A new workerless inquiline in the Lower Attini (Hymenoptera: Formicidae), with a discussion of social parasitism in fungus‐growing ants

Ant inquilines are obligate social parasites, usually lacking a sterile worker caste, which are dependent on their hosts for survival and reproduction. Social parasites are rare among the fungus‐gardening ants (Myrmicinae: tribe Attini) and only four species are known until now, all being inquilines from the Higher Attini. We describe Mycocepurus castrator sp.n. , the first inquiline social parasite to be discovered in the Lower Attini. Our study of the parasite's behaviour and life history supports the conclusion drawn from external morphology: Mycocepurus castrator is an evolutionarily derived inquiline parasite of Mycocepurus goeldii. Inquilines are of great interest to evolutionary biology because it is debated if they originated via sympatric or allopatric speciation. We discuss the life history evolution, behaviour and morphology of socially parasitic, fungus‐growing ants.     

Evolution of social parasitism in ants: size of sexuals,sex ratio and mechanisms of caste determination

Social parasitism, one of the most intriguing phenomena in ants, has evolved to various levels, the most extreme form being parasites that have lost the worker caste and rely completely on the host''s worker force to raise their brood. A remarkable feature of workerless social parasites is the small size of sexuals. It has been suggested that reduced size evolved as a means to take advantage of the host''s caste-determination system, so that parasite larvae develop into sexuals with less food than is required to produce host workers. An important consequence of size reduction is that it might restrict the host workers'' ability to discriminate between the brood of the social parasite and their own brood and might protect parasite sexuals from elimination. We found that sexuals of the workerless inquiline ant Plagiolepis xene were significantly smaller than the sexuals of their host Plagiolepis pygmaea, but remarkably similar to the host workers. The size variance of parasite sexuals was much lower than that of their host; this result possibly suggests that there is very stabilizing selection acting on size of the parasite sexuals. Comparison of the primary (egg) and secondary (adult) sex ratios of the parasite and host showed that miniaturization of P. xene sexuals has been accompanied by their ability to develop into sexuals even when the host P. pygmaea actively prevents production of its own sexuals. These results suggest that the inquiline''s size and caste threshold have been reduced such that all individuals in a parasite brood will develop into sexuals. We also found that the adult sex ratio of P. xene was heavily female-biased. This bias probably stems from local mate competition that arises from sexuals mating within the nest. There was no significant difference between the proportion of haploid eggs and adult males produced; this observation indicates that a female-biased sex ratio is achieved by queens producing a higher proportion of diploid eggs rather than by a higher mortality of haploid males.     

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.     

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.     

Reproductive division of labour and thelytoky result in sympatric barriers to gene flow in honeybees (Apis mellifera L.)

Determining the extent and causes of barriers to gene flow is essential for understanding sympatric speciation, but the practical difficulties of quantifying reproductive isolation remain an obstacle to analysing this process. Social parasites are common in eusocial insects and tend to be close phylogenetic relatives of their hosts (= Emery's rule). Sympatric speciation caused by reproductive isolation between host and parasite is a possible evolutionary pathway. Socially parasitic workers of the Cape honeybee, Apis mellifera capensis, produce female clonal offspring parthenogenetically and invade colonies of the neighbouring subspecies A. m. scutellata. In the host colony, socially parasitic workers can become pseudoqueens, an intermediate caste with queenlike pheromone secretion. Here, we show that over an area of approximately 275.000 km2, all parasitic workers bear the genetic signature of a clone founded by a single ancestral worker genotype. Any gene flow from the host to the parasite is impossible because honeybee workers cannot mate. Gene flow from the parasite to the host is possible, as parasitic larvae can develop into queens. However, we show that despite sympatric coexistence for more than a decade, gene flow between host and social parasite (F(st) = 0.32) and hybridizations (0.71%) are rare, resulting in reproductive isolation. Our data suggest a new barrier to gene flow in sympatry, which is not based on assortative matings but on thelytoky and reproductive division of labour in eusocial insects, thereby suggesting a new potential pathway to Emery's rule.     

