Host colony usurpation by the queen of the Japanese pirate ant, Polyergus samurai (hymenoptera: formicidae)

Colony usurpations by newly mated queens of Polyergus samurai were observed under artificial conditions. Newly mated queens of P. samurai were introduced into three kinds of Formica japonica host colonies: queenright, queenless (artificially orphaned), and workerless (only a queen remaining) colonies. In the queenright condition, the P. samurai queen intruded into the host nest and killed the host queen, and was subsequently adopted by the host workers. In all queenright and queenless host colonies, seven of 13 queens of P. samurai succeeded in colony usurpation, although the starting time of grooming, a nestmate behavior, by host workers in the queenright condition occurred earlier than in the queenless condition. In workerless conditions, four of five P. samurai queens ignored the F. japonica queen. The results suggest that while host-queen killing is not necessary, it is important to win acceptance by host workers.     

Cuticular spectra in the slave-making ant Polyergus rufescens and the slave species Formica rufibarbis

Abstract. The relative proportions of cuticular components having the same retention times were compared between the slave-making ant Polyergus rufescens and the slave ant Formica rufibarbis living in monospecific or mixed colonies. The two species were found to present different spectra. The Formica workers, when enslaved by Polyergus , tend to lose their colony characteristics but they do not seem to adopt the characteristics of Polyergus.     

Evidence for adaptive brain tissue reduction in obligate social parasites (Polyergus mexicanus) relative to their hosts (Formica fusca)

Brain investment is evolutionarily constrained by high costs of neural tissue. Several ecological factors favour the evolution of increased brain investment; we predict reduced brain region investment will accompany the evolution of organismal or social parasitism when parasites rely on host behaviour and cognition to solve ecological problems. To test this idea we investigated whether brain region investments differed between obligate slave‐making Polyergus mexicanus ant workers and their Formica fusca slave workers. Polyergus workers perform little labour for their colonies; enslaved workers of Formica host species forage, excavate nests and tend the brood. We focused on the calyces of the mushroom bodies, central processing brain regions that are larger in social insect workers that perform complex tasks. As predicted we found lower relative investment in mushroom body calyx in P. mexicanus workers than in F. fusca workers; by contrast, enslaved and free F. fusca workers did not differ in mushroom body calyx volume. We then tested whether slave‐makers and hosts differed in brain investment among sensory modalities. Polyergus slave‐makers employ several unique classes of pheromones during raids, and eye size relative to head size was smaller in P. mexicanus workers than in F. fusca workers. The size of antennal brain tissues relative to visual tissues was greater in Polyergus, both in the peripheral sensory lobes and in the mushroom body calyx, suggesting greater relative investment in antennal processing by slave‐makers. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 415–422.     

Integration raids in the Amazon ant Polyergus rufescens (Hymenoptera, Formicidae)

Summary. Groups of enslaved Formica fusca workers from mixed colonies of Polyergus rufescens with numerous slave workforce tend to split off and found small and almost homospecific nests around the main nest, with at least some of them connected with the latter with underground passages. Their inhabitants are able, at least temporarily, to adopt young F. fusca gynes. P. rufescens invades these satellite nests in a manner similar to the normal slave raids, and carries the slaves back to the main nest. The supposed evolutionary cause of this behaviour is to keep integrity of mixed colonies and prevent possible emancipation of slaves.Received 18 August 2004; revised 27 September 2004; accepted 11 October 2004.     

Recognition of Individuals from Mixed Colony by Formica sanguinea and Formica polyctena Ants

It was examined whether Formica polyctena and F. sanguinea ants from a mixed colony elicit higher levels of aggression of conspecific ants in comparison to ants from homospecific colonies. Individuals were confronted in an experimental arena and their behavior was recorded. It was found that F. polyctena workers behaved more aggressively toward ants from a mixed colony. This pattern, however, was not confirmed in F. sanguinea. Moreover, both species clearly discriminated between conspecific and allospecific ants from a mixed colony. It seems that as a result of social interactions both species exchanged cuticular hydrocarbons, which caused their recognition labels to adjust to some extent. Results of the present study support the idea that that F. sanguinea is able to form mixed colonies in which species-specific recognition cues are probably still retained.     

