Host Colonies Research Articles

Butterflies that trick ants with sound

Larvae of parasitic Maculinea butterflies use acoustic mimicry to induce host ants to adopt and care for them.

Alkaloid venom weaponry of three Megalomyrmex thief ants and the behavioral response of Cyphomyrmex costatus host ants.

Social parasites exploit other societies by invading and stealing resources. Some enter protected nests using offensive chemical weaponry made from alkaloid-based venom. We characterized the venoms of three Megalomyrmex thief ant species (M. mondabora, M. mondaboroides, and M. silvestrii) that parasitize the fungus-growing ants, and developed an ethogram to describe host ant reactions to raiding M. mondaboroides and M. silvestrii parasites. We compared piperidine, pyrrolidine, and pyrolizidine venom alkaloid structures with synthetic samples from previous studies, and describe the novel stereochemistry of trans 2-hexyl-5-[8-oxononyl]-pyrrolidine (3) from M. mondabora. We showed that workers of Cyphomyrmex costatus, the host of M. mondaboroides and M. silvestrii, react to a sting by Megalomyrmex parasites mainly with submissive behavior, playing dead or retreating. Host submission also followed brief antennal contact. The behavior of C. costatus ants observed in this study was similar to that of Cyphomyrmex cornutus, host of M. mondabora, suggesting that the alkaloidal venoms with pyrrolidines from M. mondabora, piperidines from M. mondaboroides, and pyrolizidines from M. silvestrii may function similarly as appeasement and repellent allomones against host ants, despite their different chemical structure. With the use of these chemical weapons, the Megalomyrmex thief ants are met with little host resistance and easily exploit host colony resources.

Fungal disease dynamics in insect societies: optimal killing rates and the ambivalent effect of high social interaction rates.

Entomopathogenic fungi are potent biocontrol agents that are widely used against insect pests, many of which are social insects. Nevertheless, theoretical investigations of their particular life history are scarce. We develop a model that takes into account the main distinguishing features between traditionally studied diseases and obligate killing pathogens, like the (biocontrol-relevant) insect-pathogenic fungi Metarhizium and Beauveria. First, obligate killing entomopathogenic fungi produce new infectious particles (conidiospores) only after host death and not yet on the living host. Second, the killing rates of entomopathogenic fungi depend strongly on the initial exposure dosage, thus we explicitly consider the pathogen load of individual hosts. Further, we make the model applicable not only to solitary host species, but also to group living species by incorporating social interactions between hosts, like the collective disease defences of insect societies. Our results identify the optimal killing rate for the pathogen that minimises its invasion threshold. Furthermore, we find that the rate of contact between hosts has an ambivalent effect: dense interaction networks between individuals are considered to facilitate disease outbreaks because of increased pathogen transmission. In social insects, this is compensated by their collective disease defences, i.e., social immunity. For the type of pathogens considered here, we show that even without social immunity, high contact rates between live individuals dilute the pathogen in the host colony and hence can reduce individual pathogen loads below disease-causing levels.

Evidence for colony-specific differences in chemical mimicry in the parasitic mite Varroa destructor

In social insects, the integrity of a colony is maintained by recognising and removing intruders. Nest-mates use chemical cues on the cuticle of the individual they encounter to determine whether or not it is part of the colony. Parasites have evolved to take advantage of this recognition system by mimicking these chemical cues to gain entry into the colony and therefore, avoid being attacked by the host during their stay. The ectoparasitic mite Varroa destructor uses chemical camouflage to access and remain undetected inside colonies of its honey bee host, Apis mellifera. It remains, however, to be tested whether the mite also mirrors colony-specific cues to retain its camouflage when switching host colonies. Here, we show that the mite’s chemical mimicry is colony-specific and that these colony-specific differences were based on differences in the n-alkane and alkene part of the mite’s chemical profile, even though overall chemical mimicry was imperfect.

Evidence for passive chemical camouflage in the parasitic mite Varroa destructor.

