Parasite Queens Research Articles

Immune Defense Strategies of Queens of the Social Parasite Ant Acromyrmex ameliae and Queens of Its Natural Hosts

Social parasitism is well known in ants, but many aspects of this social phenomenon remain mysterious and unexplored. In some cases, parasite queens, who are able to mate very rarely end up producing brood and, thus, depend virtually on the labor of host ants. In this work, we sought to test the occurrence of grooming by host workers of Acromyrmex subterraneus subterraneus Forel, to their own queens and queens of the parasite Acromyrmex ameliae De Souza, Soares and Della Lucia and to compare the immune defense responses of parasite queens and queens of A. subterraneus subterraneus and Acromyrmex subterraneus brunneus Forel, the natural hosts. Duration and frequency of behavioral acts were recorded. The relative size of the bulla and the encapsulation response to a standardized antigen were analyzed. Regarding behavioral acts, self-grooming (duration and frequency) and allogrooming (duration) were statistically different between the species; the first is more frequent and lasted longer in parasite queens, while the second act lasted longer in host ants than in parasite ants. The bulla of A. ameliae was approximately 50% wider than those of its hosts. Parasite queens exhibited a stronger immune response than host queens. The results of this work contribute to elucidate potential mechanisms involved in the parasitism capacity of A. ameliae queens such as their strategies of immune defense.

The possible role of ant larvae in the defence against social parasites.

Temporary social parasite ant queens initiate new colonies by entering colonies of host species, where they begin laying eggs. As the resident queen can be killed during this process, host colonies may lose their entire future reproductive output. Selection thus favours the evolution of defence mechanisms, before and after parasite intrusion. Most studies on social parasites focus on host worker discrimination of parasite queens and their offspring. However, ant larvae can also influence brood composition by consuming eggs. This raises the question whether host larvae can aid in preventing colony takeover by consuming eggs laid by parasite queens. To test whether larvae could play a role in anti-parasite defence, we compared the rates at which larvae of a common host species, Formica fusca, consumed eggs laid by social parasite, non-parasite, nest-mate, or conspecific non-nest-mate queens. Larvae consumed social parasite eggs more than eggs laid by a heterospecific non-parasite queen, irrespective of the chemical distance between the egg cuticular profiles. Also, larvae consumed eggs laid by conspecific non-nest-mate queens more than those laid by nest-mate queens. Our study suggests that larvae may act as players in colony defence against social parasitism, and that social parasitism is a key factor shaping discrimination behaviour in ants.

Integration strategies of a leaf-cutting ant social parasite

To enter and integrate into host nests, ant social parasites employ a variety of behavioural and chemical strategies for bypassing host defences. Alternative chemical strategies are often considered separately, because only one is assumed to be effective in each particular species or in specific phases of the usurpation process. We studied the integration process of inquiline social parasite queens of Acromyrmex insinuator into nests of its host, the leaf-cutting ant Acromyrmex echinatior. When transplanted to a new host colony, parasite queens were initially attacked but later accepted by host workers, while non-nestmate host queens were always killed in this process. Parasite queens were more readily accepted by host colonies that already contained a parasite queen. The cuticular chemical profiles of parasite queens appeared to be specific to a host colony and parasite queens had higher amounts of cuticular n-alkanes than host queens, a substance class that is typically not relevant for nestmate recognition. We found evidence for two chemical strategies that are not mutually exclusive: (1) increased n-alkane levels suggest chemical insignificance, i.e. that parasites are able to enter host colonies because crucial recognition labels are absent, and (2) colony specificity of labels and attacks by non-nestmate host workers suggest that camouflage, a gradual acquisition of host colony-specific labels during integration, applies as well. We argue that combining insignificance and camouflage may be synergistically adaptive for intruding inquiline queens when this leads to a higher likelihood of achieving permanent acceptance.

Genetic divergence between the sympatric queen morphs of the ant Myrmica rubra.

