Egg Cannibalism in a Facultative Polygynous Ant: Conflict for Reproduction or Strategy to Survive?

Policing, i.e. all behaviours that prevent a nestmate from reproducing, is currently observed in social insects. It is presumed to have evolved to regulate potential conflicts generated by genetic asymmetries or to enhance colony efficiency by avoiding surplus reproductives and brood. In the ant, Ectatomma tuberculatum, individual queen fecundity was similar in monogynous and polygynous colonies issued from a Mexican population. Egg cannibalism, however, occurred in the polygynous colonies. The stealing and destruction of reproductive queen‐laid eggs involved only nestmate queens, even if they were highly related. No queen appeared to monopolize reproduction in the polygynous colonies. But, the observed value of relatedness among workers differed from the expected value, suggesting an unequal sharing of reproduction between queens. We discussed whether the cannibalism of queen‐laid eggs in E. tuberculatum results from a competition for reproduction among queens or if this phenomenon is related to constraints on nutritional resources.     

The influence of social structure on brood survival and development in a socially polymorphic ant: insights from a cross‐fostering experiment

Animal societies vary in the number of breeders per group, which affects many socially and ecologically relevant traits. In several social insect species, including our study species Formica selysi, the presence of either one or multiple reproducing females per colony is generally associated with differences in a suite of traits such as the body size of individuals. However, the proximate mechanisms and ontogenetic processes generating such differences between social structures are poorly known. Here, we cross‐fostered eggs originating from single‐queen (= monogynous) or multiple‐queen (= polygynous) colonies into experimental groups of workers from each social structure to investigate whether differences in offspring survival, development time and body size are shaped by the genotype and/or prefoster maternal effects present in the eggs, or by the social origin of the rearing workers. Eggs produced by polygynous queens were more likely to survive to adulthood than eggs from monogynous queens, regardless of the social origin of the rearing workers. However, brood from monogynous queens grew faster than brood from polygynous queens. The social origin of the rearing workers influenced the probability of brood survival, with workers from monogynous colonies rearing more brood to adulthood than workers from polygynous colonies. The social origin of eggs or rearing workers had no significant effect on the head size of the resulting workers in our standardized laboratory conditions. Overall, the social backgrounds of the parents and of the rearing workers appear to shape distinct survival and developmental traits of ant brood.     

Facultative polygyny in Ectatomma tuberculatum (Formicidae, Ectatomminae)

Summary. Polygyny, the presence of several mated queens within the same colony, is widespread in insect societies. This phenomenon is commonly associated with ecological constraints such as limited nest sites. In habitats where solitary nest foundation is risky, monogynous colonies can reintegrate young daughter queens (secondary polygyny). We studied the reproductive structure (i.e. queen number) of the ectatommine ant Ectatomma tuberculatum from Bahia State, Brazil. This species was found to present facultative polygyny: out of a total of 130 colonies collected, 39.2% were monogynous, while 43.8% were polygynous. Polygynous colonies had significantly more workers than monogynous ones. Queen number in polygynous colonies ranged from 2 to 26, with an average of 4 ± 4 queens per colony. All nestmate queens were egg-layers with no apparent dominance hierarchy or agonistic behavior. Non-nestmate queens were adopted by monogynous colonies suggesting that polygyny is secondary, originating through queen adoption. This species is characterized by an open recognition system, which probably allows a switch from monogynous to polygynous colonies. The behavioral acts of queens showed that resident queens remained frequently immobile on or near the brood, contrarily to alien or adopted queens and gynes. In addition, monogynous queens showed no behavioral or physiological (i.e. by ovarian status) differences in comparison with polygynous ones. Secondary or facultative polygyny, probably associated with queen adoption, may have been favored in particular environmental conditions. Indeed, by increasing colony productivity (i.e. number of workers) and territory size (by budding and polydomy), polygyny could uphold E. tuberculatum as a dominant species in the mosaic of arboreal ants in Neotropical habitats.Received 7 April 2004; revised 11 November 2004; accepted 15 November 2004.     