The evolution of social parasitism in <Emphasis Type="Italic">Acromyrmex</Emphasis> leaf-cutting ants: a test of Emery’s rule

Summary Emerys rule predicts that social parasites and their hosts share common ancestry and are therefore likely to be close relatives. Within the leaf-cutting ant genus Acromyrmex, two taxa of social parasites have been found, which are thought to occupy opposite grades of permanent social parasitism, based on their contrasting morphologies: Acromyrmex insinuator differs little in morphology from its free-living congeneric host species and produces a worker caste, and is thus thought to represent an early grade of social parasitism. At the other extreme, Pseudoatta spp. exhibit a very specialised morphology and lack a worker caste, both of which are characteristics of an evolutionarily derived grade of social parasitism. Here we present a molecular phylogeny using partial sequences of cytochrome oxidase I and II of about half of the known Acromyrmex species including two social parasites, their hosts and all congeneric species occurring sympatrically. We show that the two inquiline parasites represent two separate origins of social parasitism in the genus Acromyrmex. The early-grade social parasite A. insinuator is highly likely to be the sister species of its host Acromyrmex echinator, but the derived social parasite Pseudoatta sp. is not the sister species of its extant host Acromyrmex rugosus.Received 18 November 2002; revised 16 July 2003; accepted 24 July 2003.     

The adaptive significance of inquiline parasite workers

Social parasites exploit the socially managed resources of their host's society. Inquiline social parasites are dependent on their host throughout their life cycle, and so many of the traits inherited from their free-living ancestor are removed by natural selection. One trait that is commonly lost is the worker caste, the functions of which are adequately fulfilled by host workers. The few inquiline parasites that have retained a worker caste are thought to be at a transitional stage in the evolution of social parasitism, and their worker castes are considered vestigial and non-adaptive. However, this idea has not been tested. Furthermore, whether inquiline workers have an adaptive role outside the usual worker repertoire of foraging, brood care and colony maintenance has not been examined. In this paper, we present data that suggest that workers of the inquiline ant Acromyrmex insinuator play a vital role in ensuring the parasite's fitness. We show that the presence of these parasite workers has a positive effect on the production of parasite sexuals and a negative effect on the production of host sexuals. This suggests that inquiline workers play a vital role in suppressing host queen reproduction, thus promoting the rearing of parasite sexuals. To our knowledge, these are the first experiments on inquiline workers and the first to provide evidence that inquiline workers have an adaptive role.     

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.     

SELFISH LARVAE: DEVELOPMENT AND THE EVOLUTION OF PARASITIC BEHAVIOR IN THE HYMENOPTERA

Queens of hymenopteran social parasites manipulate the workers of other social species into raising their offspring. However, nonconspecific brood care may also allow the parasite larvae to control their own development to a greater extent than possible in nonparasitic species. An evolutionary consequence of this may be the loss of the parasite's worker caste if the larvae can increase their fitness by developing into sexuals rather than workers. We argue that this loss is particularly likely in species in which there is little inclusive fitness benefit in working. Retention of a worker caste correlates with characteristics that increase the fitness of working relative to becoming a sexual, such as worker-production of males, high intracolony relatedness, and seasonal environments where the hosts of potential parasite queens are not always available. Further evidence strongly suggests that when the worker caste is evolutionarily lost in perennial species like ants, it disappears rapidly and through a reduction in caste threshold and queen size, so that parasite larvae become queens with less food than required to produce host workers. This evolutionary process, however, appears to lower overall population fitness, resulting in workerless parasite species having small populations and being geographically restricted. Conversely, in annual species like bees and wasps, workerless social parasitism evolves with no size reduction in queens, which is consistent with an expected lower level of queen/offspring conflict.     

