Formicitylenchus oregonensis n. g., n. sp. (Allantonematidae: Nematoda), the first tylenchid parasite of ants,with a review of nematodes described from ants

The first tylenchid parasite of ants, Formicitylenchus oregonensis n. g., n. sp., is described from a queen carpenter ant Camponotus vicinus Mayr in Western Oregon, USA. The new genus is characterised by the excretory pore anterior to the nerve-ring and rounded tails in the free-living adults, a stylet bearing basal thickenings in the free-living female, a smaller stylet lacking basal thickenings in the male and a short, crenulate leptoderan bursa. The mature parasitic female is light yellow and ovoviviparous. F. oregonensis n. sp. is closely related to members of Metaparasitylenchus Wachek, 1955, with species parasitising beetles living under bark or in rotten wood, a habitat similar to that of carpenter ants. However, males of Metaparasitylenchus are characterised by a fairly long tail with a broad peloderan bursa. It is suggested that this case of tylenchid parasitism in ants is an example of environmental host selection. A review of the described nematode parasites of ants is presented.     

A newly-discovered mode of colony founding among fire ants

Summary Queen ants start new colonies either unassisted by workers (independent founding), assisted by workers from their natal nest (dependent founding), or assisted by the workers of other species (dependent, socially parasitic). The monogyne form of the fire ant,Solenopsis invicta, founds independently in summer, but in the fall it also produces a few sexuals some of which overwinter, then fly and mate in early spring. These overwintered queens lack the nutritional reserves and behaviors for independent colony founding. Rather, they seek out unrelated, mature, orphaned colonies, enter them and exploit the worker force to found their own colony through intraspecific social parasitism. Success in entering orphaned colonies is higher when these lack overwintered female alates of their own. When such alates are present, orphaning causes some to dealate and become uninseminated replacement queens, usually preventing entry of unrelated, inseminated replacement queens. Such colonies produce large, all-male broods. Successful entry of a parasitic queen robs the host colony of this last chance at reproductive success. Only overwintered sexuals take part in this mode of founding.     

Fitness consequences of nest infiltration by the mutualist‐exploiter Megalomyrmex adamsae

1. Fungus‐growing ants are obligate mutualists. Their nutrient‐rich fungus garden provides a valuable food store that sustains the ant hosts, but can also attract social parasites. 2. The ‘guest ant' Megalomyrmex adamsae Longino parasitises the fungus‐growing Trachymyrmex zeteki Weber queen just after nest founding. The parasitic queen infiltrates the incipient nest, builds a cavity in the fungal garden, and lays eggs that develop into workers and reproductive males and females. 3. This study compared young parasitised and non‐parasitised laboratory colonies by measuring garden growth and biomass, and the number of host workers and reproductives. Host queen survival and parasite colony growth were also monitored. 4. Parasitised Trachymyrmex colonies had reduced host worker and alate numbers, as well as lower garden biomass, compared with non‐parasitised control colonies, confirming that M. adamsae is a xenobiotic social parasite. Host queen survival was not significantly different between parasitised and control colonies. 5. This is the first study that experimentally infects host colonies with a xenobiotic social parasite to measure fitness cost to the host. The natural history of M. adamsae and the fungus‐growing ant mutualism are evaluated in the context of three general predictions of (Bronstein, Ecology Letters, 4 , 277–287, 2001a) regarding the cost of mutualism exploiters.     

Interactional behaviors of the parasitic beetle Paussus favieri with its ant host Pheidole pallidula: the mimetic role of the acoustical signals

The social parasitic beetle Puussus favieri(Coleoptera,Carabidae,Paussini)performs different types of stridulations,which sclectively mimic those emitted by dif-ferent ant castes of its host Pheidole pallidula(Hymenoptera,Formicidae,Myrmicinae).However,the significance of this acoustical mimicry for the success of the parasitic strat-egy and the behaviors elicited in the host ants by stridulations was unknown.We reared Paussus favieri in Pheidole pallidula colonies and filmed their interacting behaviors.We analyzed in slow motion the behavior of ants near a stridulating beetle.We analyzed sep-arately trains of pulse(Pa+Pb,produced by repeated rubbings)and single pulse(Pc,produced by a single rubbing)of stridulations,clearly recognizable from the shaking up and down of the beetle hind legs.and associated them with differcent ant responscs.The full repertoire of sounds produced by P:favieri elicited benevolent responses both in workers and soldiers.We found that different signals elicit different(sometimes multiplc)bchaviors in ants,with different frequency in the two ant castes.However,Pc(alone or in conjunction with other types of pulses)appears to be the type of acoustic signal mostly responsible for all recorded behaviors.These results indicate that the acoustic channel plays a pivotal role in the host-parasite interaction.Finding that a parasite uses the acoustical channel so intensively,and in such a complicated way to trigger ant bchaviors,indicates that acoustic signals may be more important in ant societies than commonly recognized.     

