Mating success and potential male-worker conflict in a male-dimorphic ant

BACKGROUND: Males of many species adjust their reproductive tactics with regard to their condition and status. For example, large males may develop weapons and fight for access to females, whereas small or undernourished males do not express costly weapons or ornaments and sneak copulations. Different condition-dependent reproductive tactics may be associated with unequal average fitness, but the tactic chosen by a given male under given circumstances is thought to result in the highest possible fitness return.The ant species Cardiocondyla obscurior exhibits an environment-controlled polymorphism of docile, winged males and aggressive "ergatoid" males. Ergatoid males, which can replenish their sperm supply throughout their lives, engage in lethal fighting, and attempt to monopolize all female sexuals available in their nests, were previously assumed to gain higher lifetime reproductive success than the peaceful, winged males, which disperse to mate away from the nest and whose spermatogenesis is limited to the first days of adult life. However, precise data on male mating success have as yet not been available.Here, we compare the average mating success of the two male morphs, taking the high mortality rate of immature ergatoid males into account. Because individuals in insect societies may have opposing interests about their own development, we also investigate whether the interests of male larvae coincide with those of the workers and the rest of the society. RESULTS: When the survival probability of males is taken into account, winged males are more likely to mate multiply and in consequence have a higher estimated average mating success than ergatoid males. Therefore, male larvae are expected to prefer developing into winged instead of ergatoid adults. CONCLUSION: Though male larvae can expect a higher average mating success when developing into winged males, most colonies produce only ergatoid males under standard conditions. This might point at a novel type of potential kin conflict within the social insect colony. Because workers in insect societies usually control male larval development, ergatoid male production under normal conditions probably reflects the optimal allocation strategy of workers to maximise their inclusive fitness

The dynamics of male-male competition in Cardiocondyla obscurior ants

BACKGROUND: The outcome of male-male competition can be predicted from the relative fighting qualities of the opponents, which often depend on their age. In insects, freshly emerged and still sexually inactive males are morphologically indistinct from older, sexually active males. These young inactive males may thus be easy targets for older males if they cannot conceal themselves from their attacks. The ant Cardiocondyla obscurior is characterised by lethal fighting between wingless (“ergatoid”) males. Here, we analyse for how long young males are defenceless after eclosion, and how early adult males can detect the presence of rival males. RESULTS: We found that old ergatoid males consistently won fights against ergatoid males younger than two days. Old males did not differentiate between different types of unpigmented pupae several days before emergence, but had more frequent contact to ready-to-eclose pupae of female sexuals and winged males than of workers and ergatoid males. In rare cases, old ergatoid males displayed alleviated biting of pigmented ergatoid male pupae shortly before adult eclosion, as well as copulation attempts to dark pupae of female sexuals and winged males. Ergatoid male behaviour may be promoted by a closer similarity of the chemical profile of ready-to-eclose pupae to the profile of adults than that of young pupae several days prior to emergence. CONCLUSION: Young ergatoid males of C. obscurior would benefit greatly by hiding their identity from older, resident males, as they are highly vulnerable during the first two days of their adult lives. In contrast to the winged males of the same species, which are able to prevent ergatoid male attacks by chemical female mimicry, young ergatoids do not seem to be able to produce a protective chemical profile. Conflicts in male-male competition between ergatoid males of different age thus seem to be resolved in favour of the older males. This might represent selection at the colony level rather than the individual level

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

Polygyny, Inbreeding, and Wingless Males in the Malagasy Ant Cardiocondyla shuckardi Forel (Hymenoptera, Formicidae)

The ant genus Cardiocondyla exhibits a fascinating diversity of its reproductive biology, with winged and wingless males, long-winged and short-winged queens, strict monogyny and facultative polygyny with or without queen fighting. Here we report on the previously unstudied Malagasy ant C. shuckardi. We describe the nesting habits, male morphology and colony structure of this species. Furthermore, based on the genotypes from three microsatellite loci we document a very high incidence of sib-mating

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

Mating with Stressed Males Increases the Fitness of Ant Queens

BACKGROUND: According to sexual conflict theory, males can increase their own fitness by transferring substances during copulation that increase the short-term fecundity of their mating partners at the cost of the future life expectancy and re-mating capability of the latter. In contrast, sexual cooperation is expected in social insects. Mating indeed positively affects life span and fecundity of young queens of the male-polymorphic ant Cardiocondyla obscurior, even though males neither provide nuptial gifts nor any other care but leave their mates immediately after copulation and die shortly thereafter. PRINCIPAL FINDINGS: Here, we show that mating with winged disperser males has a significantly stronger impact on life span and reproductive success of young queens of C. obscurior than mating with wingless fighter males. CONCLUSIONS: Winged males are reared mostly under stressful environmental conditions, which force young queens to disperse and found their own societies independently. In contrast, queens that mate with wingless males under favourable conditions usually start reproducing in the safety of the established maternal nest. Our study suggests that males of C. obscurior have evolved mechanisms to posthumously assist young queens during colony founding under adverse ecological conditions

Terminal Investment: Individual Reproduction of Ant Queens Increases with Age

The pattern of age-specific fecundity is a key component of the life history of organisms and shapes their ecology and evolution. In numerous animals, including humans, reproductive performance decreases with age. Here, we demonstrate that some social insect queens exhibit the opposite pattern. Egg laying rates of Cardiocondyla obscurior ant queens increased with age until death, even when the number of workers caring for them was kept constant. Cardiocondyla, and probably also other ants, therefore resemble the few select organisms with similar age-specific reproductive investment, such as corals, sturgeons, or box turtles (e.g., [1]), but they differ in being more short-lived and lacking individual, though not social, indeterminate growth. Furthermore, in contrast to most other organisms, in which average life span declines with increasing reproductive effort, queens with high egg laying rates survived as long as less fecund queens

Competition and Opportunity Shape the Reproductive Tactics of Males in the Ant Cardiocondyla obscurior

Context-dependent adjustment of mating tactics can drastically increase the mating success of behaviourally flexible animals. We used the ant Cardiocondyla obscurior as a model system to study adaptive adjustment of male mating tactics. This species shows a male diphenism of wingless fighter males and peaceful winged males. Whereas the wingless males stay and exclusively mate in the maternal colony, the mating behaviour of winged males is plastic. They copulate with female sexuals in their natal nests early in life but later disperse in search for sexuals outside. In this study, we observed the nest-leaving behaviour of winged males under different conditions and found that they adaptively adjust the timing of their dispersal to the availability of mating partners, as well as the presence, and even the type of competitors in their natal nests. In colonies with virgin female queens winged males stayed longest when they were the only male in the nest. They left earlier when mating partners were not available or when other males were present. In the presence of wingless, locally mating fighter males, winged males dispersed earlier than in the presence of docile, winged competitors. This suggests that C. obscurior males are capable of estimating their local breeding chances and adaptively adjust their dispersal behaviour in both an opportunistic and a risk-sensitive way, thus showing hitherto unknown behavioural plasticity in social insect males

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