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Choosing the right mating partner is one of the most critical decisions in the life of a sexually reproducing organism and is the basis of sexual selection. This choice is usually assumed to be made by one or both of the sexual partners. Here, we describe a system in which a third party - the siblings - promote outbreeding by their sisters: workers of the tiny ant Cardiocondyla elegans carry female sexuals from their natal nest over several meters and drop them in the nest of another, unrelated colony to promote outbreeding with wingless, stationary males. Workers appear to choose particular recipient colonies into which they transfer numerous female sexuals. Assisted outbreeding and indirect female choice in the ant C. elegans are comparable to human matchmaking and suggest a hitherto unknown aspect of natural history - third party sexual selection. Our study highlights that research at the intersection between social evolution and reproductive biology might reveal surprising facets of animal behavior.

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One of the central questions of ageing research is why lifespans of organisms differ so tremendously among related taxa and, even more surprising, among members of the same species. Social insects provide a particularly pronounced example for this. Here, we review previously published information on lifespan plasticity in social insects and provide new data on worker lifespan in the ant Cardiocondyla obscurior, which because of its relatively short lifespan is a convenient model to study ageing. We show that individual lifespan may vary within species with several reproductive and social traits, such as egg-laying rate, queen number, task, colony size and colony composition. For example, in Cardiocondyla, highly fecund queens live longer than reproductively less active queens, and workers tend to live longer when transferred into a novel social environment or, as we show with new data, into small colonies. We hypothesize that this plasticity of lifespan serves to maximize the reproductive output of the colony as a whole and thus the inclusive fitness of all individuals. The underlying mechanisms that link the social environment or reproductive status with lifespan are currently unresolved. Several studies in honeybees and ants indicate an involvement of nutrient-sensing pathways, but the details appear to differ among species. This article is part of the theme issue 'Ageing and sociality: why, when and how does sociality change ageing patterns?'

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Workers in many species of social insects are capable of laying unfertilized eggs, which can develop into haploid males. This causes a conflict about male parentage between queens and workers. In a few species, this may result in matricide, that is, workers kill the colony's queen. Queen killing has so far been observed mainly in multi-queen colonies or in annual species, when the queen's fecundity declines at the end of the reproductive period. Here, we report queen expulsion and matricide in a monogynous, monandrous ant with perennial societies. Workers were seen to aggressively expel both related and unrelated queens from their nest shortly after the end of hibernation. Queen expulsion and matricide led to a significant decrease in the number of workers and brood, but eventually increased the direct fitness of workers through significant male production. Long-term observations revealed a short lifespan of queens, while workers in orphaned colonies survived and produced male offspring over several years.

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Hamilton's theory of inclusive fitness suggests that helpers in animal societies gain fitness indirectly by increasing the reproductive performance of a related beneficiary. Helpers in cooperatively breeding birds, mammals and primitively eusocial wasps may additionally obtain direct fitness through inheriting the nest or mating partner of the former reproductive. Here, we show that also workers of a highly eusocial ant may achieve considerable direct fitness by producing males in both queenless and queenright colonies. We investigated the reproductive success of workers of the ant Temnothorax crassispinus in nature and the laboratory by dissecting workers and determining the origin of males by microsatellite analysis. We show that workers are capable of activating their ovaries and successfully producing their sons independently of the presence of a queen. Genotypes revealed that at least one fifth of the males in natural queenright colonies were not offspring of the queen. Most worker-produced males could be assigned to workers that were unrelated to the queen, suggesting egg-laying by drifting workers.

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Workers of many species of social Hymenoptera have functional ovaries and are capable of laying haploid, unfertilized eggs, at least in the absence of a queen. Except for honeybees, it remains largely unknown whether worker-produced males have the same quality as queen-produced males and whether workers benefit in direct fitness by producing their sons. Previous studies in the monogynous ant Temnothorax crassispinus revealed that a high proportion of males in natural and laboratory colonies are worker offspring. Here, we compare longevity, body size, sperm length and sperm viability between queen- and worker-produced males. We either split queenright colonies into queenright and queenless halves or removed the queen from a fraction of the queenright colonies and then examined the newly produced males. Male quality traits varied considerably among colonies but differed only slightly between queen- and worker-produced males. Worker-produced males outnumbered queen-produced males and also had a longer lifespan, but under certain rearing conditions sperm from queen-produced males had a higher viability.

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Workers of several social insects are capable of gaining direct fitness by laying unfertilized eggs, which then develop into males. However, under queenright conditions, direct reproduction of workers is usually prevented by queen-induced regulatory mechanisms. In nature, some ant colonies inhabit multiple nests sites (polydomy). This might allow workers to escape queen control and to reproduce. However, whether worker-produced brood survives after colony reunion in seasonally polydomous species remains unclear. In several species, worker-produced eggs and male-destined larvae are selectively destroyed in queenright colonies. Here, we test whether workers discriminate between queen- and worker-produced larvae during colony reunion. We examined the reproductive success of workers in queenless subcolonies of our study species Temnothorax crassispinus. Our results show that present brood did not inhibit worker reproduction but had a positive effect on worker lifespan. Larvae produced by workers were readily integrated into queenright subcolonies during colony reunion and these larvae successfully developed into adult males.

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Waste disposal is important for maintaining the health of animal societies. Adults and off ;spring produce large amounts of waste and feces that could contain pathogens or toxins and may need to be stored away from the young or adult individuals. In social insects, the worker caste is responsible for nest maintenance, including sanitary behavior, and waste disposal strategies vary between species. However, individual task allocation is generally affected by queen presence and worker efficiency often decreases in the absence of a queen. Here we show that most (74%) colonies of the cavity-dwelling ant Temnothorax crassispinus construct up to two localized indoor 'latrines', which are used for defecation and only very rarely also as waste dumps. Restriction of defecation to designated areas affects the growth of mold inside the nest. Defecation strategies of colonies are furthermore affected by queen presence, with workers from queenless nests more frequently defecating outside the nest and forming latrines. As colonies do not actively avoid moldy nests, mold seems to not necessarily be a threat to the colony. While solid waste management has been more extensively studied in social insects, this study contributes a rare insight into the organization of non-easily transportable fecal waste.