Reproductive conflicts in polyandrous and polygynous ant Formica sanguinea

The occurrence of multiple reproductives within an ant colony changes the balance between indirect fitness benefits and reproductive competition. We test whether the number of matings by an ant queen (polyandry) correlates negatively with the number of reproductive queens in the colony (polygyny), whether the patrilines and matrilines differ in their contribution to the sexual and worker progeny and whether there is an overall reproductive skew. For these aims, we genotyped both worker and sexual offspring from colonies of the ant Formica sanguinea in three populations. Most colonies were monogynous, but eight (11%) were polygynous with closely related queens. Most queens in the monogynous colonies (86%) had mated with multiple males. The effective paternity was lower than the actual number of mates, and the paternity skew was significant. Furthermore, in some monogynous colonies, the patrilines were differently represented in the worker pupae and sexual pupae produced at the same time. Likewise, the matrilines in polygynous colonies were differently present in worker pupae and male offspring. The effective number of matings by a queen was significantly lower in polygynous colonies (mean m_e = 1.68) than in monogynous colonies (means 2.06–2.61). The results give support to the hypotheses that polyandry and polygyny are alternative breeding strategies and that reproductive competition can lead to different representation of patrilines and matrilines among the sexual and worker broods.     

Nestmate Recognition Differences between Honeybee Colonies of <Emphasis Type="BoldItalic">Apis cerana</Emphasis> and <Emphasis Type="BoldItalic">Apis mellifera</Emphasis>

Nestmate recognition in Apis cerana and Apis mellifera was studied by introducing sealed queen cells heterospecifically between queenless colonies. No A. cerana queens were accepted by queenless A. mellifera; but A. mellifera queens were accepted in queenless A. cerana colonies. A. mellifera queens oviposited in queenless A. cerana colonies, but A. cerana workers removed most eggs. In time, egg removals declined, and some A. mellifera larvae that hatched from these eggs reached adulthood, and eventually about half of the workers were newly emerged A. mellifera. Eventually, the colonies consisted only of A. mellifera after A. cerana workers died by attrition. A. mellifera workers are more sensitive to nestmate recognition and killed the A. cerana virgin queens. In mixed-species colonies, after newly emerged A. mellifera workers matured, they removed eggs laid by the A. cerana queens until there were no workers to replace the old ones.     

Behavioral Plasticity in Ant Queens: Environmental Manipulation Induces Aggression among Normally Peaceful Queens in the Socially Polymorphic Ant Leptothorax acervorum

The behavioral traits that shape the structure of animal societies vary considerably among species but appear to be less flexible within species or at least within populations. Populations of the ant Leptothorax acervorum differ in how queens interact with other queens. Nestmate queens from extended, homogeneous habitats tolerate each other and contribute quite equally to the offspring of the colony (polygyny: low reproductive skew). In contrast, nestmate queens from patchy habitats establish social hierarchies by biting and antennal boxing, and eventually only the top-ranking queen of the colony lays eggs (functional monogyny: high reproductive skew). Here we investigate whether queen-queen behavior is fixed within populations or whether aggression and high skew can be elicited by manipulation of socio-environmental factors in colonies from low skew populations. An increase of queen/worker ratio and to a lesser extent food limitation elicited queen-queen antagonism in polygynous colonies from Nürnberger Reichswald similar to that underlying social and reproductive hierarchies in high-skew populations from Spain, Japan, and Alaska. In manipulated colonies, queens differed more in ovarian status than in control colonies. This indicates that queens are in principle capable of adapting the magnitude of reproductive skew to environmental changes in behavioral rather than evolutionary time.     

Mating frequency and genetic relatedness of workers in the hornet Vespa analis (Hymenoptera: Vespidae)

Mating frequency of Vespa analis queens and the genetic relatedness of their workers was analyzed by DNA microsatellite genotyping. Of 20 colonies studied, 18 had a queen inseminated by a single male and two had queens each inseminated by two males. The estimated effective number of matings was 1.05 ± 0.037 (mean ± SE), with 75–85% of the offspring of the two multiply mated queens sired by a single male. The pedigree relatedness between nestmate workers averaged over the 20 colonies was estimated to be 0.74 ± 0.008, almost identical to the predicted value of 0.75 for colonies headed by a singly mated queen. Multiple matrilines; that is, the presence of workers not related to the current queens, were detected in six colonies, suggesting that queen replacement occurred via usurpation of the founding queens in these six colonies. These results demonstrate that the kin structure of V. analis is similar to that reported in other vespid species.     