Sociality in a Malagasy allodapine bee, Macrogalea antanosy, and the impacts of the facultative social parasite, Macrogalea maizina

Social parasitism has been researched extensively in many taxa of social insects, including ants, wasps and bees. However, little research has been done on allodapine bees, a taxon that has numerous independent origins of social parasitism. This study looks at two species of Macrogalea from Madagascar, one of which was previously believed to be a social parasite. Macrogalea is an important genus to study as it is the sister clade to all other allodapine genera, and the species of Macrogalea in Madagascar diverged recently, meaning that the study of a social parasite in this genera would provide insights into the very early stages of social parasite evolution. Macrogalea maizina was determined to be facultatively parasitic based on the presence of many traits that are common to other allodapine social parasites. The host, Macrogalea antanosy, was found to be quasisocial, with most females within a colony being able to reproduce. This has unique consequences for a parasitic strategy, as any invading parasite has no need to remove a queen or suppress the reproduction of the other colony members, a strategy that has been commonly observed for facultative parasites in other taxa. Received 10 May 2005; revised 22 July 2005; accepted 24 August 2005.     

Performance of Myrmica ant colonies is correlated with the presence of social parasites

1. The performance of ant colonies depends on different factors such as nest site, colony structure or the presence of pathogens and social parasites. Myrmica ants host various types of social parasites, including the larvae of Maculinea butterflies and Microdonmyrmicae (Schönrogge) hoverfly. How these social parasites affect host colony performance is still unexplored. 2. It was examined how the presence of Maculinea teleius Bergsträsser, Maculinea alcon (Denis & Schiffermüller), and M. myrmicae larvae, representing different feeding and growth strategies inside host colonies, is associated with worker survival, the number of foragers, and colony productivity parameters such as growth and reproduction. 3. It was found that the presence of social parasites is negatively associated with total colony production and the production of ant larvae and gynes. Male production was lower only in nests infested by M. teleius, whereas the number of worker pupae was significantly higher in all types of infested colonies than in uninfested colonies. Laboratory observations indicated that nests infested by Maculinea larvae are characterised by a higher number of foragers compared to uninfested nests but we did not find differences in worker survival among nest types. 4. The observed pattern of social parasite influence on colony productivity can be explained by the feeding strategies of parasitic larvae. The most negative effect was found for M. teleius, which feeds on the largest host brood and eliminates a high number of sexual forms. The strong, adverse influence of all studied parasite species on gyne production may result in low queen production in Myrmica populations exposed to these social parasites.     

Queen developmental time and fitness consequences for queens of clonal social parasitic honeybees (A. m. capensis) and its host A. m. scutellata

Summary. The social parasitic honeybees of South Africa (Apis mellifera capensis) consist of a single clonal lineage, which has been selected for traits related to worker reproduction. Viable queens of this parasitic clonal lineage have never been observed. We tested if it is possible to rear queens from eggs of the social parasitic workers. In a competitive situation, using larvae of the parasitic clonal lineage and of the host, we tested the discriminatory ability of host colonies (A. m. scutellata) between parasitic and non-parasitic larvae. We found evidence for a reduced fitness of queens reared from the social parasite lineage, resulting from a longer developmental time. The results are discussed in the light of a fitness trade-off between queen and worker caste.Received 22 July 2004; revised 22 December 2004; accepted 5 January 2005.     

Cuckoos and parasitic ants: Interspecific brood parasitism as an evolutionary arms race

Each summer thousands of nesting birds feed cuckoo chicks that have killed the hosts' own young. Likewise, worker ants rear the brood of other ants that have killed the workers' queen or even induced the workers to kill their queen themselves. In both cases the hosts spend time and energy raising offspring that, to them, are of no genetic value. Such exploitation involves intricate parasitic adaptations for deceiving hosts. It should also provoke host defences. Brood and social parasites and their hosts therefore provide excellent opportunities for the study of evolutionary arms races.     