Social insect colonies provide a stable and safe environment for their members. Despite colonies being heavily guarded, parasites have evolved numerous strategies to invade and inhabit these hostile places. Two such strategies are (true) chemical mimicry via biosynthesis of host odor, and chemical camouflage, in which compounds are acquired from the host. The ectoparasitic mite Varroa destructor feeds on hemolymph of its honey bee host, Apis mellifera. The mite's odor closely resembles that of its host, which allows V. destructor to remain undetected as it lives on the adult host during its phoretic phase and while reproducing on the honeybee brood. During the mite life cycle, it switches between host adults and brood, which requires it to adjust its profile to mimic the very different odors of honey bee brood and adults. In a series of transfer experiments, using bee adults and pupae, we tested whether V. destructor changes its profile by synthesizing compounds or by using chemical camouflage. We show that V. destructor required direct access to host cuticle to mimic its odor, and that it was unable to synthesize host-specific compounds itself. The mite was able to mimic host odor, even when dead, indicating a passive physico-chemical mechanism of the parasite cuticle. The chemical profile of V. destructor was adjusted within 3 to 9h after switching hosts, demonstrating that passive camouflage is a highly efficient, fast and flexible way for the mite to adapt to a new host profile when moving between different host life stages or colonies.

Differentiating Parasitism and Other Interactions in Fossilized Colonial Organisms.

Colonial species occur in a wide range of aquatic invertebrates, some having excellent fossil records, notably corals, bryozoans and graptolite hemichordates. In contrast to unitary animals, colonial animals grow by adding repetitive modules known as zooids. The ability of colonies to endure partial mortality and the typically plastic growth of benthic colonial species facilitates the formation of macrosymbiotic associations, some of which may be parasitic. However, as with unitary fossils, it is notoriously difficult to identify whether the symbioses are parasitisms (+/-) or mutualisms (+/+). Intergrowths between host colonies of stromatoporoid sponges, corals or bryozoans, and skeletal or soft-bodied symbionts are particularly common in Ordovician-Devonian shallow-water deposits. Soft-bodied symbionts in such intergrowths are represented by moulds in the host skeletons, a process of preservation termed bioclaustration. As yet, however, there is a lack of convincing data showing that any of these symbionts were parasites. By comparison with modern analogues, some fossil galls provide more convincing examples of parasitism, and the destructive effects of borings into the skeletons of benthic colonies also argue in favour of parasitism. Pelagic graptoloid hemichordates from the Early Palaeozoic occasionally contain cysts or tubes that have been attributed to parasites on the grounds that they would have adversely affected the hydrodynamics of the floating colonies. Future studies should test for parasitism by comparing the sizes of colonies hosting symbionts with those lacking symbionts.

Size variation in eggs laid by normal-sized and miniature queens of Plebeia remota (Holmberg) (Hymenoptera: Apidae: Meliponini)

Miniature stingless bee queens have been studied concerning frequency distribution, production and egg laying performance. This study aimed to investigate size variation in eggs laid by Plebeia remota (Holmberg) queens and whether it is due to differences in queen size or colony conditions. A sample of 10 queens (8 of typical size and 2 miniature) was measured morphometrically (head width, interorbital distance, and intertegular distance) as well the eggs they laid (length, width and volume). Initially, eggs were analyzed when laid by queens in their own colonies. Significant differences were found for length, width and volume of eggs considering the total group of queens or both queen morphotypes. However, no significant correlations were found between queen size and egg size. Afterwards, two experiments were performed to evaluate the influence of colony conditions on egg size. Firstly, we shifted the queens from their original colonies (i.e., a typical queen was placed into a miniature queen colony, and vice-versa). Secondly, they were put into another colony (both types of queens, one each time, were placed on a third colony, a ‘host colony’). In all situations, both queen morphotypes laid eggs of similar or different sizes than before, often with significant differences. The results indicate that variation in egg size is due to conditions imposed to queens in the colony (e.g. queen feeding status, number of cells available to be oviposited), and not due to variation in queen body size.

