Cooperation among unrelated individuals: the ant foundress case

Ant foundress associations are an example of cooperation among non-kin. Across a dozen genera, queens able to found a colony alone often join unrelated queens, thereby enhancing worker production and colony survivorship. The benefits of joining other queens vary with group size and ecological conditions. However, after the first workers mature, the queens fight until only one survives. The presence of cofoundresses, and their relative fighting ability, also affects the extent of cooperative investment before worker emergence. This reveals previously overlooked early conflicts among queens, which reduce the mutualistic benefits of cooperation.     

Influence of queen weight and colony origin on worker response in Solenopsis geminata

Abstract. The influence of weight and colony origin of the queen of Solenopsis geminata (F.) (Hymenoptera: Formicidae) on worker attraction is studied under laboratory conditions. In the first experiment, worker response to individual queens of different weight from the same colony is evaluated. Heavier queens are more attractive than smaller queens to their own workers. In subsequent experiments, the colony origin effect is investigated and worker response to a pair of queens of the same weight from the same or different colonies is compared. When queens are from the same colony, workers do not show a significant preference between queens. However, when queens are from a different colony, workers are significantly more attracted to their own queen than to the foreign queen. Finally, the response of workers to queens of different weight from the same or different colonies is investigated. In both cases, workers are significantly more attracted to a heavier queen than a lighter queen, even if the lighter queen is their own queen. A putative pheromonal component (E)‐6‐(1‐pentenyl)‐2H‐2‐pyranone, is not positively correlated with queen weight.     

Group defense by colony-founding queens in the fire ant Solenopsis invicta

Mutualistic associations among nonkin can form when animalsin groups have a greater chance of overcoming challenges presentedby the environment than do solitary animals. Colony foundingby small groups of unrelated queens, a habit documented in severalspecies of ants, is often interpreted as a mutualistic interactionselected by intense competition among incipient colonies. However,many new colonies in these species are founded in areas wheretheir chief enemies are mature ant colonies, rather than othernewly founded colonies. In this study, we tested whether groupnest-founding in the fire ant Solenopsis invicta improved theability of queens to survive attacks by mature colonies. Inthe laboratory, queens in groups of three were more likely thansolitary queens to survive attacks by workers of the nativefire ant Solenopsis geminata. When newly mated queens were establishedexperimentally in the field, workers from mature S. invictacolonies caused the majority of queen deaths. Queens in groupsof two, but not in groups of four, had higher survival ratesthan did solitary queens during the period between colony establishmentand the appearance of the first workers. The advantage of cooperativedefense approximately counterbalanced the disadvantages causedby competition within foundress associations of two to threequeens. Previous studies have shown that colonies founded bymultiple queens produce larger worker populations than coloniesfounded by solitary queens; however, experimentally increasingworker number in incipient colonies had no effect on colonysurvival in the field.     

Variation in queen size across a behavioral transition zone in the ant Messor pergandei

Summary. Ant colonies should be selected to optimally allocate resources to individual reproductive offspring so as to balance production costs with offspring fitness gains. Different modes of colony founding have different size-dependent fitness functions, and should thus lead to different optimal queen sizes. We tested whether a behavioral transition from solitary colony founding (haplometrosis) to group colony founding (pleometrosis) across the range of the ant Messor pergandei was associated with a difference in queen size or condition. Both winged gynes and founding queens were significantly smaller and lighter at pleometrotic than at haplometrotic sites, with an abrupt shift in these characters across the 8.5 km-wide behavioral transition zone. Both the mutualistic advantages of grouping and among-queen competition within associations are likely to be important in selecting for smaller queen size in pleometrotic populations.Received 16 January 2004; revised 13 August 2004; accepted 16 August 2004.     

Queen selection by worker groups of the ant Myrmica rubra L.

