The evolution of ageing in cooperative breeders.

Cooperatively breeding animals live longer than their solitary counterparts. This has been suggested for birds, mole rats, and social insects. A common explanation for these long lifespans is that cooperative breeding evolves more readily in long-lived species because lower mortality reduces the rate of territory turnover and thus leads to a limitation of breeding territories. Here, we reverse this argument and show that-rather than being a cause for its evolution-long lifespans are an evolutionary consequence of cooperative breeding. In evolutionary individual-based simulations, we show that natural selection favors a delayed onset of senescence in cooperative breeders, relative to solitary breeders, because cooperative breeders have a delayed age of first reproduction as helpers wait in a reproductive queue to obtain breeder status. Especially long lifespans evolve in cooperative breeders in which queue positions depend on the helpers' age rank among the helpers within the breeding territory. Furthermore, we show that lower genetic relatedness among group members leads to the evolution of longer lifespans. This is because selection against higher mortality is weaker when mortality reduces competition for breeding between relatives. Our results link the evolutionary theory of ageing with kin selection theory, demonstrating that the evolution of ageing in cooperative breeders is driven by the timing of reproduction and kin structure within breeding territories.

Resource sharing is sufficient for the emergence of division of labour.

Division of labour occurs in a broad range of organisms. Yet, how division of labour can emerge in the absence of pre-existing interindividual differences is poorly understood. Using a simple but realistic model, we show that in a group of initially identical individuals, division of labour emerges spontaneously if returning foragers share part of their resources with other group members. In the absence of resource sharing, individuals follow an activity schedule of alternating between foraging and other tasks. If non-foraging individuals are fed by other individuals, their alternating activity schedule becomes interrupted, leading to task specialisation and the emergence of division of labour. Furthermore, nutritional differences between individuals reinforce division of labour. Such differences can be caused by increased metabolic rates during foraging or by dominance interactions during resource sharing. Our model proposes a plausible mechanism for the self-organised emergence of division of labour in animal groups of initially identical individuals. This mechanism could also play a role for the emergence of division of labour during the major evolutionary transitions to eusociality and multicellularity.

Eusociality and the Evolution of Aging in Superorganisms.

AbstractEusocial 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.

Antagonistic pleiotropy and the evolution of extraordinary lifespans in eusocial organisms.

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.

Oxidative stress and senescence in social insects: a significant but inconsistent link?

The life-prolonging effects of antioxidants have long entered popular culture, but the scientific community still debates whether free radicals and the resulting oxidative stress negatively affect longevity. Social insects are intriguing models for analysing the relationship between oxidative stress and senescence because life histories differ vastly between long-lived reproductives and the genetically similar but short-lived workers. Here, we present the results of an experiment on the accumulation of oxidative damage to proteins, and a comparative analysis of the expression of 20 selected genes commonly involved in managing oxidative damage, across four species of social insects: a termite, two bees and an ant. Although the source of analysed tissue varied across the four species, our results suggest that oxidative stress is a significant factor in senescence and that its manifestation and antioxidant defenses differ among species, making it difficult to find general patterns. More detailed and controlled investigations on why responses to oxidative stress may differ across social species may lead to a better understanding of the relations between oxidative stress, antioxidants, social life history and senescence. This article is part of the theme issue 'Ageing and sociality: why, when and how does sociality change ageing patterns?'

Life history evolution in social insects: a female perspective.

Social insects are known for their unusual life histories with fecund, long-lived queens and sterile, short-lived workers. We review ultimate factors underlying variation in life history strategies in female social insects, whose social life reshapes common trade-offs, such as the one between fecundity and longevity. Interspecific life history variation is associated with colony size, mediated by changes in division of labour and extrinsic mortality. In addition to the ratio of juvenile to adult mortality, social factors such as queen number influence life history trajectories. We discuss two hypotheses explaining why queen fecundity and lifespan is higher in single-queen societies and suggest further research directions on the evolution of life history variation in social insects.

Lifespan divergence between social insect castes: challenges and opportunities for evolutionary theories of aging.

The extraordinarily long lifespans of queens (and kings) in eusocial insects and the strikingly large differences in life expectancy between workers and queens challenge our understanding of the evolution of aging and provide unique opportunities for studying the causes underlying adaptive variation in lifespan within species. Here we review the major evolutionary theories of aging, focusing on their scope and limitations when applied to social insects. We show that reproductive division of labor, interactions between kin, caste-specific gene regulation networks, and the integration of colony-level trade-offs with individual-level trade-offs provide challenges to the classical theories We briefly indicate how these challenges could be met in future models of adaptive phenotypic plasticity in lifespan between and within different castes.

Worker lifespan is an adaptive trait during colony establishment in the long-lived ant Lasius niger.