Facial markings in the social cuckoo wasp Polistes sulcifer: No support for the visual deception and the assessment hypotheses

Insect social parasites have to conquer a host colony by overcoming its defensive barriers. In addition to increased fighting abilities, many social parasites evolved sophisticated sensory deception mechanisms to elude host colonies defenses by exploiting host communication channels. Recently, it has been shown that the conspicuous facial markings of a paper wasp social parasite, Polistes sulcifer, decrease the aggressiveness of host foundresses. Two main hypotheses stand as explanations of this phenomenon: visual sensory deception (i.e. the black patterning reduces host aggression by exploiting the host visual communication system) and visual quality assessment (i.e. facial markings reduce aggressiveness as they signal the increased fighting ability of parasites). Through behavioral assays and morphological measurements we tested three predictions resulting from these hypotheses and found no support either for the visual sensory deception or for the quality assessment to explain the reduction in host aggressiveness towards the parasite. Our results suggest that other discrimination processes may explain the observed phenomenon.

Mimicry and eavesdropping enable a new form of social parasitism in ants.

Social parasitism is defined by the exploitation of the social mechanisms of one society by another whole society. Here, we use quantitative ecological data and experiments to identify the components of a new form of social parasitism by the recently discovered "mirror turtle ant," Cephalotes specularis. We show that C. specularis workers visually mimic and actively avoid contact with foragers of the hyperaggressive host ant Crematogaster ampla, allowing them to move freely in the extensive and otherwise defended foraging networks of host colonies. Workers from parasite colonies have immediate access to these networks by nesting exclusively within host territories, and 89% of all potential host territories were parasitized. Inside the network, parasite workers eavesdrop on the host's trail pheromones to locate and exploit food resources that are defended by the host to the exclusion of all other ants. Experiments demonstrated the unprecedented capacity of the parasite for superior foraging performance on its host's pheromone trails than on trails of its own. Considered together, the apparent Batesian-Wallacian mimicry, pheromone-based interceptive eavesdropping, kleptoparasitism, and xenobiotic nesting ecology displayed by C. specularis within the territory and foraging network of a host ant represents a novel adaptive syndrome for social exploitation.

Growth dynamics of the threatened Caribbean staghorn coral Acropora cervicornis: influence of host genotype, symbiont identity, colony size, and environmental setting.

BackgroundThe drastic decline in the abundance of Caribbean acroporid corals (Acropora cervicornis, A. palmata) has prompted the listing of this genus as threatened as well as the development of a regional propagation and restoration program. Using in situ underwater nurseries, we documented the influence of coral genotype and symbiont identity, colony size, and propagation method on the growth and branching patterns of staghorn corals in Florida and the Dominican Republic.Methodology/Principal FindingsIndividual tracking of> 1700 nursery-grown staghorn fragments and colonies from 37 distinct genotypes (identified using microsatellites) in Florida and the Dominican Republic revealed a significant positive relationship between size and growth, but a decreasing rate of productivity with increasing size. Pruning vigor (enhanced growth after fragmentation) was documented even in colonies that lost 95% of their coral tissue/skeleton, indicating that high productivity can be maintained within nurseries by sequentially fragmenting corals. A significant effect of coral genotype was documented for corals grown in a common-garden setting, with fast-growing genotypes growing up to an order of magnitude faster than slow-growing genotypes. Algal-symbiont identity established using qPCR techniques showed that clade A (likely Symbiodinium A3) was the dominant symbiont type for all coral genotypes, except for one coral genotype in the DR and two in Florida that were dominated by clade C, with A- and C-dominated genotypes having similar growth rates.Conclusion/SignificanceThe threatened Caribbean staghorn coral is capable of extremely fast growth, with annual productivity rates exceeding 5 cm of new coral produced for every cm of existing coral. This species benefits from high fragment survivorship coupled by the pruning vigor experienced by the parent colonies after fragmentation. These life-history characteristics make A. cervicornis a successful candidate nursery species and provide optimism for the potential role that active propagation can play in the recovery of this keystone species.

Collective defence portfolios of ant hosts shift with social parasite pressure.