Reproductive specialization in multiple-queen colonies of the ant Formica exsecta

In polygynous (multiple queens per nest) colonies of socialinsects, queens can increase their reproductive share by layingmore eggs or by increasing the proportion of eggs that developinto reproductive individuals instead of workers. We used polymorphicmicrosatellite loci to determine the genetically effective contributionof queens to the production of gynes (new queens), males, and2 different cohorts of workers in a polygynous population ofthe ant Formica exsecta. For this purpose, we developed a newmethod that can be used for diploid and haplodiploid organismsto quantify the degree of reproductive specialization amongbreeders in societies where there are too many breeders to ascertainparentage. Using this method, we found a high degree of reproductivespecialization among nest-mate queens in both female- and male-producingcolonies (sex ratio is bimodally distributed in the study population).For example, a high effective proportion of queens (25% and79%, respectively) were specialized in the production of malesin female- and male-producing colonies. Our analyses furtherrevealed that in female-producing colonies, significantly fewerqueens contributed to gyne production than to worker production.Finally, we found significant changes in the identity of queenscontributing to different cohorts of workers. Altogether, thesedata demonstrate that colonies of F. exsecta, and probably thoseof many other highly polygynous social insect species, are composedof reproductive individuals differing in their investment togynes, males, and workers. These findings demonstrate a newaspect of the highly dynamic social organization of complexanimal societies.     

Nesting patterns,ecological correlates of polygyny and social organization in the neotropical arboreal ant <Emphasis Type="Italic">Odontomachus hastatus</Emphasis> (Formicidae,Ponerinae)

Queen number varies in the population of O. hastatus in SE Brazil. Here, we evaluate how nesting ecology and colony structure are associated in this species, and investigate how reproduction is shared among nestmate queens. Queen number per colony is positively correlated with nesting space (root cluster of epiphytic bromeliads), and larger nest sites host larger ant colonies. Plant samplings revealed that suitable nest sites are limited and that nesting space at ant-occupied bromeliads differs in size and height from the general bromeliad community. Dissections revealed that queens in polygynous colonies are inseminated, have developed ovaries, and produce eggs. Behavioral observations showed that reproduction in polygynous colonies is mediated by queen–queen agonistic interactions that include egg cannibalism. Dominant queens usually produced more eggs. Field observations indicate that colonies can be initiated through haplometrosis. Polygyny in O. hastatus may result either from groups of cofounding queens (pleometrosis) or from adoption of newly mated queens by established colonies (secondary polygyny). Clumping of bromeliads increases nest space and probably adds stability through a strong root system, which may promote microhabitat selection by queens and favor pleometrosis. Rainstorms that frequently knock down bromeliads can be a source of colony break-up and may promote polygyny. Bromeliads are limited nest sites and may represent a risk for young queens leaving a suitable nest, thus favoring secondary polygyny. Although proximate mechanisms mediating queen number are poorly understood, this study suggests that heterogeneous microhabitat conditions probably contribute to the coexistence of variable forms of social structure in O. hastatus.     

Polygyny reduces rather than increases nestmate discrimination cue diversity in Formica exsecta ants

Although the majority of social insect colonies are headed by a single queen, some species possess nests that contain numerous reproductive queens (polygyny), a trait that is particularly widespread amongst the ants. Polygyny is often associated with a lack of conspecific inter-nest aggression between workers. This is hypothesised to result from increased nestmate cue diversity within nests, since polygynous nests are more genetically diverse than monogynous nests. Alternatively, it may reflect the common origin of polygynous nests that form polydomous networks. We exploit the recent discovery that the nestmate discrimination system in the ant Formica exsecta is based on cuticular hydrocarbons to investigate cue (Z9-alkenes) diversity in several monogynous and polygynous populations. Contrary to previous predictions, in all polygynous populations, the variation between nests in the Z9-alkene profiles was reduced relative to that found in monogynous populations. However, nest-specific Z9-alkene profiles with little variation amongst nestmate workers were still maintained irrespective of nest type or population. This suggests a very effective gestalt mechanism that homogenises the chemical discrimination cues, despite genetic diversity within colonies. Although the reduction in variation between nests was associated with reduced worker aggression on the population level, it cannot totally explain the weak aggression associated with polygynous populations.     