Normal queens in a colony of Myrmica rubra L. were not necessarily more attractive to the workers than strange ones grafted into the colony. Workers chose the best queens using those they already had as a standard. After winter dormancy, workers in colonies with queens were less tolerant for queen variety. One week at 20°C was enough to cause them to reject still-dormant queens, even those of their own colony, though they accepted alien queens. However, after 2–3 weeks culture queens were acceptable only if they belonged to the same colony as the natural ones or to the same colony as those queens that had been artificially implanted. To re-open the group, it was essential to remove all the resident queens; then after 2 days the workers took any queen offered, rather than remain queenless, but when offered a choice between one of their originals and an unfamiliar one, they still took the former. Three queenless weeks were required before they lost their preference for an ex-nestmate. Queens from a single colony, isolated in separate groups of workers, remained acceptable to the workers with them indefinitely, but when these queens were transferred to identical collateral groups of workers, they were rejected even after only 2 weeks' separation. Some groups of workers were less tolerant than others and some queens were more attractive than others, but their compatibility diminished with time if they lived in isolation. A group with an attractive queen was more likely to resist other queens.     

Conditions favoring queen execution in young social insect colonies

Summary. Previous attempts to explain worker aggression against extra queens in young social insect colonies have used kin selection arguments. These have been inconsistent with experimental evidence demonstrating aggression against extra queens without strong evidence of kin discrimination. Using a game theoretical model, I suggest a series of decision rules that are consistent with the current experimental evidence from study of young colonies of the fire ant Solenopsis invicta. These decision rules are: 1) When workers cannot directly determine which queen is their mother, they should behave in favor of a queen that maximizes the product of the chance that a queen is the workers mother multiplied by the chance that it will survive to colony maturity. In some cases, the survival potential of the different queens may be the only character that influences the workers decision. 2) Workers should delay aggression against extra queens until the workers can gain their greatest advantage through such aggression. 3) Queens may adopt strategies that allow them to dominate rivals, either by gaining an advantage in fights among the queens or by increasing their attractiveness to workers.Received 2 June 2004; revised 5 July 2004; accepted 14 July 2004.     

Clonal reproduction by males of the ant Vollenhovia emeryi (Wheeler)

In colonies of the queen‐polymorphic ant Vollenhovia emeryi, some colonies produce only long‐winged (L) queens, while others produce only short‐winged (S) queens. At four nuclear microsatellite loci, males in the S colony had alleles that were different from those of their queen. This suggests that the nuclear genome of males is not inherited from their colony queen, as has also been described for Wasmannia auropunctata (Roger). In V. emeryi the possibility of male transfer from other colonies has not been ruled out because previous studies of this species have obtained only nuclear gene information. We analyzed both mitochondrial and nuclear genes for S queens, S males and L queens to clarify the origins of males. Sequence analyses showed that although S queens and S males shared the same mtDNA haplotype, they had a different genotype at a nuclear gene (long‐wavelength opsin) locus. Neighbor‐joining analysis based on the four microsatellite loci also suggested gene pool separation between S queens and S males. These results are consistent with predictions of clonal reproduction by males. While L queens share opsin genotypes with S males, they have very different mtDNA sequences. Hybridization in the near past between S queens and L males or gene transmission from S males to L queen populations in the present would explain these differences.     

Competition and kin discrimination in colony founding by social Hymenoptera

Summary After mating, queens of social wasp and ant species sometimes band together to start a new colony cooperatively. I assume these queens sequentially encounter potential nest sites that may or may not already contain a queen. Whether to remain at a given site or to leave in hopes of finding a better site is modelled using dynamic programming. The results suggest that discriminating competitive ability is more valuable than discriminating kinship. Wasps, which have a high survival rate in transitions between nest site encounters and in which pleometrosis seems to have a consistently high benefit, are predicted to discriminate both competitive ability and kinship of potential partners. Ants, which have lower survivorship and variable benefits, are predicted to show conditional joining behavior (sometimes based on discriminating competitive ability, but almost never based on discriminating kinship). A survey of the literature supports the model with respect to the predictions on kin discrimination in both groups and on conditional joining behavior in ants. However, whether partners are joined based on perceptions of competitive ability needs more tests.     