Host defences become increasingly costly as parasites breach successive lines of defence. Because selection favours hosts that successfully resist parasitism at the lowest possible cost, escalating coevolutionary arms races are likely to drive host defence portfolios towards ever more expensive strategies. We investigated the interplay between host defence portfolios and social parasite pressure by comparing 17 populations of two Temnothorax ant species. When successful, collective aggression not only prevents parasitation but also spares host colonies the cost of searching for and moving to a new nest site. However, once parasites breach the host's nest defence, host colonies should resort to flight as the more beneficial resistance strategy. We show that under low parasite pressure, host colonies more likely responded to an intruding Protomognathus americanus slavemaker with collective aggression, which prevented the slavemaker from escaping and potentially recruiting nest-mates. However, as parasite pressure increased, ant colonies of both host species became more likely to flee rather than to fight. We conclude that host defence portfolios shift consistently with social parasite pressure, which is in accordance with the degeneration of frontline defences and the evolution of subsequent anti-parasite strategies often invoked in hosts of brood parasites.

Evidence that microgynes of Myrmica rubra ants are social parasites that attack old host colonies.

Ant microgynes are miniaturized queen forms found together with normal queens (macrogynes) in species occurring across the ant phylogeny. Their role is not yet fully understood: in some cases, they seem to be nonparasitic alternative reproductive morphs, in others incipient social parasites, and thus potential models for studying the evolution of social parasitism. Whether they are regarded as parasitic or not has traditionally been based on genetic differentiation from syntopic macrogynes and/or the queen/worker ratio of their offspring rather than measuring fitness traits. We confirmed previously reported genetic differentiation between microgynes and macrogynes of Myrmica rubra in a population studied for the first time. Further, we measured virulence and infectivity of M.rubra microgynes in a controlled laboratory experiment. Nests headed only by macrogynes (controls), only by microgynes, and naturally and artificially mixed nests were kept under identical conditions. We found reduction in worker numbers of both naturally and artificially mixed macrogyne/microgyne nests compared with controls, and strong reduction but also surprising variation in fitness of nests headed only by microgynes. Microgyne nests produced workers, males and microgynes. Microgynes did not themselves reproduce in artificially mixed nests, but reproduced most in naturally mixed nests that had lost their macrogyne queen. This, together with higher mortality of field-collected macrogyne queens from naturally infested colonies and greater estimated relative age of macrogyne queens in naturally infected nests, suggests that they preferentially exploit older host colonies. We conclude that M.rubra microgynes are intraspecific social parasites specialized on exploiting old host colonies.

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.

Nest relocation in the slavemaking ants Formica subintegra and Formica pergandei: a response to host nest availability that increases raiding success

Social insects typically occupy spatially fixed nests which may thus constrain their mobility. Nevertheless, colony movements are a frequent component of the life cycle of many social insects, particularly ants. Nest relocation in ants may be driven by a variety of factors, including nest deterioration, seasonality, disturbances, changes in microclimate, and local depletion of resources. The colony movements of slavemaking ants have been noted anecdotally, and in recent studies such relocations were primarily attributed to nest deterioration or shifts to overwintering locations. In this study we explore nest relocations in large colonies of formicine slavemakers which occupy stable and persistent earthen nest mounds. We investigate the hypothesis that colony relocations of these slavemakers are best explained by efforts to improve raiding success by seeking areas of higher host availability. Five summers of monitoring the raiding behavior of 11–14 colonies of the slavemakers Formica subintegra and Formica pergandei revealed relatively frequent nest relocations: of 14 colonies that have been tracked for at least three of 5 years, all but one moved at least once by invading existing host nests. Movements tended to occur in the middle of the raiding season and were typically followed by continued raiding of nearby host colonies. Spatial patterns of movements suggest that their purpose is to gain access to more host colonies to raid: the distance moved is typically farther than the mean raiding distance before the move, which may indicate an effort to escape their local neighborhood. Furthermore, the mean distance of raids after relocation is shorter than the distance before relocation. For many slavemaking ant colonies, particularly those on the verge of relocating, raiding distance increased as the raiding season progressed. In addition, movements tended to be toward areas of higher local host density. Nest relocation is likely an important component of the ecology of slavemaking ants that contributes to the dynamic nature of their interaction with the host ant population.

Arboreal ant colonies as 'hot-points' of cryptic diversity for myrmecophiles: the weaver ant Camponotus sp. aff. textor and its interaction network with its associates.