Absence of Nepotism in Worker–Queen Care in Polygynous Colonies of the Ant Ectatomma tuberculatum

The question of the occurrence of nepotism in insect societies is central to inclusive fitness theory. Here we investigated the existence of nepotism in the facultative polygynous ant Ectatomma tuberculatum because various characteristics of this species may have favored the evolution of nepotistic behavior toward queens. We thus studied worker–queen care toward their mother queen vs. an unrelated unfamiliar queen, to determine if workers cared preferentially for their mother. Although we tried to facilitate the expression of nepotistic behaviors, we did not detect significant nepotism confirming the general trend of an absence of nepotism in social insects. We discuss about the specific causes that can explain the absence of nepotism in E. tuberculatum regarding the particular social organization of this species and its ecological dominance in the mosaic of arboreal ants.     

Evolutionary transition to a semelparous life history in the socially parasitic ant Acromyrmex insinuator

The recently discovered social parasite Acromyrmex insinuator ( 25 ) exploits colonies of the leafcutter ant A. echinatior. We document that A. insinuator represents a rare early stage in the evolution of social parasitism, because a worker caste is still partially present and mating phenology has remained at least partially similar to that of the host. A. insinuator is tolerant of host queens, and sexual offspring produced in parasitized colonies can be either exclusively A. insinuator or a mix of A. insinuator and A. echinatior. The remarkably high abundance of A. insinuator in nests of the investigated Panamanian host population and the fact that A. insinuator colonies readily reproduce under laboratory conditions allowed us to test evolutionary predictions on reproductive life history evolution that are not possible in most other socially parasitic ants. We show that (1) A. insinuator has a semelparous ‘big bang’ reproductive life history which exploits host colonies without leaving reserves for survival; (2) social parasite sexuals are significantly smaller than A. echinatior host sexuals, but still large compared to host workers, confirming an evolutionary scenario of gradual size reduction and loss of the worker caste after transition towards a socially parasitic life history; (3) major changes in the life history of ants can evolve relatively quickly compared to adaptations in morphology, caste differentiation and mating phenology.     

Cryptic diversity and female host specificity in a parasitoid where the sexes utilize hosts from separate orders

Investigating complex parasitic life cycles is important for understanding the major fitness components that drive the evolution of host–parasite systems. The rare condition of heterotrophic heteronomy, in which the sexes utilize disparate host taxa, is a poorly understood complex parasitic lifestyle. One of only two known examples occurs in the Myrmecolacidae, an unusual family of the parasitoid order Strepsiptera (Insecta), in which males parasitize ants while females parasitize grasshoppers, crickets, and praying mantids. Here, we reconstruct the evolutionary pattern and timescale of host‐use in a set of morphologically cryptic myrmecolacid taxa currently identified as Caenocholax fenyesi. We find that (i) C. fenyesi contains at least ten cryptic lineages consistent with separate species; (ii) Fossil evidence suggests a very low molecular clock rate and an ancient origin for cryptic lineages; (iii) Diversity among Caenocholax species is partitioned by geography and host association of the female; and (iv) Switches in host usage are uncoupled between the sexes, with changes in female host preference accompanying diversification. This study represents the first phylogeographical analysis of any strepsipteran, and the first molecular examination of host‐use for a heterotrophic heteronomous taxon. Our results have implications for the understanding of evolution, host usage and estimated species richness in parasitic taxa.     

The genetic population structure of two socially parasitic ants: “the active slave-maker” Myrmoxenus ravouxi and the “degenerate slave-maker” M. kraussei

Slave-making ants exploit the societies of host ant species and are typically rare and patchily distributed. IUCN considers almost all slave-making ants as vulnerable, but solid data on their actual abundance are uncommon. Here we examine the genetic structure of populations of two species of the socially parasitic genus Myrmoxenus, which differ strongly in dispersal behavior and the occurrence of slave-raids. Microsatellite genotypes suggest strong differentiation even among neighboring populations of both species. F_ST-, G″_ST-, and D-values were considerably higher in the “degenerate slave-maker” M. kraussei from Northern Italy than in the active slavemaker M. ravouxi from Southern Germany. This matches observations that sexuals of M. kraussei mate in their natal nest and queens disperse on foot while sexuals of M. ravouxi engage in mating and dispersal flights. Allelic richness was surprisingly high in both species and did not suggest recent bottlenecks, indicating that populations are larger and less vulnerable than expected from the difficulties of locating nests. Despite of considerable inbreeding, only very few diploid males were detected, supporting the view that at least in M. kraussei sex is not determined by single locus complementary sex determination unlike most other social Hymenoptera. The mismatch between the genetic and social structure of M. ravouxi colonies indicates occasionally fusion of slave-maker colonies in the field, mutual raids, or queen replacement. Complementary analyses of the host species of the two social parasites, Temnothorax unifasciatus and T. recedens, revealed low levels of population differentiation and confirmed the colony structure with a single, singly-mated queen.     

