Antagonistic pleiotropy and the evolution of extraordinary lifespans in eusocial organisms

Abstract

Queens of eusocial species live extraordinarily long compared to their workers. So far, it has been argued that these lifespan divergences are readily explained by the classical evolutionary theory of ageing. As workers predominantly perform risky tasks, such as foraging and nest defense, and queens stay in the well‐protected nests, selection against harmful genetic mutations expressed in old age should be weaker in workers than in queens due to caste differences in extrinsic mortality risk, and thus, lead to the evolution of longer queen and shorter worker lifespans. However, these arguments have not been supported by formal models. Here, we present a model for the evolution of caste‐specific ageing in social insects, based on Williams’ antagonistic pleiotropy theory of ageing. In individual‐based simulations, we assume that mutations with antagonistic fitness effects can act within castes, that is, mutations in early life are accompanied by an antagonistic effect acting in later life, or between castes, where antagonistic effects emerge due to caste antagonism or indirect genetic effects between castes. In monogynous social insect species with sterile workers, large lifespan divergences between castes evolved under all different scenarios of antagonistic effects, but regardless of the degree of caste‐specific extrinsic mortality. Mutations with antagonistic fitness effects within castes reduced lifespans of both castes, while mutations with between‐caste antagonistic effects decreased worker lifespans more than queen lifespans, and consequently increased lifespan divergences. Our results challenge the central explanatory role of extrinsic mortality for caste‐specific ageing in eusocial organisms and suggest that antagonistic pleiotropy affects castes differently due to reproductive monopolization by queens, hence, reproductive division of labor. Finally, these findings provide new insights into the evolution of tissue‐specific ageing in multicellular organisms in general.

The evolution of eusociality: Kin selection theory, division of labour models, and evo-devo explanations

“…Empirically, a role of phenotypic plasticity for the production of helping and breedingphenotypes is well-supported by gene expression differences between helpers and breeders in various species of social wasps and bees [180][181][182][183][184][185] . However, the phenotypic divergence of breeders and helpers must also initially be restricted by genetic correlations because breeders and helpers might express the same genes 153,[186][187][188][189][190] . Additionally, this divergence must be restricted in species where helpers have the ability to become the breeder at some point in their life.…”

The evolution of ageing in cooperative breeders

“… 2021 ; Kreider 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.…”

“…The evolution of sociality is associated with changes in life history, especially lifespan [1][2][3] . As demonstrated in birds 4,5 and mole rats 6,7 (though not in mammals in general 8,9 ), cooperatively breeding species often have longer lifespans than solitary species, and the reproductive castes of eusocial insects outlive solitary insects by several orders of magnitude 10 .…”

“…The evolution of sociality is associated with changes in life history, especially lifespan (Kramer et al 2021;Kreider et al 2021;Pen and Flatt 2021). In birds (Arnold and Owens 1998;Downing et al 2015), mole rats (Healy 2015;Williams and Shattuck 2015) (though not in mammals in general; Lukas and Clutton-Brock 2012a; Thorley 2020), and probably in noneusocial social insects (Séguret et al 2016), cooperatively breeding species often have longer lifespans than solitary species.…”

Inclusive fitness forces of selection in an age-structured population

“…Previous theory suggests that it is longer life and overlapping generations that initially favour cooperation (26), but also that a delayed age of first reproduction as a result of queuing for reproduction might be a self-reinforcing mechanism for extended lifespan in cooperative breeders (59). However, multiple other facets of the demography of cooperative breeding systems, including the process of group formation (60), the structure of dominance hierarchies (61) and levels of reproductive skew (62) all have the potential to play a role in determining lifespan and rates of senescence. All have the potential to contribute to the shape of the age class asymptotic frequency and inclusive reproductive value distributions that, as we have shown here, underpin inclusive fitness forces of selection.…”