Ants exhibit asymmetric hybridization in a mosaic hybrid zone

Research on hybridization between species provides unparalleled insights into the pre‐ and postzygotic isolating mechanisms that drive speciation. In social organisms, colony‐level incompatibilities may provide additional reproductive barriers not present in solitary species, and hybrid zones offer an opportunity to identify these barriers. Here, we use genotyping‐by‐sequencing to sequence hundreds of markers in a hybrid zone between two socially polymorphic ant species, Formica selysi and Formica cinerea. We characterize the zone, determine the frequency of hybrid workers, infer whether hybrid queens or males are produced and investigate whether hybridization is influenced by colony social organization. We also compare cuticular hydrocarbon profiles and aggression levels between the two species. The hybrid zone exhibits a mosaic structure. The asymmetric distribution of hybrids skewed towards F. cinerea suggests a pattern of unidirectional nuclear gene flow from F. selysi into F. cinerea. The occurrence of backcrossed individuals indicates that hybrid queens and/or males are fertile, and the presence of the F. cinerea mitochondrial haplotype in 97% of hybrids shows that successful F1 hybrids will generally have F. cinerea mothers and F. selysi fathers. We found no evidence that social organization contributes to speciation, because hybrids occur in both single‐queen and multiple‐queen colonies. Strongly differentiated cuticular hydrocarbon profiles and heightened interspecific aggression further reveal that species recognition cues are both present and perceived. The discovery of fertile hybrids and asymmetrical gene flow is unusual in ants, and this hybrid zone will therefore provide an ideal system with which to investigate speciation in social insects.     

Weak patriline effects are present in the cuticular hydrocarbon profiles of isolated Formica exsecta ants but they disappear in the colony environment

Chemical recognition cues are used to discriminate among species, con‐specifics, and potentially between patrilines in social insect colonies. There is an ongoing debate about the possible persistence of patriline cues despite evidence for the mixing of colony odors via a “gestalt” mechanism in social insects, because patriline recognition could lead to nepotism. We analyzed the variation in recognition cues (cuticular hydrocarbons) with different mating frequencies or queen numbers in 688 Formica exsecta ants from 76 colonies. We found no increase in the profile variance as genetic diversity increased, indicating that patriline effects were absent or possibly obscured by a gestalt mechanism. We then demonstrated that an isolated individual's profile changed considerably relative to their colony profile, before stabilizing after 5 days. We used these isolated individuals to eliminate the masking effects of the gestalt mechanism, and we detected a weak but statistically significant patriline effect in isolated adult workers and also in newly emerged callow workers. Thus, our evidence suggests that genetic variation in the cuticular hydrocarbon profile of F. exsecta ants (n‐alkanes and alkenes) resulted in differences among patrilines, but they were obscured in the colony environment, thereby avoiding costly nepotistic behaviors.     

Cuticular spectra and inter-individual recognition in the slave-making ant Polyergus rufescens and the slave species Formica rufibarbis

Abstract. The relationship between behavioural tests and relative proportions of cuticular components were studied in the slave-making species Polyergus rufescens and the slave and Formica rufibarbis living in either monospecific or mixed colonies. A correlation between the relative proportions of the cuticular products and interindividual recognition exists in each of the two species Polyergus and Formica: Polyergus are fiercely aggressive towards individuals which have different cuticular spectra and originate from a geographically isolated nest. This seems to be true also in the case of Formica living in monospecific colonies. A similar correlation also exists between the two species, which have different cuticular spectra: encounters arranged between them show that free-living Formica are always fiercely aggressive towards Polyergus. The reason why no such correlation seems to exist, however, between Polyergus and Formica when the latter are enslaved and the two species coexist peacefully at the same nest is discussed.     

The role of an attractive brood pheromone in the obligatory,slavemaking ant,Polyergus breviceps (hymenoptera: Formicidae)

Freeliving workers of Formica occulta, an ant species enslaved by the obligatory slavemaking ant Polyergus breviceps, retrieve and nurse Polyergus pupaejust as well as conspecific pupae in a choice test. No such attraction was found toward pupae of the facultative slavemaker; Formica wheeleri,which also enslaves F. occulta. Formica neogagates,a sympatric species which is not parasitized by either slavemaker, preferentially retrieves and tends conspecific brood over that of Polyergusand F. wheeleri.It is proposed that brood of obligatory slavemaking species must possess an attractive pheromone for slavemaker colony foundation to be successful, since slavemaker brood must be nursed by adult slave workers with no prior exposure to slavemaker brood. An attractive pheromone is not necessary in the brood of facultative slavemakers, since this brood is cared for by newly eclosed slave workers who imprint on the slavemaker brood.     

