Late-life fitness gains and reproductive death in Cardiocondyla obscurior ants

Abstract

A key hypothesis for the occurrence of senescence is the decrease in selection strength due to the decrease in the proportion of newborns from parents attaining an advanced age – the so-called selection shadow. Strikingly, queens of social insects have long lifespans and reproductive senescence seems to be negligible. By lifelong tracking of 99 Cardiocondyla obscurior (Formicidae: Myrmicinae) ant colonies, we find that queens shift to the production of sexuals in late life regardless of their absolute lifespan or the number of workers present. Furthermore, RNAseq analyses of old queens past their peak of reproductive performance showed the development of massive pathology while queens were still fertile, leading to rapid death. We conclude that the evolution of superorganismality is accompanied by ‘continuusparity,’ a life history strategy that is distinct from other iteroparous and semelparous strategies across the tree of life, in that it combines continuous reproduction with a fitness peak late in life.

Assisted dispersal and reproductive success in an ant species with matchmaking

“…Their higher mortality matches the finding that in social insects mating and reproduction increase life expectancy (e.g., Hartmann & Heinze, 2003;Schrempf, Reber, et al, 2005), in contrast to many solitary insects, in which virgins outlive reproductively active, mated females (e.g., Chapman et al, 1998;Limberger et al, 2021;Service, 1989). A positive association between fecundity and longevity appears to be a trait associated with the evolution of perennial insect societies (e.g., Jaimes-Niño et al, 2022;Parker, 2010;Rodrigues & Flatt, 2016).…”

Assisted dispersal and reproductive success in an ant species with matchmaking

“…Their higher mortality matches the finding that in social insects mating and reproduction increase life expectancy (e.g., Hartmann & Heinze, 2003 ; Schrempf, Heinze, et al, 2005 ; Schrempf, Reber, et al, 2005 ), in contrast to many solitary insects, in which virgins outlive reproductively active, mated females (e.g., Chapman et al, 1998 ; Limberger et al, 2021 ; Service, 1989 ). A positive association between fecundity and longevity appears to be a trait associated with the evolution of perennial insect societies (e.g., Jaimes‐Niño et al, 2022 ; Parker, 2010 ; Rodrigues & Flatt, 2016 ).…”

Maternal control over caste allocation in the ant Cardiocondyla obscurior

“…Inbreeding results in particularly high levels of relatedness, and consequently decreased conflict potential within colonies. C. obscurior moreover has a relatively low degree of dimorphism between sexuals and workers [48,65] and queens only have six ovarioles, producing about 1-2 eggs per day and an average of 350 eggs over the course of their lives [29]. Accordingly, colonies are small and contain on average one to several queens and ∼30 workers [65]).…”

“…In Cardiocondyla obscurior , workers further refrain from manipulating brood sex ratios, giving queens control over colony-level sex allocation [27,28]. Recently, we found that in single queen colonies of this ant, production of new queens increases as the resident queen ages, irrespective of absolute queen fitness, queen lifespan or colony size [29]. This suggests that queens also control caste allocation, and points towards relaxed selection on potentially costly traits related to caste allocation conflict.…”