Pairs of obligate social parasites and their hosts, where some of the parasites have recently diverged from their host through intraspecific social parasitism, provide intriguing systems for studying the modes and processes of speciation. Such speciation, probably in sympatry, has also been propounded in the ant Myrmica rubra and its intraspecific social parasite. In this species, parasitism is associated with queen size dimorphism, and the small microgyne has become a social parasite of the large macrogyne. Here, we investigated the genetic divergence of the host and the parasite queen morphs in 11 localities in southern Finland, using nuclear and mitochondrial markers of queens and workers. We formulated and tested four speciation-related hypotheses that differed in the degree of genetic divergence between the morphs. The queen morphs were genetically distinct from each other with little hybridization. In the nuclear data, when localities were nested within queen morphs in the hierarchical amova, 39% of the genetic variation was explained by the queen morph (standardized F'CT = 0.63, uncorrected FCT = 0.39), whereas 18% was explained by the locality (F'SC = 0.39, FSC = 0.29). This result corroborated the hypothesis of advanced sympatric speciation. In contrast, the mitochondrial DNA could not settle between the hierarchical levels of locality and queen morph, thus substantiating equally the hypotheses of incipient and advanced sympatric speciation. Together, our results support the view that the microgynous parasite has genetically diverged from its macrogynous host to the level of a nascent species.

Colony take-over and brood survival in temporary social parasites of the ant genus Formica

Parasites reduce host fitness, and so instigate counter adaptations by their hosts. In temporary social parasitism, usurpers must not only enter the colony unharmed, but also have their eggs reared by the host workers. We introduced parasitic Formica lugubris and Formica aquilonia queens into queen right and orphaned fragments of three host species, Formica cinerea, Formica picea and Formica fusca, and show that workers of all three host species kill over 40 % of the introduced queens within 10 days, regardless of the presence/absence of a resident queen, and parasite species. More parasite queens died in F. cinerea than in F. picea and F. fusca. There were no major differences in survival between the parasite species (except that F. lugubris survived longer than F. aquilonia in F. fusca colonies compared to F. picea colonies), but parasite queens survived longer in orphaned than in queen right fragments of F. fusca. Experimental introduction of parasite (F. aquilonia) eggs into orphaned colonies of F. fusca showed that none of the parasite eggs were reared until pupation; whereas on average, 12 % of the con-specific hetero-colonial eggs introduced in the same manner were reared until pupation. In all colonies that received parasite brood, all offspring consisted of worker-laid males, whereas the corresponding value was 50 % for colonies that received con-specific hetero-colonial brood. Thus, when the risks of entering host colonies and brood failure are combined, the rate of successful colony take-over is very low. Moreover, the host workers can to some extent alleviate the costs of parasitism by producing a final batch of own offspring.

Raiders from the sky: slavemaker founding queens select for aggressive host colonies

Reciprocal selection pressures in host-parasite systems drive coevolutionary arms races that lead to advanced adaptations in both opponents. In the interactions between social parasites and their hosts, aggression is one of the major behavioural traits under selection. In a field manipulation, we aimed to disentangle the impact of slavemaking ants and nest density on aggression of Temnothorax longispinosus ants. An early slavemaker mating flight provided us with the unique opportunity to study the influence of host aggression and demography on founding decisions and success. We discovered that parasite queens avoided colony foundation in parasitized areas and were able to capture more brood from less aggressive host colonies. Host colony aggression remained consistent over the two-month experiment, but did not respond to our manipulation. However, as one-fifth of all host colonies were successfully invaded by parasite queens, slavemaker nest foundation acts as a strong selection event selecting for high aggression in host colonies.