Queen–worker caste ratio depends on colony size in the pharaoh ant (<Emphasis Type="Italic">Monomorium pharaonis</Emphasis>)

The success of an ant colony depends on the simultaneous presence of reproducing queens and non-reproducing workers in a ratio that will maximize colony growth and reproduction. Despite its presumably crucial role, queen–worker caste ratios (the ratio of adult queens to workers) and the factors affecting this variable remain scarcely studied. Maintaining polygynous pharaoh ant (Monomorium pharaonis) colonies in the laboratory has provided us with the opportunity to experimentally manipulate colony size, one of the key factors that can be expected to affect colony level queen–worker caste ratios and body size of eclosing workers, gynes and males. We found that smaller colonies produced more new queens relative to workers, and that these queens and workers both tended to be larger. However, colony size had no effect on the size of males or on the sex ratio of the individuals reared. Furthermore, for the first time in a social insect, we confirmed the general life history prediction by Smith and Fretwell (Am Nat 108:499–506, 1974) that offspring number varies more than offspring size. Our findings document a high level of plasticity in energy allocation toward female castes and suggest that polygynous species with budding colonies may adaptively adjust caste ratios to ensure rapid growth.     

Mating structure and male production in Vespa analis and Vespa simillima (Hymenoptera: Vespidae)

We estimated queen mating frequency, genetic relatedness between workers and worker reproduction in the hornets Vespa analis and Vespa simillima using microsatellite DNA genotyping. The 20 V. analis colonies studied each contained a queen inseminated by a single male. Of the 15 V. simillima colonies studied, nine had a queen inseminated by a single male, four had a queen inseminated by two males, and two had a queen inseminated by three males. The estimated effective number of matings was 1.33 ± 0.74 (mean ± SD), with 75–85% of the offspring of the six multiply mated queens sired by single males. The values for genetic relatedness between the workers of V. analis and V. simillima were 0.739 ± 0.004 and 0.698 ± 0.013 (mean ± SD), respectively. We conclude that V. analis and V. simillima colonies are genetically monogynous and monandrous. When high relatedness between the workers occurs within colonies, kin selection theory predicts a potential conflict between queens and workers over male production. To determine whether males were derived from queens or workers, males from V. analis and V. simillima colonies were genotyped at four microsatellite loci and the level of ovary activation in workers was determined. None of the 787 V. analis workers and only 15 of 3520 V. simillima workers had developed ovaries. Furthermore, the genotyping identified no worker‐produced males in any colony. The presence of reproductive workers correlated positively with the number of workers within the colony. These results suggest that eusocial colonies with an annual life cycle tend to break down socially when they become large and are close to dying.     

Egg Recognition and Social Parasitism in Formica Ants

Nests of social insects are an attractive resource in terms of nutrition and shelter and therefore targeted by a variety of pathogens and parasites that harness the resources of a host colony in their own reproductive interests. Colonies of the ants Formica fusca and F. lemani serve as hosts for mound‐building Formica species, the queens of which use host colonies during colony founding. Here, we investigate whether workers of the host species can mitigate the costs imposed on them by invading parasite queens by recognizing and selectively removing eggs laid by these queens. We used behavioural assays, allowing host workers to choose between con‐colonial eggs and eggs laid by the parasite species F. truncorum. We show that workers of both host species discriminate between the two types of eggs in favour of con‐colonial eggs. Moreover, workers of F. fusca rejected more con‐colonial eggs than F. lemani. This higher rate of error in F. fusca may reflect a greater selectivity or a greater difficulty in discriminating between the two egg types. Nevertheless, both host species removed parasite eggs at a similar rate, when these were artificially introduced into the colonies, although some eggs remained after 10 d. In addition, upon receiving parasite eggs, host workers started to lay unfertilized male‐destined eggs within 6 d, thus employing an alternative pathway to gain direct fitness when the resident queen is no longer present and the colony is parasitized.     