IntroductionSystematic surveys of macrofaunal diversity within ant colonies are lacking, particularly for ants nesting in microhabitats that are difficult to sample. Species associated with ants are generally small and rarely collected organisms, which makes them more likely to be unnoticed. We assumed that this tendency is greater for arthropod communities in microhabitats with low accessibility, such as those found in the nests of arboreal ants that may constitute a source of cryptic biodiversity.Materials and MethodsWe investigated the invertebrate diversity associated with an undescribed, but already threatened, Neotropical Camponotus weaver ant. As most of the common sampling methods used in studies of ant diversity are not suited for evaluating myrmecophile diversity within ant nests, we evaluated the macrofauna within ant nests through exhaustive colony sampling of three nests and examination of more than 80,000 individuals.ResultsWe identified invertebrates from three classes belonging to 18 taxa, some of which were new to science, and recorded the first instance of the co-occurrence of two brood parasitoid wasp families attacking the same ant host colony. This diversity of ant associates corresponded to a highly complex interaction network. Agonistic interactions prevailed, but the prevalence of myrmecophiles was remarkably low.ConclusionsOur data support the hypothesis of the evolution of low virulence in a variety of symbionts associated with large insect societies. Because most myrmecophiles found in this work are rare, strictly specific, and exhibit highly specialized biology, the risk of extinction for these hitherto unknown invertebrates and their natural enemies is high. The cryptic, far unappreciated diversity within arboreal ant nests in areas at high risk of habitat loss qualifies these nests as ‘hot-points’ of biodiversity that urgently require special attention as a component of conservation and management programs.

Cryptic diversity hides host and habitat specialization in a gorgonian-algal symbiosis.

Shallow water anthozoans, the major builders of modern coral reefs, enhance their metabolic and calcification rates with algal symbionts. Controversy exists over whether these anthozoan-algae associations are flexible over the lifetimes of individual hosts, promoting acclimative plasticity, or are closely linked, such that hosts and symbionts co-evolve across generations. Given the diversity of algal symbionts and the morphological plasticity of many host species, cryptic variation within either partner could potentially confound studies of anthozoan-algal associations. Here, we used ribosomal, organelle and nuclear sequences, along with microsatellite variation, to study the relationship between lineages of a common Caribbean gorgonian and its algal symbionts. The gorgonian Eunicea flexuosa is a broadcast spawner, composed of two recently diverged, genetically distinct lineages largely segregated by depth. We sampled colonies of the two lineages across depth gradients at three Caribbean locations. We find that each host lineage is associated with a unique Symbiodinium B1/184 phylotype. This relationship between host and symbiont is maintained when host colonies are reciprocally transplanted, although cases of within phylotype switching were also observed. Even when the phylotypes of both partners are present at intermediate depths, the specificity between host and symbiont lineages remained absolute. Unrecognized cryptic diversity may mask host-symbiont specificity and change the inference of evolutionary processes in mutualistic associations. Symbiotic specificity thus likely contributes to the ecological divergence of the two partners, generating species diversity within coral reefs.

Ecologically differentiated stress-tolerant endosymbionts in the dinoflagellate genus Symbiodinium (Dinophyceae) Clade D are different species

:We used an integrative genetics approach using sequences of (1) nuclear ribosomal rDNA (internal transcribed spacers and partial large subunit rDNA), (2) single-copy microsatellite nuclear DNA, (3) chloroplast-encoded 23S rDNA, (4) mitochondrial cytochrome b, and (5) repeat variation at eight microsatellite markers, to test the hypothesis that the stress-tolerant, ‘morphologically cryptic’ Clade D Symbiodinium (Dinophyceae) was composed of more than one species. Concordant phylogenetic and population genetic evidence clearly differentiate separately evolving, reproductively isolated lineages. We describe Symbiodinium boreum sp. nov. and S. eurythalpos sp. nov., two symbionts known to occur in colonies of the zebra coral, Oulastrea crispata (Scleractinia), which lives in turbid, marginal habitats extending from equatorial Southeast Asia to the main islands of Japan in the temperate northwest Pacific Ocean. Symbiodinium boreum was associated with O. crispata in temperate latitudes and S. eurythalpos was common to colonies in the tropics. The geographical ranges of both symbiont species overlapped in the subtropics where they sometimes co-occurred in the same host colony. Symbiodinium trenchii sp. nov. is also described. As a host-generalist symbiont, it often occurs in symbiosis with various species of Scleractinia possessing open (horizontal) modes of symbiont acquisition and is common to reef coral communities thriving in warm turbid reef habitats in the western Pacific Ocean, Indian Ocean, Arabian/Persian Gulf, Red Sea and western Atlantic (Caribbean). As is typical for dinoflagellates, S. boreum and S. eurythalpos were haploid, but microsatellite loci from field-collected and cultured S. trenchii often possessed two alleles, implying that a genome-wide duplication occurred during the evolution of this species. The recognition that Clade D Symbiodinium contains species exhibiting marked differences in host specificity and geographical distribution will yield greater scientific clarity about how stress-tolerant symbionts function in the ecological response of coral–dinoflagellate symbioses to global climate change.

