Chemical and Behavioural Strategies along The Spectrum of Host Specificity in Ant-Associated Silverfish

Background Host range is a fundamental trait to understand the ecological and evolutionary dynamics of symbionts. Increasing host specificity is expected to be accompanied with specialization in different symbiont traits. We tested this specificity-specialization association in a large group of 16 ant-associated silverfish species by linking their level of host specificity with their degree of behavioural integration into the colony and their accuracy of chemically deceiving the host’s recognition system, i.e. the cuticular hydrocarbon (CHC) profile. Results As expected, facultative associates and host generalists (targeting multiple unrelated ants) tend to avoid the host, whereas host-specialists (typically restricted to Messor ants) were bolder, approached the host and allowed inspection. Generalists and host specialists regularly followed a host worker, unlike the other silverfish. Host aggression was extremely high toward non-ant-associated silverfish and modest to low in ant-associated groups. Surprisingly, the degree of chemical deception was not linked with host specificity as most silverfish, including facultative ant associates, imitated the host’s CHC profile. Messor specialists retained the same CHC profile as the host after moulting, in contrast to a host generalist, suggesting an active production of the cues (chemical mimicry). Host generalist and facultative associates flexibly copied the highly different CHC profiles of alternative host species, pointing at passive acquisition (chemical camouflage) of the host’s odour. Conclusions Overall, we found that behaviour that seems to facilitate the integration in the host colony was more pronounced in host specialist silverfish. Chemical deception, however, was employed by all ant-associated species, irrespective of their degree of host specificity.

Genetic Variation in Antimicrobial Activity of Honey Bee (Apis mellifera) Seminal Fluid

Honey bees can host a remarkably large number of different parasites and pathogens, and some are known drivers of recent declines in wild and managed bee populations. Here, we studied the interactions between the fungal pathogen Nosema apis and seminal fluid of the Western honey bee (Apis mellifera). Honey bee seminal fluid contains multiple antimicrobial molecules that kill N. apis spores and we therefore hypothesized that antimicrobial activities of seminal fluid are genetically driven by interactions between honey bee genotype and different N. apis strains/ecotypes, with the virulence of a strain depending on the genotype of their honey bee hosts. Among the antimicrobials, chitinases have been found in honey bee seminal fluid and have the predicted N. apis killing capabilities. We measured chitinase activity in the seminal fluid of eight different colonies. Our results indicate that multiple chitinases are present in seminal fluid, with activity significantly differing between genotypes. We therefore pooled equal numbers of N. apis spores from eight different colonies and exposed subsamples to seminal fluid samples from each of the colonies. We infected males from each colony with seminal fluid exposed spore samples and quantified N. apis infections after 6 days. We found that host colony had a stronger effect compared to seminal fluid treatment, and significantly affected host mortality, infection intensity and parasite prevalence. We also found a significant effect of treatment, as well as a treatment × colony interaction when our data were analyzed ignoring cage as a blocking factor. Our findings provide evidence that N. apis-honey bee interactions are driven by genotypic effects, which could be used in the future for breeding purposes of disease resistant or tolerant honey bee stock.

Co-occurrence in ant primary parasitoids: a Camponotus rectangularis colony as host of two eucharitid wasp genera

Different assemblages of parasitoids may attack a given host species and non-random distribution patterns in parasitoid species assemblages have been reported on various occasions, resulting in co-occurrence at the population, colony, or even individual host levels. This is the case for different closely related species of eucharitid wasps (a family of specialized ant parasitoids) sharing similar niches and co-occurring on the same host at different levels. Here we reviewed all known associations between eucharitid wasps and the ant host genus Camponotus Mayr, 1861 and reported new ant-parasitoid associations. In addition, we report a new case of co-occurrence in eucharitid wasps, at the host colony level, involving a new undescribed species of Pseudochalcura Ashmead, 1904 and an unidentified species of Obeza Heraty, 1985, which attack the common but very poorly known neotropical arboreal ant Camponotus rectangularis Emery, 1890. Most attacks were solitary, but various cocoons were parasitized by two (16%) or three (8%) parasitoids. Globally, parasitism prevalence was very low (3.7%) but showed an important variability among samples. Low parasitism prevalence along with host exposure to parasitoid attack on host plants and overlapping reproductive periods of both parasitoid species may have allowed the evolution of co-occurrence. We also provided some additional data regarding the host ant nesting habits, the colony composition and new symbiotic associations with membracids and pseudococcids. The seemingly polydomous nesting habits of C. rectangularis could play a part in the reduction of parasitism pressure at the population level and, combined with occasionally important local parasitism rates, could also contribute to some parts of the colonies escaping from parasites, polydomy possibly representing an effective parasitism avoidance trait.