Behavioral differences between two ant cricket species in Nansei Islands: host-specialist versus host-generalist

Ant crickets (Orthoptera, Myrmecophilidae) are typical ant guests that obtain nourishment from the ants in their nests. Some ant crickets are host-specific, whereas other species are host-generalists. We investigated the behavioral polarization between the specialist cricket Myrmecophilus albicinctus and generalist Myrmecophilus formosanus. In the field, M. albicinctus was found exclusively in nests of Anoplolepis gracilipes (185/185), whereas 62 M. formosanus were found in nests of 9 ant species from 3 subfamilies. Behavioral observations revealed that M. albicinctus could not survive in the absence of A. gracilipes and was killed when it was introduced into colonies of non-host ant species. In addition, M. albicinctus showed intimate behavior, such as trophallaxis, with its host. In contrast, M. formosanus swiftly avoided frequent attacks by host ants, independently took food, and survived well in the absence of ants. Overall, the specialist adapted its behavior and physiology to those of a specific ant host, whereas the generalist adopted versatile parasitic behaviors, such as quick movements. Our findings revealed interspecific polarization in the degree of host dependence and inquiline–host interaction, and they indicate that trade-offs occur between specialization to specific hosts and retention of generalization in order to exploit alternative hosts.     

Sex allocation in fungus‐growing ants: worker or queen control without symbiont‐induced female bias

The fungal cultivars of fungus‐growing ants are vertically transmitted by queens but not males. Selection would therefore favor cultivars that bias the ants’ sex ratio towards gynes, beyond the gyne bias that is optimal for workers and queens. We measured sex allocation in 190 colonies of six sympatric fungus‐growing ant species. As predicted from relatedness, female bias was greater in four singly mated Sericomyrmex and Trachymyrmex species than in two multiply mated Acromyrmex species. Colonies tended to raise mainly a single sex, which could be partly explained by variation in queen number, colony fecundity, and fungal garden volume for Acromyrmex and Sericomyrmex, but not for Trachymyrmex. Year of collection, worker number and mating frequency of Acromyrmex queens did not affect the colony sex ratios. We used a novel sensitivity analysis to compare the population sex allocation ratios with the theoretical queen and worker optima for a range of values of k, the correction factor for sex differences in metabolic rate and fat content. The results were consistent with either worker or queen control, but never with fungal control for any realistic value of k. We conclude that the fungal symbiont does not distort the ants’ sex ratio in these species.     

A heritable component in sex ratio and caste determination in a Cardiocondyla ant

Studies on sex ratios in social insects provide among the most compelling evidence for the importance of kin selection in social evolution. The elegant synthesis of Fisher's sex ratio principle and Hamilton's inclusive fitness theory predicts that colony-level sex ratios vary with the colonies' social and genetic structures. Numerous empirical studies in ants, bees, and wasps have corroborated these predictions. However, the evolutionary optimization of sex ratios requires genetic variation, but one fundamental determinant of sex ratios - the propensity of female larvae to develop into young queens or workers ("queen bias") - is thought to be largely controlled by the environment. Evidence for a genetic influence on sex ratio and queen bias is as yet restricted to a few taxa, in particular hybrids. Because of the very short lifetime of their queens, ants of the genus Cardiocondyla are ideal model systems for the study of complete lifetime reproductive success, queen bias, and sex ratios. We found that lifetime sex ratios of the ant Cardiocondyla kagutsuchi have a heritable component. In experimental single-queen colonies, 22 queens from a genetic lineage with a highly female-biased sex ratio produced significantly more female-biased offspring sex ratios than 16 queens from a lineage with a more male-biased sex ratio (median 91.5% vs. 58.5% female sexuals). Sex ratio variation resulted from different likelihood of female larvae developing into sexuals (median 50% vs. 22.6% female sexuals) even when uniformly nursed by workers from another colony. Consistent differences in lifetime sex ratios and queen bias among queens of C. kagutsuchi suggest that heritable, genetic or maternal effects strongly affect caste determination. Such variation might provide the basis for adaptive evolution of queen and worker strategies, though it momentarily constrains the power of workers and queens to optimize caste ratios.     

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.     