Eusociality has been recognized as a strong driver of lifespan evolution. While queens show extraordinary lifespans of 20years and more, worker lifespan is short and variable. A recent comparative study found that in eusocial species with larger average colony sizes the disparities in the lifespans of the queen and the worker are also greater, which suggests that lifespan might be an evolved trait. Here, we tested whether the same pattern holds during colony establishment: as colonies grow larger, worker lifespan should decrease. We studied the mortality of lab-reared Lasius niger workers from colonies at two different developmental stages (small and intermediate-sized) in a common garden experiment. Workers were kept in artificial cohorts that differed only with respect to the stage of the colony they were born in. We found that the stage of the birth colony affected the body size and the survival probability of the workers. The workers that had emerged from early stage colonies were smaller and had lower mortality during the first 400days of their life than the workers born in colonies at a later stage. Our results suggest that early stage colonies produce small workers with an increased survival probability. These workers are gradually augmented by larger workers with a decreased survival probability that serve as a redundant workforce with easily replaceable individuals. We doubt that the observed differences in lifespan are driven by differences in body size. Rather, we suspect that physiological mechanisms are the basis for the observed differences in lifespan.

Ant Colonies Do Not Trade-Off Reproduction against Maintenance.

The question on how individuals allocate resources into maintenance and reproduction is one of the central questions in life history theory. Yet, resource allocation into maintenance on the organismic level can only be measured indirectly. This is different in a social insect colony, a "superorganism" where workers represent the soma and the queen the germ line of the colony. Here, we investigate whether trade-offs exist between maintenance and reproduction on two levels of biological organization, queens and colonies, by following single-queen colonies of the ant Cardiocondyla obscurior throughout the entire lifespan of the queen. Our results show that maintenance and reproduction are positively correlated on the colony level, and we confirm results of an earlier study that found no trade-off on the individual (queen) level. We attribute this unexpected outcome to the existence of a positive feedback loop where investment into maintenance (workers) increases the rate of resource acquisition under laboratory conditions. Even though food was provided ad libitum, variation in productivity among the colonies suggests that resources can only be utilized and invested into additional maintenance and reproduction by the colony if enough workers are available. The resulting relationship between per-capita and colony productivity in our study fits well with other studies conducted in the field, where decreasing per-capita productivity and the leveling off of colony productivity have been linked to density dependent effects due to competition among colonies. This suggests that the absence of trade-offs in our laboratory study might also be prevalent under natural conditions, leading to a positive association of maintenance, (= growth) and reproduction. In this respect, insect colonies resemble indeterminate growing organisms.

Aging and potential for self-renewal: hydra living in the age of aging - a mini-review.

Hydra present an interesting deviation from typical life histories: they have an extensive capacity to regenerate and self-renew and seem to defy the aging process. Hydra have the ability to decouple the aging process from their life history and therefore provide us with a unique opportunity to gain insight into the aging process not only for basal hydrozoans but also for other species across the tree of life. We argue that under steady feeding and asexual reproduction Hydra species are able to escape aging as a result of high levels of cell proliferation and regenerative ability. We further highlight cellular processes for stem cell maintenance, such as the telomere dynamic, which prevent the accumulation of damage and protect against diseases and pathogens that mediate this condition. In addition, we discuss the causes of aging in other Hydra species.

Life span evolution in eusocial workers--a theoretical approach to understanding the effects of extrinsic mortality in a hierarchical system.

While the extraordinary life span of queens and division of labor in eusocial societies have been well studied, it is less clear which selective forces act on the short life span of workers. The disparity of life span between the queen and the workers is linked to a basic issue in sociobiology: How are the resources in a colony allocated between colony maintenance and reproduction? Resources for somatic maintenance of the colony can either be invested into quality or quantity of workers. Here, we present a theoretical optimization model that uses a hierarchical trade-off within insect colonies and extrinsic mortality to explain how different aging phenotypes could have evolved to keep resources secure in the colony. The model points to the significance of two factors. First, any investment that would generate a longer intrinsic life span for workers is lost if the individual dies from external causes while foraging. As a consequence, risky environments favor the evolution of workers with a shorter life span. Second, shorter-lived workers require less investment than long-lived ones, allowing the colony to allocate these resources to sexual reproduction or colony growth.

Environmental challenges improve resource utilization for asexual reproduction and maintenance in hydra.

Variation in life history can reflect genetic differences, and may be caused by environmental effects on phenotypes. Understanding how these two sources of life history variation interact to express an optimal allocation of resources in a changing environment is central to life history theory. This study addresses variation in the allocation of resources to asexual reproduction and to maintenance of Hydra magnipapillata in relation to differences in temperature and food availability. Hydra is a non-senescent, persistent species with primarily clonal reproduction. We recorded changes in budding rate and mean survival under starvation, which indicate changes in the allocation of resources to asexual reproduction and maintenance. In constant conditions we observed a clear trade-off between asexual reproduction and maintenance, where budding increased linearly with food intake while starvation survival stayed rather constant. In contrast, an environment with fluctuations in temperature or food availability promotes maintenance and increases the survival chances of hydra under starvation. Surprisingly, asexual reproduction also tends to be positively affected by fluctuating environmental conditions, which suggests that in this case there is no clear trade-off between asexual reproduction and maintenance in hydra. Environmental stresses have a beneficial impact on the fitness-related phenotypical traits of the basal metazoan hydra. The results indicate that, if the stress occurs in hormetic doses, variable stressful and fluctuating environments can be salutary for hydra. A closer examination of this dynamic can therefore enable us to develop a deeper understanding of the evolution of aging and longevity.