Extraordinary lifespans in ants: a test of evolutionary theories of ageing

Abstract

Senescence presents not only a medical problem, but also an evolutionary paradox because it should be opposed by natural selection. Evolutionary hypotheses propose that ageing evolves as the necessary cost of processes increasing early reproductive success 1,2 , or because of weaker selection against late-acting mutations 3 . A prediction of these hypotheses is that the rate of ageing should increase and the average lifespan decrease as the rate of extrinsic mortality increases 1-7 . Alternatively, non-adaptive, purely mechanistic hypotheses invoke damage to DNA, cells, tissues and organs as being the unique cause of senescence and ineluctable death of organisms 8 . Here we show that the evolution of eusociality is associated with a 100-fold increase in insect lifespan. Such an increase is predicted by evolutionary theories because termite, bee and ant queens live in colonies that are sheltered and heavily defended against predators. Moreover, a comparison of ants with contrasting life histories also reveals an association between lifespan and extrinsic rate of mortality. These results provide strong support for evolutionary theories of ageing, as purely mechanistic hypotheses of senescence do not propose any association between the rate of extrinsic mortality and lifespans.The physiological deterioration of organisms as they age presents an evolutionary paradox: if organisms can function well in youth, why can they not continue to do so in old age 5 ? Evolutionary and non-adaptive, purely mechanistic hypotheses have been developed separately to account for the apparently universal occurrence of ageing in vertebrates and arthropods 2 and, with the exception of some experimental studies conducted with several Drosophila species, few attempts have been made to distinguish them 2,9 . Evolutionary hypotheses predict that ageing rate should generally increase and average lifespan should decrease as the rate of age-and condition-independent (extrinsic) mortality increases and that it should be higher in those organisms whose fecundity does not increase markedly after maturity compared to those showing such an increase 1,3-6,10 . In contrast, and all else being equal, purely physiological theories of senescence predict no relationship between extrinsic mortality, age-dependent fecundity, and rate of senescence. Instead, they frequently predict an association between duration of life and metabolic rate, whereby organisms with lower metabolic rates should have greater lifespans 8,11 . It is important to note that evolutionary hypotheses do not deny that proximate mechanisms such as DNA damage are responsible for ageing: they only predict that natural selection will act on these proximate mechanisms. For example, a lower rate of extrinsic mortality should decrease the frequency of late-acting genes that reduce the efficiency of DNA repair and cause greater DNA damage.Owing to their peculiar life history, highly eusocial insects with specialized worker and queen morphological castes (ants, termites and the honeybee) provid...

Intergenerational transfers may have decoupled physiological and chronological age in a eusocial insect

“…Yet, the hypothesis that stage-dependent senescence in worker bees is the outcome of selection on transfers does not provide useful information about the evolutionary trajectory of aging in queens and drones (see Keller and Genoud (1997) for more information on the longevity of social insect queens). Moreover, the idea does not present a mechanistic basis for honey bee senescence.…”

“…This may imply that the vitellogenin concentration of a bee communicates the level of investment embodied in her; or equivalently, if the bees' trajectories of transfers and mortality are joined at the physiological level through the functions of vitellogenin, the protein may exemplify an evolutionary end point connection between investments, transfers and senescence. Yet, future research on social invertebrates, including ants that represent another major eusocial model for aging and longevity (Keller and Genoud, 1997;Chapuisat and Keller, 2002), is needed to establish whether resource transfers have been of importance for the evolution of senescence in social insects. Temporal transfer dynamics in honey bee workers.…”

Senescence in the worker honey bee Apis Mellifera

“…E-mail: kahughes@life.uiuc.edu. E-mail addresses: remolina@uiuc.edu, dhafez@uiuc.edu, generobi@life.uiuc.edu, kahughes@life.uiuc.edu. longer lifespans than the non-reproductive workers (Winston, 1987;Keller and Genoud, 1997;Page and Peng, 2001). Strikingly, the long life of social insect queens does not come at the cost of low reproduction: queens of many social insects lay hundreds or thousands of eggs per day throughout their adult life.…”

Age, caste, and behavior determine the replicative activity of intestinal stem cells in honeybees (Apis mellifera L.)

“…Naturally occurring plasticity in aging and lifespan variation has recently attracted considerable interest because it may lead to the discovery of longevity mechanisms that have not been revealed by classic genetic or pharmacological approaches ( [Keller and Genoud, 1997], [Tatar and Yin, 2001], [Gardner et al, 2006] and [Jaureguy and Etges, 2007]). Furthermore, aging plasticity, apparent as intra-specific variation in life expectancy, is the rule rather than the exception: species have not only evolved an average lifespan but also a certain degree of plasticity in response to social or environmental selection ( [Carey, 2001] and [Carey et al, 2005]).…”