Unparasitized Colonies Research Articles

Extreme lifespan extension in tapeworm-infected ant workers.

Social insects are hosts of diverse parasites, but the influence of these parasites on phenotypic host traits is not yet well understood. Here, we tracked the survival of tapeworm-infected ant workers, their uninfected nest-mates and of ants from unparasitized colonies. Our multi-year study on the ant Temnothorax nylanderi, the intermediate host of the tapeworm Anomotaenia brevis, revealed a prolonged lifespan of infected workers compared with their uninfected peers. Intriguingly, their survival over 3 years did not differ from those of (uninfected) queens, whose lifespan can reach two decades. By contrast, uninfected workers from parasitized colonies suffered from increased mortality compared with uninfected workers from unparasitized colonies. Infected workers exhibited a metabolic rate and lipid content similar to young workers in this species, and they received more social care than uninfected workers and queens in their colonies. This increased attention could be mediated by their deviant chemical profile, which we determined to elicit more interest from uninfected nest-mates in a separate experiment. In conclusion, our study demonstrates an extreme lifespan extension in a social host following tapeworm infection, which appears to enable host workers to retain traits typical for young workers.

Parasitism and queen presence interactively shape worker behaviour and fertility in an ant host

Parasites with complex life cycles regularly alter host traits in their own interest. In social hosts, phenotypic alterations induced by parasites can also affect uninfected group members. The tapeworm Anomotaenia brevis uses Temnothorax nylanderi ants as intermediate hosts, reducing host activity and behavioural repertoire, but increasing life span. Uninfected nestmates are less active and less aggressive and suffer from higher mortality. Next to parasites, the social environment, such as the queen, influences worker behaviour, reproduction and longevity. Here, we studied how tapeworm parasitism interacts with the queen to affect the behaviour and reproductive potential of ant workers. We collected naturally parasitized and unparasitized ant colonies, and experimentally removed the sole queen in half of each colony type to induce worker reproduction. We examined the behaviour and ovary development of tapeworm-infected workers, uninfected nurses and uninfected foragers from parasitized and unparasitized colonies living under queenright and queenless conditions. Remarkably, fertility induction was most pronounced in tapeworm-infected workers, which quickly responded to queen removal by developing their ovaries. The fertility of nurses, known to have the highest reproductive potential and to be in close contact with infected workers, was not reduced by tapeworm parasitism. However, their behaviour was impacted by an interaction between parasitism and queen removal: nurses from parasitized, queenless colonies became less active, whereas no behavioural changes were observed in nurses from unparasitized colonies. Behaviour and ovary development of foragers were unaffected by the presence of tapeworm-infected workers and the queen. Our findings indicate that parasitism by a tapeworm increases rather than decreases the reproductive potential of infected workers. We further show that parasites and the presence of dominant group members interactively shape fertility and behaviour of infected and healthy group members.

Regulation of host colony activity by the social parasite Polistes semenowi

The productivity of social groups depends critically on effective regulation of work effort among group members. In social insect colonies, regulation of work may be decentralised or alternatively may be controlled by one or a few individuals (‘pacemakers’) within the colony. Social parasites, which usurp host colonies and replace the dominant as the principal reproductive, similarly depend on efficient regulation of work by hosts to rear parasite offspring, but few studies have explored the strategies used by parasites to achieve this. We compared the role of the social parasite Polistes semenowi in regulating host activity with that of the dominant individual on unparasitized nests of the host species, P. dominula. Dominant foundresses acted as pacemakers within unparasitized colonies, interacting frequently with colony members to initiate activity bursts and foraging trips, whereas parasites did not initiate more activity than the average colony member. Nonetheless, overall activity levels were similar in parasitized and unparasitized colonies, indicating that parasites may use other, indirect means to control the host activity. Colony activity did not change significantly following the removal of parasites or dominant host foundresses, perhaps because other individuals rapidly assumed the dominant position, or because of persistent indirect effects on colony activity. The role of P. semenowi in regulating the host activity differs strikingly from that reported for a second Polistes social parasite, P. atrimandibularis, suggesting that different Polistes social parasites may have fundamentally different social roles within host colonies, despite being closely phylogenetically related to one another.

Gene expression patterns underlying parasite-induced alterations in host behaviour and life history.

