The importance of direct fitness for helpers in advanced social societies

Social insect societies are characterized by a caste determined reproductive and non-reproductive division of labor. Usually, queens stay in the safe surrounding of the nest and produce offspring, while workers refrain from reproduction and care for the brood, forage or defend the nest. However, workers of many social insect species are principally capable of laying unfertilized eggs, which can develop into males. In cooperatively breeding birds or mammals, helpers forgo early reproduction to benefit from brood care experience or nest inheritance and thus, gain an increased direct fitness later in life. However, workers in highly social insect species as in many ants, bees and wasps, generally cannot inherit the nest and replace a fully fertile queen due to physiological restrictions, and the importance of direct fitness benefits for workers has long been neglected. Referring to Hamilton (1964b), it is assumed that ant workers refrain from direct fitness (their own produced offspring) to benefit from indirect fitness the offspring produced by the queen due to their help) and thereby, increase their inclusive fitness. Questions arose whether this is sufficient to explain a lifetime resignation from reproduction in social insect workers. Indeed, several studies report selfish behaviors like worker policing, egg dumping or the refusal of costly tasks, possibly to increase the chance for future direct fitness in individual workers. Here, we studied the importance of direct fitness for workers in the monogynous, monandrous ant Temnothorax crassispinus. We examined the reproductive success of workers by ovary dissections and genotyping workers and males from natural queenless and queenright colonies (chapter 2), and monitored the survival and productivity of queenless and queenright colonies for four years in captivity (chapter 3). We compared fitness traits of queen- and worker-produced males under near-natural and standardized conditions (chapter 4) and investigated whether males produced by workers in the absence of a queen, are accepted in queenright colonies during colony reunification before hibernation (chapter 5). Moreover, we hypothesized that the reproductive potential of young workers might induce selfishness and limit behavioral flexibility under pathogen threat (chapter 6) and examined the effect of selfish reproduction on sanitary behavior of the workers (chapter 7). Our studies show, that queen presence or absence, respectively did not affect ovary development in workers and that around 30% of the genotyped males were not produced by the estimated queen in natural colonies. Most males that were not produced by the queen, were produced by workers not related to the colony. Accordingly, the reproductive success of workers related to the queen seemed to be comparably low in nature but increased under laboratory conditions. Workers seem to be capable of increasing their direct fitness by the expulsion or killing of the queen and a reinforced reproduction afterwards. Queenless colonies were highly productive and persistent and sperm traits of worker-produced males varied only little from that of queen-produced males. Furthermore, larvae produced in queenless colony fragments could be readily integrated in queenright laboratory colonies during colony reunification before hibernation, and contributed considerably to male production in queenright colonies. However, the prospect of future reproductive success did not affect altruistic self-removal in health compromised workers, but microbiota growth seemed to be encouraged in queenless colonies when sanitary behavior is neglected

Queen execution in a monogynous ant

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

Ant queens increase their reproductive efforts after pathogen infection

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

Worker ants promote outbreeding by transporting young queens to alien nests

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

Group demography affects ant colony performance and individual speed of queen and worker aging

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

The plasticity of lifespan in social insects

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?

Queens stay, workers leave: caste-specific responses to fatal infections in an ant

Abstract 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

The Ant Cardiocondyla elegans as Host of the Enigmatic Endoparasitic Fungus Myrmicinosporidium durum

Data on host species and the distribution of the endoparasitic fungus Myrmicinosporidium durum increased continuously in recent decades. Here, we add the ant Cardiocondyla elegans as new host species. Colonies of the monogynous species were found infested in the region of Languedoc-Roussillon (South France). Samples from the nest indicate high infection rates. All castes and sexes were infected by the spores. Variations of infection rates between sampling methods and species are discussed

Sanitary behavior in queenright and queenless ant colonies

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