Blending in with the crowd: social parasites integrate into their host colonies using a flexible chemical signature

Social parasites are able to exploit their host's communication code and achieve social integration. For colony foundation, a newly mated slave-making ant queen must usurp a host colony. The parasite's brood is cared for by the hosts and newly eclosed slave-making workers integrate to form a mixed ant colony. To elucidate the social integration strategy of the slave-making workers, Polyergus rufescens, behavioural and chemical analyses were carried out. Cocoons of P. rufescens were introduced into subcolonies of four potential host species: Formica subgenus Serviformica (Formica cunicularia and F. rufibarbis, usual host species; F. gagates, rare host; F. selysi, non-natural host). Slave-making broods were cared for and newly emerged workers showed several social interactions with adult Formica. We recorded the occurrence of abdominal trophallaxis, in which P. rufescens, the parasite, was the donor. Social integration of P. rufescens workers into host colonies appears to rely on the ability of the parasite to modify its cuticular hydrocarbon profile to match that of the rearing species. To study the specific P. rufescens chemical profile, newly emerged callows were reared in isolation from the mother colony (without any contact with adult ants). The isolated P. rufescens workers exhibited a chemical profile closely matching that of the primary host species, indicating the occurrence of local host adaptation in the slave-maker population. However, the high flexibility in the ontogeny of the parasite's chemical signature could allow for host switching.     

Chemical mimicry of the ant Oecophylla smaragdina by the myrmecophilous spider Cosmophasis bitaeniata: Is it colony-specific?

Workers of most social insects can distinguish between nestmates and non-nestmates, and actively attack the latter if they attempt to intrude into the nest or surrounding territory. Nevertheless, there are many records of heterospecific organisms living within the nests of social insects, and they are thought to gain access through chemical mimicry. The salticid spider Cosmophasis bitaeniata lives within the leaf nests of the ant Oecophylla smaragdina, where it preys on the ant larvae. We investigated, using behavioural bioassays and chemical analyses, whether the previously reported resemblance of the cuticular hydrocarbons of ant and spider was colony-specific. Behavioural experiments revealed that the spiders can distinguish between nestmate and non-nestmate major workers and are less inclined to escape when confined with ants that are nestmates. More significantly, C. bitaeniata were more likely to capture ant larvae from nestmate minor workers than non-nestmate minor workers. The chemical analyses revealed that the cuticular hydrocarbon profiles of the spiders and the major workers of the ant colonies were colony-specific. However, the hydrocarbon profiles of C. bitaeniata do not match those of the major workers of O. smaragdina from the same colony. Perhaps the colony-specific cuticular hydrocarbon profiles of C. bitaeniata function to obtain prey from the minor workers rather than avoid eliciting aggression from the major workers.     

Workers and queens of the European hornetVespa crabro L. have colony-specific cuticular hydrocarbon profiles (Hymenoptera: Vespidae)

Summary Cuticular hydrocarbons were extracted from sixty individual workers from six colonies ofVespa crabro L. and analyzed by combined gas-chromatography/mass spectrometry. Discriminant analysis of the cuticular hydrocarbon profiles of workers and queens showed that the wasps could be grouped by colony and by caste. Stepwise discriminant analysis selected the components which were weighted most heavily in these analyses. Different combinations of cuticular hydrocarbons were important in grouping workers by colony, queens and workers by colony, and workers and queens by caste.     