Social interactions between an inquiline ant, <Emphasis Type="Italic">Ectatomma parasiticum</Emphasis>, and its host, <Emphasis Type="Italic">Ectatomma tuberculatum</Emphasis> (Formicidae,Ectatomminae)

Inquilines, workerless social parasites, frequently show advanced adaptations to their parasitic life style that indicate a long co-evolutionary history with their host. Ectatomma parasiticum, the first inquiline described in the poneromorph group, usurps established colonies of E. tuberculatum and produces only sexuals. In laboratory colonies, parasites were specifically attacked by the host workers, showing a failure in their social integration. Social interactions were frequent between parasites and their hosts, especially antennation, interpreted as attempts to promote colonial odor transfer. Inquilines destroyed eggs laid by the other queens (67 out of 209 eggs laid), including conspecific parasites, which is unusual. Such partial integration into the host colony and potential parasite virulence argue for a recent evolution of social parasitism in E. tuberculatum.     

Wolbachia in leafcutter ants: a widespread symbiont that may induce male killing or incompatible matings

Wolbachia is a maternally inherited bacterium that manipulates host reproduction by inducing cytoplasmic incompatibility (CI), parthenogenesis or male killing (MK). Here, we report on a screening of seven leafcutter ant species of the genera Atta and Acromyrmex. Using Wolbachia‐specific polymerase chain reaction (PCR) primers we show that all species are infected, usually by double A + B strain infections. For Acromyrmex echinatior and A. octospinosus, a screening across all castes shows that gynes (prospective queens) have higher infection rates than workers and males. The low infection rate of workers suggests that workers lose their infection during development. This we interpret as adaptive, because a heritable symbiont does not benefit from being present in sterile workers. Both CI and MK could potentially account for the low infection rate of males. Formal theoretical models show greater support for the MK scenario in the free living species A. echinatior and A. octospinosus but indicate that Wolbachia in the social parasite A. insinuator may cause CI, supporting a scenario of sympatric speciation of the social parasite. We conclude that Wolbachia represents a previously unrecognized source of reproductive conflict in leafcutter ant colonies.     

Sociobiology of slave-making ants

Social parasitism is the coexistence in the same nest of two species of social insects, one of which is parasitically dependent on the other. Though parasitism in general is known to be of crucial importance in the evolution of host species, social parasites, though intriguing, are often considered as a phenomenon of marginal interest and are typically not taken into account in reviews on parasitism. Nevertheless, social parasites are rather common in social bees, wasps, and ants and therefore may offer unique model systems to study a number of fundamental problems in evolutionary biology. Here we review several aspects of the peculiar life history of slave-making ants, which is characterized by socially parasitic founding of colonies and the pillage of broods from neighboring host colonies during slave raids. In particular we focus on the evolution of slave-making habits (dulosis), communication mechanisms between slave makers and their hosts, sex-allocation ratios and reproductive conflict, and the effect of slave makers on host populations. Received: 2 February 2000 / Received in revised form: 21 December 2000 / Accepted: 8 January 2001     

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.     

The reproductive phenology of an Amazonian ant species reflects the seasonal availability of its nest sites

In saturated tropical ant assemblages, reproductive success depends on queens locating and competing for scarce nest sites. Little is known about how this process shapes the life histories of tropical ants. Here I investigate the relationship between nest site availability and an important life history trait, reproductive phenology, in the common Amazonian ant species Allomerus octoarticulatus. A. octoarticulatus is a plant-ant that nests in the hollow, swollen stem domatia on Cordia nodosa. I provide evidence that nest sites are limiting for A. octoarticulatus. Most queens produced by A. octoarticulatus colonies died before locating suitable host plants, and most queens that located hosts died before founding colonies, probably from intraspecific competition among queens for control of host plants. I further show that the reproductive phenology of A. octoarticulatus closely matches the seasonal availability of its nest sites, domatia-bearing C. nodosa saplings. Both the production and flight of A. octoarticulatus reproductives, and the number of C. nodosa saplings available for colonization by ants, peaked from March to May. There was correlative evidence that A. octoarticulatus colonies use temperature as a cue to synchronize their reproduction to the availability of C. nodosa saplings: both the production of reproductives by ant colonies and the number of C. nodosa saplings available for colonization were correlated with temperature, and not with rainfall. All of these results suggest that nest site limitation constrains the reproductive phenology of A. octoarticulatus.     

