polygyny and worker reproduction, tend to reduce the evolutionary divergence in life span between queens and workers. Caste-specific extrinsic hazards also affect life span divergence, but to a much smaller extent than reproductive monopolization.

The evolution of ageing in cooperative breeders

“…Additionally, queens of eusocial insects typically only produce reproductive offspring after an extended period of producing workers and thus investing in colony growth (Kramer et al 2016;Jaimes-Nino et al 2022). As our model predicts for cooperative breeders, such a delay of the production of reproductive offspring should impose strong selection against mortality even at advanced ages, potentially explaining the extraordinarily long lifespans of eusocial insect queens and kings (in termites) (Keller and Genoud 1997;Kramer et al 2021;. Furthermore, following the logic from our model, we predict that, in eusocial organisms with high relatedness between queens and workers, workers should be more long-lived than in species where relatedness between queens and workers is lower, for example, through multiple mating of queens (Kramer et al 2021).…”

“…As our model predicts for cooperative breeders, such a delay of the production of reproductive offspring should impose strong selection against mortality even at advanced ages, potentially explaining the extraordinarily long lifespans of eusocial insect queens and kings (in termites) (Keller and Genoud 1997;Kramer et al 2021;. Furthermore, following the logic from our model, we predict that, in eusocial organisms with high relatedness between queens and workers, workers should be more long-lived than in species where relatedness between queens and workers is lower, for example, through multiple mating of queens (Kramer et al 2021). This is because the strength of natural selection should scale positively with the amount of indirect fitness that can be gained through helping.…”

The indispensable soma of Cardiocondyla obscurior ants

“…It has also been argued that in species with multiple queen colonies such as C. obscurior , new cohorts of workers produced by young queens can outnumber older workers, decreasing the average relatedness of workers to the previous generations of queens. This increases the risk of queens being “dismissed” earlier by younger worker cohorts and may select for shorter lifespans in queens of polygynous species (Boomsma et al, 2014; Kramer et al, 2022). However, C. obscurior shows no signs of conflict between castes over sex or caste allocation (De Menten et al, 2005; Schultner et al, 2021) in contrast to many other ants (Heinze, 2004), speaking against this adaptationist explanation.…”

“…The presumed universality of queen/worker lifespan divergence in ants, if true (~130MYR evolution, ~14.000 species), provokes the question why queens do not live longer (or workers shorter) in C. obscurior. While it seems futile to speculate without more data from more species for perspective, one explanation may be that this ant does not display traits thought to be associated with the evolution of lifespan divergence between castes, including extreme size polyphenism, colonies headed by single, highly fertile queens, and large colony sizes (Kramer et al, 2022;Kramer and Schaible, 2013b). It has also been argued that in species with multiple queen colonies such as C. obscurior, new cohorts of workers produced by young queens can outnumber older workers, decreasing the average relatedness of workers to the previous generations of queens.…”

“…As progress is made in understanding aging in ant queens, the aging patterns of workers remain largely unknown. Anecdotal references such as “mother queens live much longer than workers in all groups of ants” (Hölldobler and Wilson, 1990), and “all eusocial taxa show a divergence of long queen and shorter worker life spans, despite their shared genomes and even under risk-free laboratory environments” (Kramer et al, 2022) have been made. However, studies of worker lifespan lacked age-controlled cohorts (Chapuisat and Keller, 2002; Gordon and Hölldobler, 1987; Modlmeier et al, 2013; Negroni et al, 2021; Schmid-Hempel and Schmid-Hempel, 1984), surveyed marked individuals in the field without distinguishing between extrinsic and intrinsic mortality (Calabi and Porter, 1989; Gordon and Hölldobler, 1987; Schmid-Hempel and Schmid-Hempel, 1984), or monitored lifespan of temperate species with artificial hibernation (Kramer et al, 2016).…”