Many parasites manipulate their hosts' phenotype. In particular, parasites with complex life cycles take control of their intermediate hosts' behaviour and life history to increase transmission to their definitive host. The proximate mechanisms underlying these parasite-induced alterations are poorly understood. The cestode Anomotaenia brevis affects the behaviour, life history and morphology of parasitized Temnothorax nylanderi ants and indirectly of their unparasitized nestmates. To gain insights on how parasites alter host phenotypes, we contrast brain gene expression patterns of T.nylanderi workers parasitized with the cestode, their unparasitized nestmates and unparasitized workers from unparasitized colonies. Over 400 differentially expressed genes between the three groups were identified, with most uniquely expressed genes detected in parasitized workers. Among these are genes that can be linked to the increased lifespan of parasitized workers. Furthermore, many muscle (functionality) genes are downregulated in these workers, potentially causing the observed muscular deformations and their inactive behaviour. Alterations in lifespan and activity could be adaptive for the parasite by increasing the likelihood that infected workers residing in acorns are eaten by their definitive host, a woodpecker. Our transcriptome analysis reveals numerous gene expression changes in parasitized workers and their uninfected nestmates and indicates possible routes of parasite manipulation. Although causality still needs to be established, parasite-induced alterations in lifespan and host behaviour appear to be partly explained by morphological muscle atrophy instead of central nervous system interference, which is often the core of behavioural regulation. Results of this study will shed light upon the molecular basis of antagonistic species interactions.

Vibratory signals predict rank and offspring caste ratio in a social insect

In complex societies, communication signals function as fine tools for regulating social structure and coordinating activities, while enabling groups to adjust their strategies flexibly in response to ecological conditions. Social wasps of the genus Polistes perform vibratory movements, which are expressed by dominant individuals mainly during adult-larva feeding interactions. Recent investigations have hypothesized that these signals may influence caste differentiation during larval development. We tested this hypothesis by conducting behavioural observations in the field, in three populations of social wasps (Polistes biglumis) differing in caste ratio: In some populations, foundresses produce workers and future reproductives; in others, workers are rarely produced. We observed that only foundresses produced vibratory signals, which were expressed during larval feeding sessions and only in the period before offspring emergence. Foundresses belonging to populations with workers spent more time producing vibratory signals than those from populations where workers are rare. In some populations, social parasites invaded colonies and subdued host foundresses. Subdued foundresses produced fewer vibratory signals than foundresses of unparasitized colonies. Our data suggest that the dominant status is necessary for the expression of vibratory signals and show that foundresses from different populations produced different numbers of vibratory signals. This difference can be explained well by the hypothesis that vibratory signals influence larval development and promote the production of workers. We suggest that these signals may have been the target of selective forces, in order to regulate caste ratio and maximize colony fitness under local conditions.

Degenerate slave‐makers, but nevertheless slave‐makers? Host worker relatedness in the ant Myrmoxenus kraussei

Socially parasitic ants of the formicoxenine genus Myrmoxenus exhibit considerable diversity in colony structure and life history. While some species are active slave-makers with many workers and others are workerless 'murder-parasites,' Myrmoxenus kraussei is considered as a 'degenerate slave-maker' because of its very low worker numbers. Here, we document that Temnothorax recedens host workers in single colonies of M. kraussei from Lago di Garda, Italy, exhibit significantly more genetic diversity than workers in unparasitized colonies. This raises the possibility that, despite its low worker numbers, M. kraussei may actively engage in slave raids in nature.

Using social parasitism to test reproductive skew models in a primitively eusocial wasp.

Remarkable variation exists in the distribution of reproduction (skew) among members of cooperatively breeding groups, both within and between species. Reproductive skew theory has provided an important framework for understanding this variation. In the primitively eusocial Hymenoptera, two models have been routinely tested: concessions models, which assume complete control of reproduction by a dominant individual, and tug-of-war models, which assume on-going competition among group members over reproduction. Current data provide little support for either model, but uncertainty about the ability of individuals to detect genetic relatedness and difficulties in identifying traits conferring competitive ability mean that the relative importance of concessions versus tug-of-war remains unresolved. Here, we suggest that the use of social parasitism to generate meaningful variation in key social variables represents a valuable opportunity to explore the mechanisms underpinning reproductive skew within the social Hymenoptera. We present a direct test of concessions and tug-of-war models in the paper wasp Polistes dominulus by exploiting pronounced changes in relatedness and power structures that occur following replacement of the dominant by a congeneric social parasite. Comparisons of skew in parasitized and unparasitized colonies are consistent with a tug-of-war over reproduction within P. dominulus groups, but provide no evidence for reproductive concessions.