Myrmica ants host highly diverse parasitic communities: from social parasites to microbes

Myrmica ants have been model species for studies in a variety of disciplines, including insect physiology, chemical communication, ant social dynamics, ant population, community ecology, and ant interactions with other organisms. Species belonging to the genus Myrmica can be found in virtually every habitat within the temperate regions of the northern hemisphere and their biology and systematics have been thoroughly studied. These ants serve as hosts to highly diverse parasitic organisms from socially parasitic butterfly caterpillars to microbes, and many Myrmica species even evolved into parasitizing species of their own genus. These parasites have various impacts both on the individuals and on the social structure of their hosts, ranging from morphological malformations to reduction in colony fitness. A comprehensive review of the parasitic organisms supported by Myrmica and the effects of these organisms on individuals and on whole ant colonies has not yet been compiled. Here, we provide a review of the interactions of these organisms with Myrmica ants by discussing host and parasite functional, behavioral or physiological adaptations. In addition, for all “symbiont groups” of Myrmica ants described in this paper, we examine the present limitations of the knowledge at present of their impact on individuals and host colony fitness. In conclusion, we argue that Myrmica ants serve as remarkable resource for the evolution of a wide variety of associated organisms.     

Phylogeny of Lasius ants based on mitochondrial DNA and morphology, and the evolution of social parasitism in the Lasiini (Hymenoptera: Formicidae)

Phylogeny of ants of the tribe Lasiini (Lasius, Acanthomyops, Prenolepis, Euprenolepis, Paratrechina, Pseudolasius, and Myrmecocystus) was analysed using 81 morphological, ecological, and behavioural characters (for 41 species) and mitochondrial DNA sequences (COI, COII, tRNA-Leu; for 19 species). The free-living subgenus Lasius s. str. is paraphyletic with respect to the rest of genus; the traditional "genus" Acanthomyops should be considered a part of Lasius s. lat.; free-living subgenus Cautolasius is a member of the clade of socially parasitic Lasius ants (=Chtonolasius+Acanthomyops+Austrolasius+Dendrolasius). The tree topology is congruent with two alternative scenarios of origin of the temporary social parasitism: (i) a single origin of the parasitic strategy in a derived subclade of Lasius and a secondary loss of this trait in Cautolasius, (ii) a parallel origin of the social parasitism within the clade of hypogeic Lasius ants (in Chtonolasius, and in Acanthomyops+Dendrolasius+Austrolasius). Emery's rule in the strict sense does not apply to this group because most parasites exploit any ecologically available, even phylogenetically distant host species. The parasitic strategy in Lasius could have originated from the aggressive interactions between cofounding queens during pleometric colony founding and/or from the secondary queen adoption.     

Sympatric speciation and radiative evolution of socially parasitic ants - Heretic hypotheses and their factual background

According to current hypotheses the main types of social parasitism among ants, namely slavery, temporary parasitism, and inquilinism, arose from such features as predation on other ants, or territorial behavior, both presumed precursors of slavemaking, and polygyny, a presumed precursor of temporary parasitism and inquilinism. The latter is believed also to represent a final instar in several evolutionary pathways leading from slavery, temporary parasitism, and xenobiosis to this permanently parasitic, workerless condition. Speciation, the origin of parasitic species from their usually closely related host species, is suggested to occur due to temporary geographic isolation and subsequent transition of one of the newly formed daughter species to parasitism in the nests of the other. Evidence is presented suggesting that the main types of social parasitism originated independently of each other. 15 ant genera are parasitized exclusively by inquilines, Eve other genera exclusively by temporary parasites. Only four groups of non-parasitic ant species (Formica, Tet-ramorium, Leptothorax subgenera Leptothorax and Myrafant) have parasites of several types each. Within these roups, however, there is little evidence of evolutionary transitions from one type to another. The few exceptions, mainly workerless species of the genera Epimyrma and Chalepoxenus, represent parasites which clearly derive from slave-making congeners, but differ from ordinary inquilines in that they eliminate the host colony queens like their actively dulotic ancestors. The new hypothesis suggests that all forms of interspecific true social parasitism (excluding xenobiosis) orginated from a common “preparasitic” stage, a subpopulation of reproductives in polygynous colonies and species, with diverging sexual behavior (near-nest mating vs. swarming) and caste ratios (production of more sexuals vs. workers). Arguments for sympatric speciation are compiled. Various features of the ancestral, and then host species (colony sizes, population density and structure, transition from polygyny to monoyny, etc.), and of the “preparasite” (production of few, or no workers, etc.) may shape the developing parasite to become a slave-maker, inquiline, or temporary parasite. These features usually leave open only one, or in a few genera, several options. The different types of parasitism within one host species group thus may have developed in a radiative manner from the common, preparasitic stage, which explains that independent colony foundation is a common feature of all true social parasites among ants.