The Inquiline Ant Myrmica karavajevi Uses Both Chemical and Vibroacoustic Deception Mechanisms to Integrate into Its Host Colonies

Social parasitism represents a particular type of agonistic interaction in which a parasite exploits an entire society instead of a single organism. One fascinating form of social parasitism in ants is the “inquilinism”, in which a typically worker-less parasitic queen coexists with the resident queen in the host colony and produces sexual offspring. To bypass the recognition system of host colonies, inquilines have evolved a repertoire of deceiving strategies. We tested the level of integration of the inquiline Myrmica karavajevi within the host colonies of M. scabrinodis and we investigated the mechanisms of chemical and vibroacoustic deception used by the parasite. M. karavajevi is integrated into the ant colony to such an extent that, in rescue experiments, the parasite pupae were saved prior to the host’s brood. M. karavajevi gynes perfectly imitated the cuticular hydrocarbon profiles of M. scabrinodis queens and the parasite vibroacoustic signals resembled those emitted by the host queens eliciting the same levels of attention in the host workers during playback experiments. Our results suggest that M. karavajevi has evolved ultimate deception strategies to reach the highest social status in the colony hierarchy, encouraging the use of a combined molecular and behavioural approach when studying host–parasite interactions.

Differential investment in visual and olfactory brain regions mirrors the sensory needs of a paper wasp social parasite and its host

ABSTRACTObligate social parasites evolve traits to effectively locate and then exploit their hosts, whereas hosts have complex social behavioral repertoires, which include sensory recognition to reject potential conspecific intruders and heterospecific parasites. While social parasite and host behaviors have been studied extensively, less is known about how their sensory systems function to meet their specific selective pressures. Here, we compare investment in visual and olfactory brain regions in the paper wasp Polistes dominula, and its obligate social parasite P. sulcifer, to explore the link between sensory systems and brain plasticity. Our results show opposite and significant differences, consistent with their very different life-histories, in the sensory investments between these two closely-related species. Social parasites initially invest in the optic lobes to likely locate their hosts. After host colony usurpation, the parasite increases its brain volume, with specific investment in antennal lobes, which mirrors the behavioral switch from a usurping parasite to an integrated parasitic queen of the host colony. Contrastingly, hosts initially invest in the antennal lobes and sensory processing compared to social parasites, as predicted by their need to maintain social cohesion, allocate colony tasks, and recognize con- and heterospecific intruders. Host queens show a trend of higher investment in all sensory brain regions compared to workers, paralleling differences in task allocations. Our work provides novel insights into how intraspecific brain plasticity can facilitate the unique sensory adaptations needed to perform specific tasks by the host or to transition from searching to successful host exploitation by the social parasite.

The Exocrine Chemistry of the Parasitic Wasp Sphecophaga orientalis and Its Host Vespa orientalis: A Case of Chemical Deception?

The main challenge facing a parasite of social insects lies in deceiving its host’s detection and defense systems in order to enter and survive within the host colony. Sphecophaga orientalis is an ichneumonid wasp that parasitizes the pupae of the Oriental hornet Vespa orientalis. In Israel’s Mediterranean region, this parasitoid infects on average 23.48% (8–56%) of the host pupal cells. Observation of colonies brought to the laboratory revealed that the parasite moves around within the colony without being aggressed by the host workers. To assess how the parasite evades host detection and defense, we compared the cuticular hydrocarbon (CHC) profiles of both species. There was little similarity between the parasite and the host workers’ CHC, refuting the hypothesis of chemical mimicry. The parasite’s CHCs were dominated by linear alkanes and alkenes with negligible amounts of branched alkanes, while the host workers’ CHCs were rich in branched alkanes and with little or no alkenes. Moreover, the parasite cuticular wash was markedly rich in oleic acid, previously reported as a cue eliciting necrophoric behavior. Since nests of Oriental hornets are typified by large amounts of prey residues, we suggest that, due to its unfamiliar CHCs and the abundance of oleic acid, the parasite is considered as refuse by the host. We also detected rose oxide in the parasitoid head extracts. Rose oxide is a known insect repellent, and can be used to repel and mitigate aggression in workers. These two factors, in concert, are believed to aid the parasite to evade host aggression.