Chemical camouflage of the slave-making ant Polyergus samurai queen in the process of the host colony usurpation (Hymenoptera: Formicidae)

Founding queens of the obligatory social parasite ant Polyergus samurai usurp the host ant Formica japonica colony. The aggressive behaviors of F. japonica workers on the parasite queen disappear after the parasite queen kills the resident queen. To determine whether the parasite queen chemically mimics the host ants, we examined the aggressive behavior of F. japonica workers toward glass dummies applied with various extracts of the parasite queen and host workers. The crude extracts and hydrocarbon fraction reproduced the host workers’ behavior to the live ants. The extracts of the post-adoption parasite queen, as well as the nestmate extracts of F. japonica, did not elicit the aggressive behavior, but the extract of the pre-adoption parasite queen triggered attacks by the host workers. The nestmate recognition of host workers did not change, regardless of contact with the parasite. The gas chromatography and gas chromatography–mass spectrometry analyses indicated that the cuticular hydrocarbon (CHC) profile of the parasite queen drastically changed during the process of usurpation. Discriminant analysis showed the successfully usurped P. samurai queen had colony-specific CHC profiles. CHC profiles of the P. samurai queen who killed the host queen were more similar to those of the host queen than the workers, while the P. samurai queen who usurped the queenless colony had a profile similar to those of host workers. These results suggest that the P. samurai queen usually acquires the CHCs from the host queen during the fight, but from host wokers in queenless host colonies.

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.

Comparative reproductive biology of the social parasite Acromyrmex ameliae de Souza, Soares & Della Lucia and of its host Acromyrmex subterraneus subterraneus Forel (Hymenoptera: Formicidae)

Social parasites exhibit several characteristics that allow them to exploit their host species efficiently. The smaller size of parasite species is a trait commonly found in ants. In this work, we investigated several aspects of the reproductive biology of Acromyrmex ameliae De Souza, Soares & Della Lucia, a recently discovered parasite of Acromyrmex subterraneus subterraneus Forel. Sexuals of A. ameliae are substantially smaller than those from host species. Parasite queens laid significantly less worker eggs than host queens and inhibit sexual production of the host. The sex ratio of parasite species is highly female biased. Interestingly, we have observed parasite coupling on the laboratory, inside the nests and in the ground, opening the possibility to use controlled mating to study genetic approaches of parasitism in the ants.

Repellent effect on host Formica workers of queen Dufour's gland secretion of the obligatory social parasite ant, Polyergus samurai (Hymenoptera: Formicidae)

Founding queens of the obligatory social parasite ant Polyergus samurai usurp the host Formica japonica colony. The queen secretes chemicals from its gaster when killing the host queen. At this time, the parasite queen is hardly attacked by host workers. We hypothesized that the queen's secretion acts as a repellent to deter host workers' aggression during host queen killing. Gas chromatograph-mass spectrometry analyses confirmed that the chemical composition of Dufour's gland contents of P. samurai queens was almost identical to the chemicals remaining on the body surface of host Formica queens killed by them. Host F. japonica workers were used for bioassays. In an encounter with an intruder ant, the workers' aggression to the intruder was reduced significantly when Dufour's gland extract was applied to the intruder. Treatment of workers with the gland extract significantly increased the receding behavior of nestmates. The host workers receded from a glass dummy treated with the gland extract. The time necessary for a worker to get over a barricade applied with gland extract was significantly longer than that of controls. These results strongly suggest that Dufour's gland secretion acts as a repellent allomone.

Do these eggs smell funny to you?: an experimental study of egg discrimination by hosts of the social parasite Polyergus breviceps (Hymenoptera: Formicidae)

Social parasites exploit the behaviours of other social species. Infiltration of host systems involves a variety of mechanisms depending on the conditions within the host society and the needs of the social parasite. For many species of socially parasitic ants, colony establishment entails the usurpation of colonies of other species. This frequently involves the eviction or death of the host colony queen and the subsequent adoption of the invading queen. The social parasite queen achieves host worker acceptance by either manipulating the nest-mate recognition processes of the host or undergoing chemical modification. Little is known, however, about how host workers respond to social parasite eggs or whether host species defend against brood parasitism during parasite invasions. Host species are believed to adopt social parasite offspring because the recent common ancestry between many social parasites and their hosts may grant the sharing of certain characteristics such as chemical cues. Use of multiple host species, however, suggests other processes are needed for the social bond between host and parasite young to form. This study reports the findings of adoption bioassays in which eggs from a slave-maker ant, Polyergus breviceps, were offered to workers of two of its host species from unparasitised or newly parasitised nests to determine whether P. breviceps eggs generally elicit rearing behaviours from multiple host species. Comparisons of parasite egg survival until adulthood with conspecific egg survival reveal that workers of both host species, free-living or newly enslaved, do not typically accept slave-maker eggs. Both host species thus have sufficient discriminatory power to reject social parasite eggs although our hydrocarbon analysis indicates parasite eggs may be adapted to their local host species. Combined these results suggest that host rearing of P. breviceps eggs may reflect an evolutionary equilibrium that is maintained by probability and cost of recognition errors.