Population genetics of the socially polymorphic ant <Emphasis Type="Italic">Formica podzolica</Emphasis>

Summary. We used microsatellite markers to analyze the hierarchical genetic structure of the North American mound building ant, Formica podzolica. About one-third of all colonies were headed by a single queen (monogynous) whose effective mating frequency was close to one (nestmate worker relatedness r = 0.70), while the remaining colonies were polygynous, with low average nestmate relatedness (r = 0.16). The low worker relatedness found in most polygynous colonies furthermore suggested that the numbers of queens in polygynous colonies of this ant are usually high. Contrary to what has been described from other ants with a queen number dichotomy, we did not find an effect of social form variation on the partitioning of genetic variation above the level of the colony. We found no significant differentiation between the sympatric social forms of F. podzolica, nor did differentiation among populations appear to be affected by colony social organization. These unexpected patterns of genetic structure may have resulted from differences either in the spatial distribution of the social forms or in their social flexibility.Received 12 January 2004; revised 23 February 2004; accepted 10 March 2004.     

Foreign ant queens are accepted but produce fewer offspring

Understanding social evolution requires us to understand the processes regulating the number of breeders within social groups and how they partition reproduction. Queens in polygynous (multiple queens per colony) ants often seek adoption in established colonies instead of founding a new colony independently. This mode of dispersal leads to potential conflicts, as kin selection theory predicts that resident workers should favour nestmate queens over foreign queens. Here we compared the survival of foreign and resident queens as well as their relative reproductive share. We used the ant Formica exsecta to construct colonies consisting of one queen with workers related to this resident queen and introduced a foreign queen. We found that the survival of foreign queens did not differ from that of resident queens over a period of 136 days. However, the genetic analyses revealed that resident queens produced a 1.5-fold higher number of offspring than introduced queens, and had an equal or higher share in 80% of the colonies. These data indicate that some discrimination can occur against dispersing individuals and that dispersal can thus have costs in terms of direct reproduction for dispersing queens.     

Kin structure and colony male reproduction in the hornet<Emphasis Type="Italic"> Vespa crabro</Emphasis> (Hymenoptera: Vespidae)

We estimated queen mating frequency, genetic relatedness among workers, and worker reproduction in Vespa crabro flavofasciata using microsatellite DNA markers. Of 20 colonies examined, 15 contained queens inseminated by a single male, 3 colonies contained queens inseminated by two males, and 2 colonies contained queens inseminated by three males. The genetic relatedness among workers was estimated to be 0.73±0.003 (mean±SE). For this high relatedness, kin selection theory predicts a potential conflict between queens and workers over male production. To verify whether males are derived from queens or workers, 260 males from 13 colonies were genotyped at four microsatellite loci. We found that all of the males were derived from the queens. This finding was further supported by the fact that only 33 of 2,990 workers dissected had developed ovaries. These workers belonged to 2 of the 20 colonies. There was no relationship between queen mating frequency and worker reproduction, and no workers produced male offspring in any of the colonies. These results suggest that male production dominated by queens in V. crabro flavofasciata is possibly due to worker policing.     

No evidence that reproductive bumblebee workers reduce the production of new queens

Kin selection theory predicts potential conflict between queen and workers over male parentage in hymenopteran societies headed by one, singly mated queen, because each party is more closely related to its own male offspring. In ‘late-switching’ colonies of the bumblebee Bombus terrestris, i.e. colonies whose queens lay haploid eggs relatively late in the colony cycle, workers start to lay male eggs shortly after the queen lays the female eggs that will develop into new queens. It has been hypothesized that this occurs because workers recognize, via a signal given by the queen instructing female larvae to commence development as queens, that egg laying is now in their kin-selected interest. This hypothesis assumes that aggressive behaviour in egg-laying workers does not substantially reduce the production of new queens, which would decrease the workers' fitness payoff from producing males. We tested the hypothesis that reproductive activity inB. terrestris workers does not reduce the production of new queens. We used microsatellite genotyping to sex eggs and hence to select eight size-matched pairs of ‘late-switching’ colonies from a set of commercial colonies. From one colony of each pair we removed every egg-laying or aggressive worker observed. From the other colony, we simultaneously removed a nonegg-laying, nonaggressive worker. Removed workers were replaced with young workers from separate colonies at equal frequencies within the pair. There was no significant difference in queen productivity between colonies with reduced or normal levels of egg-laying or aggressive workers. Therefore, as predicted, reproductive B. terrestris workers did not significantly reduce the production of new queens.     