Colony structure of a slavemaking ant. II. Frequency of slave raids and impact on the host population

The parasite pressure exerted by the slavemaker ant Protomognathus americanus on its host species Leptothorax longispinosus was analyzed demographically and genetically. The origin of slaves found in colonies of the obligate slavemaker was examined with nuclear and mitochondrial DNA markers to make inferences about the frequency and severity of slave raids. Relatedness of enslaved L. longispinosus workers in the same nest was very low, and our data suggest that, on average, each slavemaker nest raids six host colonies per season. Therefore, the influence of slavemaker species on their hosts is much stronger than simple numerical ratios suggest. We also found that slave relatedness was higher in small than in large slavemaker nests; thus, larger nests wield a much stronger influence on the host. We estimated that in the study population, on average, a host nest has a 50% chance of being attacked by a slavemaker colony per year. Free-living Leptothorax colonies in the vicinity of slavemaker nests did not represent the source of slaves working in P. americanus colonies, which suggests that raided nests either do not survive or migrate after being raided. Colony composition and intranest relatedness of free-living L. longispinosus colonies differed markedly between areas with slavemakers and those that are parasite-free. In the presence of slavemakers, host colonies were less likely to be polygynous and had fewer workers and a higher relatedness among worker brood. Host nests with slavemaker neighbors allocated more resources into sexuals, possibly caused by these shifts in nest demography. Finally, enslaved Leptothorax workers in P. americanus nests appeared to be less efficient than their counterparts in free-living colonies. Thus, slavemakers exert a much stronger impact on their hosts than had previously been suspected and represent an unique system to study parasite-host coevolution.     

Colony stage and not facultative policing explains pattern of worker reproduction in the Saxon wasp

Inclusive fitness theory predicts that in colonies of social Hymenoptera headed by a multiple‐mated queen, workers should benefit from policing eggs laid by other workers. Foster & Ratnieks provided evidence that in the vespine wasp Dolichovespula saxonica, workers police other workers’ eggs only in colonies headed by a multiple‐mated queen, but not in those headed by a single‐mated one. This conclusion, however, was based on a relatively small sample size, and the original study did not control for possible confounding variables such as the seasonal colony progression of the nests. Our aim, therefore, was to reinvestigate whether or not facultative worker policing occurs in D. saxonica. Remarkably, our data show that in the studied Danish population, there was no correlation between worker–worker relatedness and the percentage of worker‐derived males. In addition, we show that variability in cuticular hydrocarbon profiles among the workers did not significantly correlate with relatedness and that workers therefore probably did not have sufficient information on queen mating frequency from the workers’ cuticular hydrocarbon profiles. Hence, there was no evidence that workers facultatively policed other workers’ eggs in response to queen mating frequency. Nevertheless, our data do show that the seasonal progression of the nest and the location in which the males were reared both explain the patterns of worker reproduction found. Overall, our results suggest that the earlier evidence for facultative worker policing in D. saxonica may have been caused by accidental correlations with certain confounding variables, or, alternatively, that there are large interpopulation differences in the expression of worker policing.     

Selective acceptance of the brood of two formicine slave-making ants by host and non-host related species

Summary In a laboratory choice-test, free-living ant workers ofFormica cunicularia andF. rufibarbis (subgenusServiformica), both potentially slave species of the obligatory slave-makerPolyergus rufescens, cared for cocoons of this parasite and for homocolonial cocoons at comparable rates. Both potential hosts did not differ in their capacity to rear the parasite brood. This fact is discussed in relation to host selection and specificity inP. rufescens. No such attraction and/or tolerance was found towards cocoons of the facultative slave-makerFormica sanguinea, which also enslaves both host species. Workers ofF. lugubris, a species which is never enslaved, destroyed cocoons from both slave-making species. The attractiveness of the brood ofP. rufescens for both potentially slave species could be due to an interspecific brood pheromone in addition to brood mimicry. An alternative hypothesis is a close phylogenetic distance between this slave-maker andServiformica species. The capacity to gain acceptance by adult slave workers might be one of the crucial evolutionary steps separating obligatory from facultative slave-making ants.     

Raiding behavior of the Japanese slave-making antPolyergus samurai

Summary Raiding behavior of the Japanese slave-making antPolyergus samurai was investigated in the field. Raiding trips occurred from early June to early September. A raiding column of several hundreds workers would rush into a target nest and rob mainly worker pupae of the host species,Formica (Serviformica) japonica. Most trips occurred on sunny days. Air temperature, soil temperature, relative humidity, and radiation energy at the ground surface were significantly different between days with and without raiding trips. Nuptial flights occurred on hot, sunny days, and mostPolyergus colonies released alates simultaneously. Behaviors of newly mated queens are also provided and are compared with otherPolyergus species.     