Nylanderia deceptrix sp. n., a new species of obligately socially parasitic formicine ant (Hymenoptera,Formicidae)

Obligately socially parasitic ants are social parasites that typically lack the sterile worker caste, and depend on the host species for survival and brood care. The genus Nylanderia has over 130 described species and subspecies, none of which, until this study, were known social parasites. Here we describe the first social parasite known in the genus, Nylanderia deceptrix. Aspects of the biology of the host species, Nylanderia parvula (Mayr 1870), and Nylanderia deceptrix are examined. The data from both the host and the parasite species are combined to better understand the host-parasite relationship.     

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.     

Correlates of reproductive success among field colonies of Bombus lucorum: the importance of growth and parasites

Abstract.

• 1 In natural populations, colonies of bumble bees vary in many important life history traits, such as colony size and age at maturity, or the number and sex of reproductives produced. We investigated how the presence of parasites in field populations of the bumble bee Bombus lucorum L. relates to variation in life history traits and reproductive performance. A total of thirty-six colonies was placed in accessible nest sites in the field and monitored at regular intervals throughout a season.
• 2 Among the life history correlates, early nest foundation was strongly associated with large maximum colony size, old age and large size at maturity, and this in turn with successful production of males and queens, as well as with the number of sexuals produced. Overall, reproductive success was highly skewed with only five colonies producing all the queens. Sixteen colonies failed to reproduce altogether.
• 3 The social parasite Psithyrus was abundant early in the Bombus colony cycle and preferentially invaded host nests with many first brood workers and thus disproportionately large size, i.e. those colonies that would otherwise be more likely to reproduce or produce (daughter) queens rather than males. To prevent nest loss, Psithyrus had to be removed soon after invasion. Therefore, the effects reported here can only be crude estimates.
• 4 Parasitoid conopid flies are likely to cause heavy worker mortality when sexuals are reared by the colonies. Their inferred effect was a reduction in biomass that could be invested in sexuals as well as a shift in the sex ratio at the population level resulting from failure to produce queens. We suggest to group the inferred correlates into ‘early events’ surrounding colony initiation and social parasitism, and ‘late events’ surrounding attained colony size in summer and parasitism by conopid flies. Our evidence thus provides a heuristic approach to understand the factors that affect reproductive success of Bombus colonies.

     

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.     

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.     

Cuticular profiles and mating preference in a slave-making ant

The remarkable ability of slave-making ants to integrate chemically in the colonies of their host species makes them useful model systems for investigating the role of cuticular hydrocarbons in chemical recognition. The purpose of our study was to examine the influence of the rearing host species on the cuticular hydrocarbon profile and on the mating behaviour of sexuals of the slave-making ant Chalepoxenus muellerianus. Sexuals from a population parasitizing exclusively the host species Temnothorax unifasciatus were reared in the laboratory either with their natural host or another potential host species, Temnothorax recedens. C. muellerianus males reared with T. unifasciatus investigated and mounted female sexuals reared with the same host significantly more often than female sexuals reared with T. recedens. Similarly, C. muellerianus males reared with T. unifasciatus discriminated against female sexuals from natural T. recedens colonies. Males experimentally or naturally reared with T. recedens did not clearly discriminate between female sexuals reared by the two host species and only rarely engaged in mating attempts with either type of female sexuals. Chemical analyses showed that host species affect the chemical profile of C. muellerianus sexuals and vice versa. Our findings indicate that cuticular hydrocarbons might be important in the mating success of this ant species. Received 21 June 2006; revised 20 February 2007; accepted 1 March 2007.