Knowing your enemies: seasonal dynamics of host-social parasite recognition.

Despite its evolutionary significance, behavioural flexibility of social response has rarely been investigated in insects. We studied a host-social parasite system: the slave-making ant Polyergus rufescens and its host Formica rufibarbis. Free-living host workers from parasitized and from unparasitized areas were compared in their level of aggression against the parasite and alien conspecifics. We expected that a seasonal change would occur in the acceptance threshold of F. rufibarbis workers from a parasitized area towards the parasite, whereas F. rufibarbis workers from an unparasitized area would not show substantial changes connected with the parasite's peak in activity (raiding and colony-founding season). The results showed a significant adaptive behavioural flexibility of host species workers and are consistent with the acceptance threshold model's (Reeve 1989) prediction that recognition systems are not fixed but context-dependent. In particular, host workers from the unparasitized area were highly aggressive towards the parasite regardless of the season, whereas host workers from the parasitized area significantly increased their aggression towards the parasite during its raiding and colony-founding season. Being able to detect and possibly kill a Polyergus scout searching for host nests can be an effective strategy for a Formica colony to avoid being raided or usurped by a parasite queen.

Ant parasite queens revert to mating singly.

Multiple mating (polyandry) is widespread among animal groups, particularly insects. But the factors that maintain it and underlie its evolution are hard to verify because benefits and costs are not easily quantified and they tend to be similar in related species. Here we compare the mating strategies of the leaf-cutting ant Acromyrmex echinatior and its recently derived social parasite Acromyrmex insinuator, which is also its closest relative. We find that although the host queens mate with up to a dozen different males, the social parasite mates only singly. This rapid and surprising reversion to single mating in a socially parasitic ant indicates that the costs of polyandry are probably specific to a free-living lifestyle.

Social wasp parasites affect the nestmate recognition abilities of their hosts ( Polistes atrimandibularis and P. biglumis , Hymenoptera, Vespidae)

Queens of the parasitic social wasp, Polistes atrimandibularis, temporarily mimic the odor of their host species, Polistes biglumis, but their offspring have parasite-specific odors. As a consequence, in parasitized colonies individuals with different odors co-inhabit the colony and host workers, who are responsible for colony defense, accept wasps with different odors. In order to verify whether this particular condition causes a change in recognition abilities of hosts, we tested nestmate/non-nestmate discrimination in field colonies invaded by social parasites (and in non-parasitized colonies as controls). Results show that parasitized colonies distinguish between nestmates and non-nestmates, distinguish their parasite queen from those that usurped alien colonies, and accept their parasite's non-mimetic offspring but make more recognition errors than non-parasitized colonies. The optimal acceptance threshold model predicts that when the frequency of encountering non-kin increases, residents become less permissive towards intruders. However, my data show that parasitized colonies are more permissive towards non-nestmates with respect to non-parasitized colonies but they are also more aggressive towards nestmates, suggesting that host workers' learning abilities are impaired.