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BACKGROUND: The intense interactions among closely related individuals in animal societies provide perfect conditions for the spread of pathogens. Social insects have therefore evolved counter-measures on the cellular, individual, and social level to reduce the infection risk. One striking example is altruistic self-removal, i.e., lethally infected workers leave the nest and die in isolation to prevent the spread of a contagious disease to their nestmates. Because reproductive queens and egg-laying workers behave less altruistically than non-laying workers, e.g., when it comes to colony defense, we wondered whether moribund egg-layers would show the same self-removal as non-reproductive workers. Furthermore, we investigated how a lethal infection affects reproduction and studied if queens and egg-laying workers intensify their reproductive efforts when their residual reproductive value decreases ("terminal investment"). RESULTS: We treated queens, egg-laying workers from queenless colonies, and non-laying workers from queenright colonies of the monogynous (single-queened) ant Temnothorax crassispinus either with a control solution or a solution containing spores of the entomopathogenic fungus Metarhizium brunneum. Lethally infected workers left the nest and died away from it, regardless of their reproductive status. In contrast, infected queens never left the nest and were removed by workers only after they had died. The reproductive investment of queens strongly decreased after the treatment with both, the control solution and the Metarhizium brunneum suspension. The egg laying rate in queenless colonies was initially reduced in infected colonies but not in control colonies. Egg number increased again with decreasing number of infected workers. CONCLUSIONS: Queens and workers of the ant Temnothorax crassispinus differ in their reaction to an infection risk and a reduced life expectancy. Workers isolate themselves to prevent contagion inside the colony, whereas queens stay in the nest. We did not find terminal investment; instead it appeared that egg-layers completely shut down egg production in response to the lethal infection. Workers in queenless colonies resumed reproduction only after all infected individuals had died, probably again to minimize the risk of infecting the offspring.

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BACKGROUND: The performance and fitness of social societies mainly depends on the efficiency of interactions between reproductive individuals and helpers. Helpers need to react to the group's requirements and to adjust their tasks accordingly, while the reproductive individual has to adjust its reproductive rate. Social insects provide a good system to study the interrelations between individual and group characteristics. In general, sterile workers focus on brood care and foraging while the queen lays eggs. Reproductive division of labor is determined by caste and not interchangeable as, e.g., in social mammals or birds. Hence, changing social and environmental conditions require a flexible response by each caste. In the ant Cardiocondyla obscurior, worker task allocation is based on age polyethism, with young workers focusing on brood care and old workers on foraging. Here, we examine how group age demography affects colony performance and fitness in colonies consisting of only old or young workers and a single old or young queen. We hypothesized that both groups will be fully functional, but that the forced task shift affects the individuals' performance. Moreover, we expected reduced worker longevity in groups with only young workers due to precocious foraging but no effect on queen longevity depending on group composition. RESULTS: Neither the performance of queens nor that of workers declined strongly with time per se, but offspring number and weight were influenced by queen age and the interaction between queen and worker age. Individual residual life expectancy strongly depended on colony demography instead of physiological age. While worker age affected queen longevity only slightly, exposing old workers to the conditions of colony founding increased their life spans by up to 50% relative to workers that had emerged shortly before colony set-up. CONCLUSIONS: The social environment strongly affected the tempo of aging and senescence in C. obscurior, highlighting the plasticity of life expectancy in social insects. Furthermore, colonies obtained the highest reproductive output when consisting of same-aged queens and workers independent of their physiological age. However, workers appeared to be able to adjust their behavior to the colony's needs and not to suffer from age-dependent restrictions.

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Infections with potentially lethal pathogens may negatively affect an individual's lifespan and decrease its reproductive value. The terminal investment hypothesis predicts that individuals faced with a reduced survival should invest more into reproduction instead of maintenance and growth. Several studies suggest that individuals are indeed able to estimate their body condition and to increase their reproductive effort with approaching death, while other studies gave ambiguous results. We investigate whether queens of a perennial social insect (ant) are able to boost their reproduction following infection with an obligate killing pathogen. Social insect queens are special with regard to reproduction and aging, as they outlive conspecific non-reproductive workers. Moreover, in the ant Cardiocondyla obscurior, fecundity increases with queen age. However, it remained unclear whether this reflects negative reproductive senescence or terminal investment in response to approaching death. Here, we test whether queens of C. obscurior react to infection with the entomopathogenic fungus Metarhizium brunneum by an increased egg-laying rate. We show that a fungal infection triggers a reinforced investment in reproduction in queens. This adjustment of the reproductive rate by ant queens is consistent with predictions of the terminal investment hypothesis and is reported for the first time in a social insect.

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One of the central tenets of life-history theory is that organisms cannot simultaneously maximize all fitness components. This results in the fundamental trade-off between reproduction and life span known from numerous animals, including humans. Social insects are a well-known exception to this rule: reproductive queens outlive nonreproductive workers. Here, we take a step forward and show that under identical social and environmental conditions the fecundity-longevity trade-off is absent also within the queen caste. A change in reproduction did not alter life expectancy, and even a strong enforced increase in reproductive efforts did not reduce residual life span. Generally, egg-laying rate and life span were positively correlated. Queens of perennial social insects thus seem to maximize at the same time two fitness parameters that are normally negatively correlated. Even though they are not immortal, they best approach a hypothetical "Darwinian demon" in the animal kingdom.

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