Asexual and sexual reproduction are two separate developmental pathways in a Termitomyces species

Although mutualistic symbioses per definition are beneficial for interacting species, conflict may arise if partners reproduce independently. We address how this reproductive conflict is regulated in the obligate mutualistic symbiosis between fungus-growing termites and Termitomyces fungi. Even though the termites and their fungal symbiont disperse independently to establish new colonies, dispersal is correlated in time. The fungal symbiont typically forms mushrooms a few weeks after the colony has produced dispersing alates. It is thought that this timing is due to a trade-off between alate and worker production; alate production reduces resources available for worker production. As workers consume the fungus, reduced numbers of workers will allow mushrooms to ‘escape’ from the host colony. Here, we test a specific version of this hypothesis: the typical asexual structures found in all species of Termitomyces —nodules—are immature stages of mushrooms that are normally harvested by the termites at a primordial stage. We refute this hypothesis by showing that nodules and mushroom primordia are macro- and microscopically different structures and by showing that in the absence of workers, primordia do, and nodules do not grow out into mushrooms. It remains to be tested whether termite control of primordia formation or of primordia outgrowth mitigates the reproductive conflict.

Importance of the Host Phenotype on the Preservation of the Genetic Diversity in Codling Moth Granulovirus

To test the importance of the host genotype in maintaining virus genetic diversity, five experimental populations were constructed by mixing two Cydia pomonella granulovirus isolates, the Mexican isolate CpGV-M and the CpGV-R5, in ratios of 99% M + 1% R, 95% M + 5% R, 90% M + 10% R, 50% M + 50% R, and 10% M + 90% R. CpGV-M and CpGV-R5 differ in their ability to replicate in codling moth larvae carrying the type I resistance. This ability is associated with a genetic marker located in the virus pe38 gene. Six successive cycles of replication were carried out with each virus population on a fully-permissive codling moth colony (CpNPP), as well as on a host colony (RGV) that carries the type I resistance, and thus blocks CpGV-M replication. The infectivity of offspring viruses was tested on both hosts. Replication on the CpNPP leads to virus lineages preserving the pe38 markers characteristic of both isolates, while replication on the RGV colony drastically reduces the frequency of the CpGV-M pe38 marker. Virus progeny obtained after replication on CpNPP show consistently higher pathogenicity than that of progeny viruses obtained by replication on RGV, independently of the host used for testing.

Infection Outcomes are Robust to Thermal Variability in a Bumble Bee Host–Parasite System

Climate change-related increases in thermal variability and rapid temperature shifts will affect organisms in multiple ways, including imposing physiological stress. Furthermore, the effects of temperature may alter the outcome of biotic interactions, such as those with pathogens and parasites. In the context of host–parasite interactions, the beneficial acclimation hypothesis posits that shifts away from acclimation or optimum performance temperatures will impose physiological stress on hosts and will affect their ability to resist parasite infection. We investigated the beneficial acclimation hypothesis in a bumble bee–trypanosome parasite system. Freshly emerged adult worker bumble bees, Bombus impatiens, were acclimated to 21, 26, or 29°C. They were subsequently experimentally exposed to the parasite, Crithidia bombi, and placed in a performance temperature that was the same as the acclimation temperature (constant) or one of the other temperatures (mismatched). Prevalence of parasite transmission was checked 4 and 6 days post-parasite exposure, and infection intensity in the gut was quantified at 8 days post-exposure. Parasite strain, host colony, and host size had significant effects on transmission prevalence and infection load. However, neither transmission nor infection intensity were significantly different between constant and mismatched thermal regimes. Furthermore, acclimation temperature, performance temperature, and the interaction of acclimation and performance temperatures had no significant effects on infection outcomes. These results, counter to predictions of the beneficial acclimation hypothesis, suggest that infection outcomes in this host–parasite system are robust to thermal variation within typically experienced ranges. This could be a consequence of adaptation to commonly experienced natural thermal regimes or a result of individual and colony level heterothermy in bumble bees. However, thermal variability may still have a detrimental effect on more sensitive stages or species, or when extreme climatic events push temperatures outside of the normally experienced range.