Behavior of Usurping Queens in Colonies of the Ant species Leptothorax nylanderi (Hymenoptera: Formicidae)

Animals can reduce their costs of parental care by exploiting the behavior of unrelated conspecifics. Such 'intraspecific parasitism' has been observed in the small ant species, Leptothorax nylanderi. This study aims to identify how parasite queens of Leptothorax nylanderi are integrated into established colonies. Both in natural multi-queen colonies and in manipulated laboratory colonies, workers were temporarily aggressive towards the usurper queen, which herself remained initially passive and inconspicuous but later attacked the resident queen, the workers and the brood. Queen-queen aggression led to the elimination of one of the two queens and the restoration of monogyny. Usurpation is not associated with size polymorphism in L nylanderi.

Social parasitism in ants: effects of the inquiline parasite Plagiolepis xene St. on queen distribution and worker production of its host Plagiolepis pygmaea Latr.

The ant Plagiolepis pygmaea forms polygynous (several mated queens per colony) and polydomous (multiple nests per colony) colonies that may be parasitized by the workerless social parasite Plagiolepis xene. Earlier laboratory experiments showed that P. xene strongly restricts host worker production (Passera, 1972); however, this negative effect seems not to occur under natural conditions. Here, we explored the hypothesis that, in infested natural colonies of P. pygmaea, parasite queens affect the distribution of the host queens resulting in the latter inhabiting unparasitized nests of the colony at the period of egg-laying. Our field studies show that the presence of the inquiline ant P. xene influences host queen distribution, with a higher level of dispersion within parasitized colonies. In winter, there is a positive association between the number of host queens and the number of parasites in queenright nests. Such a relationship does not occur in summer, so that when egg-laying reaches its maximum activity most queens of the host are found in unparasitized nests. Moreover, the proportion of queenright nests parasitized was dramatically lower than in the winter. A detailed comparison of worker production between parasitized and unparasitized field colonies reveals no difference. Experiments show that reduced worker production in parasitized nests reared under laboratory conditions results from oophagy by the parasitic queens. Overall, our data suggest that the segregation of the host and parasite queens in different nests at the time of egg-laying results in part from host queens avoiding inhabiting parasitized nests to reduce oophagy by the parasite. We discuss the behavioral and ecological implications of our findings.

Changes in the cuticular hydrocarbon profile of the slave-maker ant queen, Polyergus breviceps emery, after killing a Formica host queen (Hymenoptera: Formicidae).

Queens of the slave-maker ant, Polyergus breviceps, take over nests of their Formica host species by fatally attacking the resident queen. As workers only begin grooming the P. breviceps queen once she has ceased her attack, we investigated whether a change in parasite queen chemistry may account for the change in worker behavior. Cuticular hydrocarbon profiles of newly mated P. breviceps queens and of queens of their two Formica host species were found to be species-specific. Profiles of newly mated P. breviceps queens that had attacked a Formica queen, however, were virtually identical to the queen profile of the species killed. Mass spectral analysis revealed that the hydrocarbons on the cuticles of newly mated P. breviceps changed from primarily normal alkanes to methyl and di-methyl branched alkanes after attacks. The results suggest that cuticular compounds from the host queen were transferred to the parasite queen during their aggressive interaction.

Chemical ecology and social parasitism in ants.

The chemical strategies by which parasites manage to break into the social fortresses of ants offer a fascinating theme in chemical ecology. Semiochemicals used for interindividual nestmate recognition are also involved in the mechanisms of tolerance and association between the species, and social parasites exploit these mechanisms. The obligate parasites are odorless ("chemical insignificance") at the time of usurpation, like all other callow ants, and this "invisibility" enables their entry into the host colony. By chemical mimicry (sensu lato), they later integrate the gestalt odor of this colony ("chemical integration"). We hypothesize that host and parasite are likely to be related chemically, thereby facilitating the necessary mimicry to permit bypassing the colony odor barrier. We also review the plethora of chemical weapons used by social parasites (propaganda, appeasement, and/or repellent substances), particularly during the usurpation period, when the young mated parasite queen synthesizes these chemicals before usurpation and ceases such biosynthesis afterwards. We discuss evolutionary trends that may have led to social parasitism, focusing on the question of whether slave-making ants and their host species are expected to engage in a coevolutionary arms race.