Brood exchange experiments and chemical analyses shed light on slave rebellion in ants

Parasites and hosts frequently engage in coevolutionary arms races, in which newly developed host defenses will be counteracted by parasite adaptations. Slave-making ants are virulent social parasites that trick enslaved host workers into caring for their brood. These slaves also have to accept stolen host pupae, which slavemakers retrieve during raids. Previously, selection was thought to be unable to act on traits of these enslaved host ants. Yet, a recent study demonstrated rebellion of enslaved Temnothorax workers, which selectively killed female pupae of the slave-making ant Protomognathus americanus. This defensive trait could lower the costs of parasitism because slowed growth of parasite nests reduces raiding impact on related neighboring host colonies. In crossfostering experiments, we investigated the acceptance of host and parasite pupae by Temnothorax workers in parasitized and unparasitized colonies. Host workers commonly killed transferred pupae, and the presence of the social parasite only increased acceptance of parasite pupae in 1 host species and that of heterospecific host pupae in a second host. Parasite pupae survived better when transferred to sympatric host colonies than to allopatric ones, possibly indicating local adaptation in the parasite P. americanus. Cuticular hydrocarbon analyses explain this with chemical differences in pupae profiles between communities. Overall, parasite and host pupae have highly divergent profiles. Hence, cuticular hydrocarbons can potentially be used by host workers to identify and destroy parasite pupae. The parasite P. americanus should be under strong selection to adapt its pupal recognition cues to those of its hosts to counteract slave rebellion. Key words: brood parasites, chemical communication, coevolution, cuticular hydrocarbons, host defenses, slave-making ants. [Behav Ecol]

Oviposition avoidance of parasitized aphid colonies by the syrphid predator Episyrphus balteatus mediated by different cues

Abstract Oviposition decisions made by members of a guild of natural enemies can have evolved to avoid intraguild predation, potentially avoiding the disruption of the extraguild prey control. We have studied the oviposition preference of the aphidophagous predator Episyrphus balteatus De Geer (Diptera: Syrphidae) within colonies of Myzus persicae Sulzer (Hemiptera: Aphididae) in the presence of two developmental stages of the aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Aphidiidae). Results from a greenhouse choice experiment showed that E. balteatus females lay significantly fewer eggs in colonies with mummified aphids than in unparasitized colonies. Colonies of parasitized, but not yet mummified did not contain significantly fewer eggs than colonies with unparasitized aphids. In three no-choice experiments, we assessed stimuli coming from aphid honeydew, from the aphids themselves and also from extracts of the aphid bodies, and all of these stimuli mediate the discrimination of mummified aphids from healthy aphids. To a lesser extent these stimuli also contribute to the discrimination against aphids that are parasitized but not yet mummified. These results suggest that the effects of these two species could be complementary for the control of M. persicae, since the species that acts as an intraguild predator, E. balteatus, avoids ovipositing on aphid colonies parasitized by the intraguild prey, A. colemani.

Acanthocephalan (Oligacanthorhynchidae) parasitism of the Caribbean termite Nasutitermes acajutlae: implications for reproductive success

Few studies have examined the impact of parasitism on free-living social insects. We documented the association between an acanthocephalan parasite and survival, reproduction and growth of a Caribbean termite (Nasutitermes acajutlae). We measured these parameters yearly in ≥100 termite colonies for 4 years. In 2001 and 2002 we also compared the rate at which parasitized and unparasitized colonies rebuilt damaged foraging trails because trails protect foragers from predation as well as fluctuations in temperature and humidity. Although there were no significant differences in growth or survival between parasitized and unparasitized colonies, parasitized colonies reproduced significantly less often and rebuilt foraging trails significantly more slowly than unparasitized colonies. The average parasitized colony may sustain a loss of alate production =30% in the year in which it is parasitized, and a loss of up to 19% if it is parasitized once in a 5-year period. We conclude that the acanthocephalan parasite is associated with significant alteration of fitness parameters of individual N. acajutlae colonies. However, prevalence of parasitism is low (6.8%) and alate production by non-parasitized colonies is likely to compensate for losses due to parasitism. Therefore, it seems unlikely that this parasite affects N. acajutlae at the population level.

Species and Colony Components in the Recognition Odor of Young Social Wasps: Their Expression and Learning ( Polistes biglumis and P. atrimandibularis; Hymenoptera: Vespidae)

In Polistes, nestmate recognition relies on the learning of recognition cues from the nest. When wasps recognize nestmates, they match the template learned with the odor of the encountered wasp. The social wasp Polistes biglumis use the homogeneous odor of their colony to recognize nestmates. When these colonies become host colonies of the social parasite P. atrimandibularis, colony odor is no longer homogeneous, as the parasite offspring have an odor that differs from that of their hosts. In trying to understand how the mechanism of nestmate recognition works in parasitized colonies and why parasite offspring are accepted by hosts, we tested the responses of resident Polistes biglumis wasps from parasitized and unparasitized colonies to newly emerged parasites and to nestmate and non-nestmate conspecifics. The experiments indicate that immediately upon eclosion both young parasites and young hosts lack a colony odor and that colony odor can be soon acquired from the accepting colony. In addition, while residents of nonparasitized colonies recognize only the odor of their species, resident hosts of parasitized colonies have learned a template that fits the odors of two species.