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

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

Alternative reproductive tactics and their consequences in the ant genus Cardiocondyla

The ant genus Cardiocondyla is characterised by the occurrence of �workerlike�, ergatoid males that mate inside the nest. In many species of this genus, �normal�, winged males occur in addition, and a dimorphism of wingless and winged males is exhibited. The two male morphs represent alternative reproductive tactics with aggressive territorial males and peaceful disperser males. The latter mate inside the colony and then leave after several days to establish further matings with alien queens. The male morph is determined environmentally and thus the result of a conditional strategy. Generally, in the male dimorphic species C. obscurior only ergatoid males are produced. The bigger and more �expensive� winged male develops only in case where environmental conditions become worse. Investigations have shown that the larvae themselves are insensitive to changes in environmental conditions, but that workers determine the winged male morph by treating the larvae differently. The colony is able to react to environmental changes quickly, as the sensitive phase of morph determination is late (at the end of the second larval instar). After approximately two and a half weeks, adult winged males can already eclose and disperse to reach new habitats. At an individual level, males would appear to be better winged, as they are not recognized by ergatoid males as competitors (due to female mimicry) and thus avoid being killed, and still have the opportunity to mate inside the nest before dispersing. However, larvae appear to have no possibility to influence their fate as it is usual in an eusocial community. Local mating within the colony is accompanied with high levels of inbreeding. Inbreeding in haplo-diploids is less detrimental than in diploid organisms, as deleterious and lethal alleles are purged in haploid males. Exceptions are Hymenoptera with a complementary sex determination system, because in these, inbreeding leads to diploid male production. The study demonstrates that the inbreeding level in Cardiocondyla is very high. Inbreeding in addition to local mate competition, leads to even more female-biased sex ratios. As expected, another sex determination system than single-locus complementary sex determination or multi-locus complementary sex determination (with few loci), based probably not on heterozygosity, evolved in Cardiocondyla. Nevertheless, inbreeding depression can be seen after several generations of sib mating in the laboratory. Genetic data suggest that events of outbreeding alternate with inbreeding in the colonies, and this may prevent inbreeding depression in nature. As queens appear to be able to recognize kin from non-kin, they may prefer to mate with unrelated males when a selection is available. Furthermore, multiple mating may promote outbreeding, and the costs of intranidal mating in terms of risk of pathogens and predators can be neglected. Moreover, mating has no negative effect, as it can be seen in many species with sexual conflict, but instead prolongs the lifespan of the queens. A dimorphism in the female sex of long winged and short winged queens is not representative of the typical alternative reproductive tactics of dispersing and territorial queens, but appears to correlate with the switch from polygynous, dependent founding ancestors to monogyny. All queens found their colonies independently after shedding their wings, but short winged queens invest into fat instead of flight muscle mass and consequently are more successful in establishing new colonies

Social influence on age and reproduction reduced lifespan and fecundity in multi queen ant colonies

Evolutionary theories of ageing predict that life span increases with decreasing extrinsic mortality, and life span variation among queens in ant species seems to corroborate this prediction: queens, which are the only reproductive in a colony, live much longer than queens in multi-queen colonies. The latter often inhabit ephemeral nest sites and accordingly are assumed to experience a higher mortality risk. Yet, all prior studies compared queens from different single- and multi-queen species. Here, we demonstrate an effect of queen number on longevity and fecundity within a single, socially plastic species, where queens experience the similar level of extrinsic mortality. Queens from single- and two-queen colonies had significantly longer lifespan and higher fecundity than queens living in associations of eight queens. As queens also differ neither in morphology nor the mode of colony foundation, our study shows that the social environment itself strongly affects ageing rate