Nestmate recognition by guards of the Asian hive bee <Emphasis Type="Italic">Apis cerana</Emphasis>

When a honey bee colony becomes queenless and broodless its only reproductive option is for some of its workers to produce sons before the colony perishes. However, for this to be possible the policing of worker-laid eggs must be curtailed and this provides the opportunity for queenless colonies to be reproductively parasitized by workers from other nests. Such reproductive parasitism is known to occur in Apis florea and A. cerana. Microsatellite analyses of worker samples have demonstrated that the proportion of non-natal workers present in an A. cerana colony declines after a colony is made queenless. This observation suggests that queenless A. cerana colonies may be more vigilant in repelling potentially parasitic non-natal workers than queenright colonies. We compared rates of nestmate and non-nestmate acceptance in both queenright and queenless A. cerana colonies using standard assays and showed that there is no statistical difference between the proportion of non-nestmate workers that are rejected in queenless and queenright colonies. We also show that, contrary to earlier reports, A. cerana guards are able to discriminate nestmate workers from non-nestmates, and that they reject significantly more non-nestmate workers than nestmate workers. Received 25 February 2008; revised 21 May 2008; accepted 25 June 2008.     

Prediction of social structure and genetic relatedness in colonies of the facultative polygynous stingless bee Melipona bicolor (Hymenoptera, Apidae)

Stingless bee colonies typically consist of one single-mated mother queen and her worker offspring. The stingless bee Melipona bicolor (Hymenoptera: Apidae) shows facultative polygyny, which makes this species particularly suitable for testing theoretical expectations concerning social behavior. In this study, we investigated the social structure and genetic relatedness among workers from eight natural and six manipulated colonies of M. bicolor over a period of one year. The populations of M. bicolor contained monogynous and polygynous colonies. The estimated genetic relatedness among workers from monogynous and polygynous colonies was 0.75 ± 0.12 and 0.53 ± 0.16 (mean ± SEM), respectively. Although the parental genotypes had significant effects on genetic relatedness in monogynous and polygynous colonies, polygyny markedly decreased the relatedness among nestmate workers. Our findings also demonstrate that polygyny in M. bicolor may arise from the adoption of related or unrelated queens.     

Polygynous supercolonies of the acacia‐ant Pseudomyrmex peperi,an inferior colony founder

In ant–plant protection mutualisms, plants provide nesting space and nutrition to defending ants. Several plant–ants are polygynous. Possessing more than one queen per colony can reduce nestmate relatedness and consequently the inclusive fitness of workers. Here, we investigated the colony structure of the obligate acacia‐ant Pseudomyrmex peperi, which competes for nesting space with several congeneric and sympatric species. Pseudomyrmex peperi had a lower colony founding success than its congeners and thus, appears to be competitively inferior during the early stages of colony development. Aggression assays showed that P. peperi establishes distinct, but highly polygynous supercolonies, which can inhabit large clusters of host trees. Analysing queens, workers, males and virgin queens from two supercolonies with eight polymorphic microsatellite markers revealed a maximum of three alleles per locus within a colony and, thus, high relatedness among nestmates. Colonies had probably been founded by one singly mated queen and supercolonies resulted from intranidal mating among colony‐derived males and daughter queens. This strategy allows colonies to grow by budding and to occupy individual plant clusters for time spans that are longer than an individual queen’s life. Ancestral states reconstruction indicated that polygyny represents the derived state within obligate acacia‐ants. We suggest that the extreme polygyny of Pseudomyrmex peperi, which is achieved by intranidal mating and thereby maintains high nestmate relatedness, might play an important role for species coexistence in a dynamic and competitive habitat.