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.     

Raiding Activity of an Obligate (Polyergus breviceps) and Two Facultative (Formica puberula and F. gynocrates) Slave-Making Ants

Slave-making ants are social parasites that exploit the labor of workers from their host species by keeping them captive in the slave-maker nest. Slave-makers vary in their degree of specialization, ranging from obligate slave-makers that cannot survive without captives, to facultative slave-makers, which are often found living independently. Our study system included one obligate slave-maker, Polyergus breviceps, two facultative slave-makers, Formica puberula and F. gynocrates, and two hosts, F. occulta and F. sp. cf. argentea. We observed all raids conducted during two raiding seasons by seven P. breviceps colonies, two F. puberula colonies, and two F. gynocrates colonies. We report on raiding frequency, average raid distances, and then compare the probability of being raided multiple times in a single raiding season for the two host species. We also report on the spatial distribution of slave raids, which suggests that slave-makers avoid raiding in areas used by other slave-maker colonies. This is the first report of raiding activity for P. breviceps in this location, and the first report of raiding activity of any kind for F. puberula and F. gynocrates.     

Intraspecific nestmate recognition in two parabiotic ant species: acquired recognition cues and low inter-colony discrimination

Parabiotic ants—ants that share their nest with another ant species—need to tolerate not only conspecific nestmates, but also nestmates of a foreign species. The parabiotic ants Camponotus rufifemur and Crematogaster modiglianii display high interspecific tolerance, which exceeds their respective partner colony and extends to alien colonies of the partner species. The tolerance appears to be related to unusual cuticular substances in both species. Both species possess hydrocarbons of unusually high chain lengths. In addition, Cr. modiglianii carries high quantities of hereto unknown compounds on its cuticle. These unusual features of the cuticular profiles may affect nestmate recognition within both respective species as well. In the present study, we therefore examined inter-colony discrimination within the two parabiotic species in relation to chemical differentiation. Cr. modiglianii was highly aggressive against workers from alien conspecific colonies in experimental confrontations. In spite of high inter-colony variation in the unknown compounds, however, Cr. modiglianii failed to differentiate between intracolonial and allocolonial unknown compounds. Instead, the cuticular hydrocarbons functioned as recognition cues despite low variation across colonies. Moreover, inter-colony aggression within Cr. modiglianii was significantly influenced by the presence of two methylbranched alkenes acquired from its Ca. rufifemur partner. Ca. rufifemur occurs in two varieties (‘red’ and ‘black’) with almost no overlap in their cuticular hydrocarbons. Workers of this species showed low aggression against conspecifics from foreign colonies of the same variety, but attacked workers from the respective other variety. The low inter-colony discrimination within a variety may be related to low chemical differentiation between the colonies. Ca. rufifemur majors elicited significantly more inter-colony aggression than medium-sized workers. This may be explained by the density of recognition cues: majors carried significantly higher quantities of cuticular hydrocarbons per body surface.     

The Effect of Social Parasitism by Polyergus breviceps on the Nestmate Recognition System of Its Host,Formica altipetens

Highly social ants, bees and wasps employ sophisticated recognition systems to identify colony members and deny foreign individuals access to their nest. For ants, cuticular hydrocarbons serve as the labels used to ascertain nest membership. Social parasites, however, are capable of breaking the recognition code so that they can thrive unopposed within the colonies of their hosts. Here we examine the influence of the socially parasitic slave-making ant, Polyergus breviceps on the nestmate recognition system of its slaves, Formica altipetens. We compared the chemical, genetic, and behavioral characteristics of colonies of enslaved and free-living F. altipetens. We found that enslaved Formica colonies were more genetically and chemically diverse than their free-living counterparts. These differences are likely caused by the hallmark of slave-making ant ecology: seasonal raids in which pupa are stolen from several adjacent host colonies. The different social environments of enslaved and free-living Formica appear to affect their recognition behaviors: enslaved Formica workers were less aggressive towards non-nestmates than were free-living Formica. Our findings indicate that parasitism by P. breviceps dramatically alters both the chemical and genetic context in which their kidnapped hosts develop, leading to changes in how they recognize nestmates.