Forewarned is forearmed: aggression and information use determine fitness costs of slave raids

Many animals use reliable indicators of upcoming events such as antagonistic interactions to prepare themselves. In group-living animals, not only the cue perceiving individuals are involved in mobilization, but the entire group can use this information. In this study, we analyze whether social insects, which perceive reliable information on an upcoming social parasite attack, can use this knowledge to better defend their colony. We focus on the interaction between the ant Temnothorax longispinosus and the slave-making ant Protomognathus americanus, which conducts destructive raids on host colonies to steal their brood. As a behavioral defense, host colonies show aggression, which has a constitutive and inducible component: earlier studies demonstrated both behavioral consistency and an increase in aggression after slavemaker contact. Here, we analyze the fitness benefits of aggression in the context of slave raids. Aggression only facilitated host colony defense if the hosts were informed about a pending slave raid: slavemaker scouts were not only less likely to enter forewarned host colonies, but more aggressive colonies who previously encountered a slavemaker saved a higher fraction of their brood. We thus demonstrate that the fitness costs of raids depend on an interaction between the collective defense abilities and reliable information on impending dangers.

Body condition of the coral-dwelling fish Dascyllus aruanus (Linnaeus 1758) following host colony bleaching

Coral bleaching and degradation often results in the depletion of abundance of many reef fishes. However, the effects of coral degradation on coral habitat dependent fishes are poorly understood. Hence, in this study we examine the sublethal effects of coral bleaching on the physiological condition of Dascyllus aruanus, an obligate coral-dwelling damselfish. The results of this study showed that fish associated with bleached coral habitat showed similar levels of hepatocyte vacuolation compared to individuals associated with healthy colonies.

The evolution of multiqueen breeding in eusocial lineages with permanent physically differentiated castes

The hypothesis that obligate eusociality always evolved from ancestral states of strict lifetime monogamy implies that (1) facultatively eusocial lineages had to abandon multifemale breeding to achieve permanent morphologically differentiated castes, and (2) lineages of obligatorily eusocial insects had to independently re-evolve multifemale breeding when that served the inclusive fitness interests of nursing workers. Multiqueen nesting (eusocial polygyny) is known to be common across the ants, but rare in the corbiculate (eusocial) bees, the vespine wasps and the higher termites, but we show that this difference is mostly due to cases of obligate polygyny being restricted to the ants. This pattern is remarkably similar to the distribution of inquiline social parasites that use stealth rather than aggression to invade host colonies, which also repeatedly evolved in ants only. We explore the lineage-specific selection forces that have allowed or constrained de novo evolution of stable eusocial polygyny in Hamiltonian inclusive fitness terms. We argue that perennial life histories, male survival as stored sperm rather than as lifetime mates, and sib competition are possibly sufficient to explain the general prevalence of secondary polygyny across the obligatorily eusocial insects. We infer that obligate polygyny compromises eusocial ‘soma’ and ‘germ-line’ segregation in ways known to decrease developmental stability in metazoans, and we briefly evaluate the selection forces that reduce queen life span in highly, but probably not facultatively, polygynous species. We conclude that secondary polygyny in its obligate (ant) form resembles cooperative breeding with multiple ‘tragedy of the commons’ aspects, but in a peculiar manner because breeding females are selected to exploit the services of unmated workers rather than each other’s. This breeding system has likely been maintained in ants because it allows modular extensions of colonies in directly adjacent habitat of similar quality without the re-emergence of sexual conflicts or unproductive local competition with kin.