Sex ratio conflicts, mating frequency, and queen fitness in the ant Formica truncorum

We examined the effect of facultative sex allocation by workerson queen fitness in a Furnish population of the ant Formicatruncorum. Workers rear female-biased broods in colonies headedby a singly mated queen and male-biased broods in colonies headedby a multiply mated queen. As a result, multiply mated queenshave a 37% fitness advantage over singly mated queens. Neitherreproductive output nor worker population of colonies variedwith queen mating frequency. We suggest that singly mated queenspersist in the population because fitness benefits to multiplymated queens via sex allocation are balanced by costs of additionalmatings. Alternatively, singly mated queens may persist simplybecause some queens lack opportunities to mate multiply or becausemale control sometimes prevents additional matings by queens.     

The significance of multiple mating in the social wasp Vespula maculifrons

The evolution of the complex societies displayed by social insects depended partly on high relatedness among interacting group members. Therefore, behaviors that depress group relatedness, such as multiple mating by reproductive females (polyandry), are unexpected in social insects. Nevertheless, the queens of several social insect species mate multiply, suggesting that polyandry provides some benefits that counteract the costs. However, few studies have obtained evidence for links between rates of polyandry and fitness in naturally occurring social insect populations. We investigated if polyandry was beneficial in the social wasp Vespula maculifrons. We used genetic markers to estimate queen mate number in V. maculifrons colonies and assessed colony fitness by counting the number of cells that colonies produced. Our results indicated that queen mate number was directly, strongly, and significantly correlated with the number of queen cells produced by colonies. Because V. maculifrons queens are necessarily reared in queen cells, our results demonstrate that high levels of polyandry are associated with colonies capable of producing many new queens. These data are consistent with the explanation that polyandry is adaptive in V. maculifrons because it provides a fitness advantage to queens. Our research may provide a rare example of an association between polyandry and fitness in a natural social insect population and help explain why queens in this taxon mate multiply.     

WHY DO SOME SOCIAL INSECT QUEENS MATE WITH SEVERAL MALES? TESTING THE SEX‐RATIO MANIPULATION HYPOTHESIS IN LASIUS NIGER

Although multiple mating most likely increases mortality risk for social insect queens and lowers the kin benefits for nonreproductive workers, a significant proportion of hymenopteran queens mate with several males. It has been suggested that queens may mate multiply as a means to manipulate sex ratios to their advantage. Multiple paternity reduces the extreme relatedness value of females for workers, selecting for workers to invest more in males. In populations with female-biased sex ratios, queens heading such male-producing colonies would achieve a higher fitness. We tested this hypothesis in a Swiss and a Swedish population of the ant Lasius niger. There was substantial and consistent variation in queen mating frequency and colony sex allocation within and among populations, but no evidence that workers regulated sex allocation in response to queen mating frequency; the investment in females did not differ among paternity classes. Moreover, population-mean sex ratios were consistently less female biased than expected under worker control and were close to the queen optimum. Queens therefore had no incentive to manipulate sex ratios because their fitness did not depend on the sex ratio of their colony. Thus, we found no evidence that the sex-ratio manipulation theory can explain the evolution and maintenance of multiple mating in L. niger.     

Weight changes in adult hornets,Vespa affinis (Hymenoptera: Vespidae)

Summary After sexuals emerge from their cells, they remain within the nest for 8–11 days (males) or 13–14 days (queens). During this time their weight increases (males 38 %, queens 40 %) due to the laying down of fat in the gaster. The weight of workers does not change over the same period. The fat is utilized by the queen during the 4–5 month overwintering period. When queens emerge in spring their weight is at its lowest, and they feed on nectar. Ovarian development, which was delayed during winter, now begins. During summer, queens again gain weight but this is now due to the development of the ovaries. The queen lives for about 1 year.     

The behaviour of queen honeybees and their attendants

Abstract. The behaviour of queen and worker honeybees (Apis mellifera L.) was observed using small colonies in observation hives. Workers paid more attention to queens which had been mated for 2 months or more than to those which were newly mated; virgin queens received least attention. Queens received most attention when they were stationary and least when they were walking over the comb; virgin queens were most active. Queen cells had as many attendants as virgin queens and queen larvae were inspected almost continuously. The queen pheromone component 9–oxo-trans-2–decenoic acid stimulated 'court' behaviour when presented on small polyethylene blocks, but workers responded aggressively to complete extracts of queens' heads. Both the heads and abdomens of mated queens received much attention from court workers but the abdomens were palpated by more workers for longer and were licked much more. The queens' thoraces were least attended. Abdominal tergites posterior to tergite glands were licked for longer than those anterior to the glands. Only worker bees very near to the queen reacted to her and joined her 'court'.
No evidence was found of a diel periodicity in the behaviour of a queen or her 'court'. During the winter the queen's court was smaller than in summer and she walked less and laid fewer eggs. When colonies were fed with sucrose syrup in winter, their queens laid more eggs and workers reared more brood but there was no change in the attention received by the queens.
The implications of these findings for the secretion and distribution of queen pheromones are discussed.     