New Host for the Parasitic Ant Solenopsis daguerrei (Hymenoptera: Formicidae) in Argentina

The parasitic ant Solenopsis daguerrei (Santschi) has been reported as an inquiline of fire ants in South America. It lacks a worker caste, so all adults are reproductive males and females. The parasite queens and occasionally some virgin females attach themselves to the host queens, and divert resources from them. The fire ant workers tend S. daguerrei in a manner similar to their own mother queens (Bruch 1930). The host workers also feed and maintain the brood of S. daguerrei. According to Silveira-Guido et al. (1973) this parasite inhibits the egg production of the fire ant mother queen, thus causing the ant colony to collapse and eventually die out. Recently it was reported that multiple-queen colonies of fire ants parasitized with S. daguerrei have fewer queens than non parasitized ones (Calcaterra et al. 1999). Because of these findings, this parasitic ant is a candidate for introduction for the biological control of imported fire ants in the United States and is under quarantine conditions at the USDA-ARS CMAVE, Gainesville, FL. However, before S. daguerrei can be released from quarantine, its host specificity must be determined. Surveys on fire ant natural enemies in South America revealed that S. daguerrei has been found in Argentina, Uruguay, and Brazil, in colonies of S. richteri Forel, S. invicta Buren, S. saevissima F. Smith, and S. macdonaghi Santschi (Silveira-Guido et al. 1973, Briano et. al. 1997, Pesquero et al. 1998, Calcaterra et al. 1999). Here we report a new host species for S. daguerrei. As part of the study of the specificity of S. daguerrei, a field host range survey was conducted in San Eladio (60 km W of Buenos Aires), Argentina, the only place where S. daguerrei has been found consistently since 1995. This area had the highest abundance (7% of fire ant colonies) of S. daguerrei recorded in South America to date (Briano et al. 1997). The surveys were conducted from December 1996 to May 1997 and from November 1997 to May 1998 and consisted in walking through the pastures to visually detect the ant colonies. When an ant nest was found, it was excavated, scattered on the ground, and thoroughly examined for S. daguerrei adults. Some colonies were excavated and put into 10-liter buckets for separation in the laboratory by flotation (Banks et al. 1981). The floated colonies were put in rearing trays (40 by 30 by 15 cm) and examined later. Alcohol samples were kept of most ant species found. Samples of 34 parasitized fire ant colonies were preserved in hexane to confirm their identification by gas chromatography analysis of cuticular hydrocarbons and venom alkaloids (Vander Meer & Lofgren 1988). Voucher samples were deposited at the USDA-ARS, SABCL collection and at the USDA-ARS, CMAVE, Gainesville, FL. We sampled a total of 4,316 ant colonies of 9 different species in 4 subfamilies, however 96% of them were fire ants. Other species examined were: Pheidole bergi Mayr, Acromyrmex lundi Gu6rin, A. ambiguus Mayr, Camponotus punctulatus Mayr, Neivamyrmex pertyi Shuckard, Linepithema humile Mayr, and Brachymyrmex sp. S. daguerrei was found exclusively in 161 colonies of fire ants (Table 1). Taxonomic studies revealed that 95% of the parasitized colonies corresponded to S. richteri. The

Social hackers: integration in the host chemical recognition system by a paper wasp social parasite.

Obligate social parasites in the social insects have lost the worker caste and the ability to establish nests. As a result, parasites must usurp a host nest, overcome the host recognition system, and depend on the host workers to rear their offspring. We analysed cuticular hydrocarbon profiles of live parasite females of the paper wasp social parasite Polistes sulcifer before and after usurpation of host nests, using the non-destructive technique of solid-phase micro-extraction. Our results reveal that hydrocarbon profiles of parasites change after usurpation of host nests to match the cuticular profile of the host species. Chemical evidence further shows that the parasite queen changes the odour of the nest by the addition of a parasite-specific hydrocarbon. We discuss the possible role of this in the recognition and acceptance of the parasite and its offspring in the host colony.