Kreider Jan J, Pen Ido, Kramer Boris H
Theoretical Research in Evolutionary Life Sciences, Groningen Institute for Evolutionary Life Sciences University of Groningen Nijenborgh 7 Groningen 9747 AG The Netherlands.
Evol Lett. 2021 May 17;5(3):178-186. doi: 10.1002/evl3.230. eCollection 2021 Jun.
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.
与工蚁相比，群居性物种中的蚁后寿命极长。到目前为止，有人认为这些寿命差异很容易用经典的衰老进化理论来解释。由于工蚁主要执行危险任务，如觅食和巢穴防御，而蚁后待在受到良好保护的巢穴中，由于外在死亡风险的等级差异，针对老年期表达的有害基因突变的选择在工蚁中应比在蚁后中更弱，因此导致蚁后寿命延长和工蚁寿命缩短的进化。然而，这些观点尚未得到正式模型的支持。在此，我们基于威廉姆斯的衰老拮抗多效性理论，提出了一个关于社会性昆虫特定等级衰老进化的模型。在基于个体的模拟中，我们假设具有拮抗适合度效应的突变可以在等级内起作用，即生命早期的突变伴随着在生命后期起作用的拮抗效应，或者在等级之间起作用，其中拮抗效应由于等级拮抗或等级之间的间接遗传效应而出现。在具有不育工蚁的单蚁后社会性昆虫物种中，在所有不同的拮抗效应场景下，等级之间都出现了很大的寿命差异，但与特定等级外在死亡率的程度无关。等级内具有拮抗适合度效应的突变缩短了两个等级的寿命，而等级间具有拮抗效应的突变对工蚁寿命的缩短幅度大于蚁后寿命，从而增加了寿命差异。我们的结果挑战了外在死亡率在群居生物特定等级衰老中的核心解释作用，并表明由于蚁后对繁殖的垄断，即繁殖分工，拮抗多效性对不同等级的影响不同。最后，这些发现总体上为多细胞生物组织特异性衰老的进化提供了新的见解。