Queen fecundity and reproductive skew in the termite Nasutitermes corniger

A major goal of studies on social animals is to understand variation in reproduction within and between groups. We used hierarchical regressions to analyze oviposition rates in the neotropical termite Nasutitermes corniger, a species with both monogynous and polygynous colonies. Queen fecundity was a non-linear, saturating function of queen weight. Greater queen weight was associated with larger nest size and with lower numbers of queens per nest, suggesting competition among queens for resources acquired by the colony. The collective egglaying rate of pairs of queens exceeded that of single queens, but further increases in queen number did not raise total fecundity. Skew in oviposition rates, as quantified by Morisita’s index I _δ, averaged 1.2, indicating inequalities in reproductive rates that are only moderately greater than expected for random apportionment. The leveling off of oviposition with increasing queen weight suggests that it is costly for individual females to produce eggs at high rates, which could favor tolerance of reproduction by other females, reducing reproductive skew. We hypothesize that the incentive to tolerate reproduction by other females is especially pronounced for heavier queens, because these queens are close to the limit of their own reproductive capacity. Consistent with this hypothesis, skew in oviposition rates was inversely related to the mean weight of queens within a nest. Received 8 March 2007; revised 17 September 2007; accepted 3 October 2007.     

Breeding behaviour, relatedness and sex-investment ratios inLeptothorax tuberum Fabricius

The ant speciesLeptothorax tuberum was shown to be predominantly monogynous. Queens usually mate once only but some nests may have a multiply-mated queen or are partially or serially polygynous. As expected from these results, within nest relatedness between workers and between workers and alate queens was found to be high. Almost fifty percent of nests had no nest queen which may indicate high queen mortality, queens leaving to found new nests or nest fragmentation. Observed female investment frequencies (IF _o ) were not significantly different from those expected on the basis of worker control of sexual production and the relatedness estimates of workers to alate queens and workers to males calculated from isozyme data (IF _E ). These values were not consistent with queen control. There was no evidence for lower IF _o s in queenless nests nor for higher IF _o s in larger nests classified by worker number. When nests were classified by sexual productivity, however, there was a strong rank correlation between productivity and female bias. This is the first study of an ant species to test observed IF against expected IF calculated without inferring between caste relatedness from worker data or pooling of data from different castes.     

A comparison of queen oviposition rates from monogyne and polygyne fire ant, Solenopsis invicta, colonies

Abstract. The oviposition rate of individual queens of Solenopsis invicta Buren (Hymenoptera: Formicidae) in relation to their weight and number of queens present in the colony was investigated by direct 2 h observations. There is a strong positive correlation between the weight of a queen and its oviposition rate in both monogyne and polygyne colonies. However, the number of eggs laid per mg queen is higher for moonogyne queens than for polygyne queens. This difference is more evident when the total weight of queens present in a colony is considered. The individual queen oviposition rate is negatively correlated with the number of queens in the colony. In addition, the weight loss per egg laid is significantly greater for polygyne than for monogyne queens, probably due to differences in egg size. These data suggest that oviposition is more efficient in monogyne than in polygyne queens at the individual level; however, at the colony level, polygyne colonies produce significantly more eggs. Comparison of colony level efficiency predicts that polygyne colonies must have at least nine queens to compete reproductively with a mature monogyne queen. Therefore, oligogyny does not appear to be a viable strategy for S.invicata.     

Queen reproduction, chemical signalling and worker behaviour in polygyne colonies of the ant Formica fusca

Potential reproductive conflicts are common in social insects and may occur between and within castes. In multiqueen (polygyne) colonies of ants, reproductive conflicts among coexisting queens may be resolved by aggressive interactions and/or by pheromonal signalling. Pheromonal signals may be directed at workers, which may adjust the reproductive shares of queens behaviourally. Workers are expected to favour a queen that is more likely to be their mother and to produce offspring of close kin to them. We used microsatellite markers to study reproductive partitioning between cobreeding Formica fusca queens in a laboratory experiment where workers received a choice between two queens. We expected queens of this species to communicate their reproductive status by chemical communication, because no aggressive interactions between queens have been observed. We found that queens of different reproductive status (with majority, minority or no production) differed in their cuticular hydrocarbon (CHC) profiles. The fecundity of a queen was associated with worker behaviour; the higher a queen's fecundity, the more attention she received from workers. Our results suggest that a queen fecundity signal is encoded in her CHC profile and acts as a pheromone for workers, which respond to the signal by discriminating between queens. Copyright 2002 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour     

Semi-claustral colony founding in the seed-harvester ant Pogonomyrmex californicus: a comparative analysis of colony founding strategies

The evolution of queens that rear their first brood solely using body reserves, i.e. fully claustral, is viewed as a major advance for higher ants because it eliminated the need for queens to leave the nest to forage. In an apparently unusual secondary modification, the seed-harvester ant Pogonomyrmex californicus displays obligate queen foraging, i.e. queens must forage to garner the resources necessary to survive and successfully rear their first brood. I examined the potential benefits of queen foraging by comparing ecological and physiological traits between P. californicus and several congeners in which the queen can rear brood using only body reserves. The primary advantage of foraging appears to lie in providing the queens of P. californicus with the energy to raise significantly more brood than possible by congeners that use only body reserves; the workers reared in the first brood were also heavier in mass than that predicted by their head width. Other correlates of queen foraging in P. californicus relative to tested congeners included a significantly lower total fat content for alate queens, a small queen body size, and a low queen to worker body mass ratio. Queens also forage in several other well-studied species of Pogonomyrmex, suggesting the possibility that queen foraging may be more common than previously thought in higher ants.     

The genetic structure of swarms and the timing of their production in the queen cycles of neotropical wasps

Kin selection theory has received some of its strongest support from analyses of within-colony conflicts between workers and queens in social insects. One of these conflicts involves the timing of queen production. In neotropical wasps, new queens are only produced by colonies with just one queen while males are produced by colonies with more queens, a pattern favoured by worker interests. We now show that new colonies, or swarms, have few queens and variable within-colony relatednesses which means that their production is not tied to new queen production. The queens in these swarms are seldom the mothers of the workers in the swarm. Therefore, either colonies producing swarms have very many queens, or queens joining daughter swarms are reproductive losers on the original colonies. As new colony production is not linked to queen production, it can occur at the ecologically optimum time, i.e. the rainy season. This disassociation between queen production and new colony production allows worker interests in sex ratios to prevail without hampering new colony production at the most favourable season, an uncoupling that may contribute to the ecological success of the Epiponini.     

The value of oviposition timing,queen presence and kinship in a social insect

Reproductive cooperation confers benefits, but simultaneously creates conflicts among cooperators. Queens in multi-queen colonies of ants share a nest and its resources, but reproductive competition among queens often results in unequal reproduction. Two mutually non-exclusive factors may produce such inequality in reproduction: worker intervention or queen traits. Workers may intervene by favouring some queens over others, owing to either kinship or queen signals. Queens may differ in their intrinsic fecundity at the onset of oviposition or in their timing of the onset of oviposition, leading to their unequal representation in the brood. Here, we test the role of queen kin value (relatedness) to workers, timing of the onset of oviposition and signals of presence by queens in determining the maternity of offspring. We show that queens of the ant Formica fusca gained a significantly higher proportion of sexuals in the brood when ovipositing early, and that the presence of a caged queen resulted in a significant increase in both her share of sexual brood and her overall reproductive share. Moreover, the lower the kin value of the queen, the more the workers invested in their own reproduction by producing males. Our results show that both kinship and breeding phenology influence the outcome of reproductive conflicts, and the balance of direct and indirect fitness benefits in the multi-queen colonies of F. fusca.