Social Hymenopterans Research Articles

“Surface Ultra-Structural Studies on Antennae in Polymorphs of Weaver Ant Oecophylla smaragdina; Fabricius” (Hymenoptera: Formicidae) with Reference to Sensilla

Oecophylla smaragdina is an established biological pest control agent in south-east Asian continent for cash crops like cashew and mango. It is a cosmopolitan species found all over the Asian continent. Being a social hymenopteran insect, Oecophylla smaragdina has a colony comprising of polymorphs. The morphological and ultra-structural investigation of such polymorphs antenna was done with scanning electron microscopy to reveal presence of various chemosensory, thermo-sensory and tactile sensory sensillae on the antennal segments with their specific role in the polymorphs. The role of worker in foraging activity is supported with the presence of large number of sensilla compared to other castes.

Hormone-mediated dispersal and sexual maturation in males of the social paper wasp Polistes lanio.

Sex-biased dispersal is common in social species, but the dispersing sex may delay emigration if associated benefits are not immediately attainable. In the social Hymenoptera (ants, some bees and wasps), newly emerged males typically disperse from the natal nest whilst most females remain as philopatric helpers. However, little information exists on the mechanisms regulating male dispersal. Furthermore, the conservation of such mechanisms across the Hymenoptera and any role of sexual maturation are also relatively unknown. Through field observations and mark-recapture, we observed that males of the social paper wasp Polistes lanio emerge from pupation sexually immature, and delay dispersal from their natal nest for up to 7 days whilst undergoing sexual maturation. Delayed dispersal may benefit males by allowing them to mature in the safety of the nest and thus be more competitive in mating. We also demonstrate that both male dispersal and maturation are associated with juvenile hormone (JH), a key regulator of insect reproductive physiology and behaviour, which also has derived functions regulating social organisation in female Hymenoptera. Males treated with methoprene (a JH analogue) dispersed earlier and possessed significantly larger accessory glands than their age-matched controls. These results highlight the wide role of JH in social hymenopteran behaviour, with parallel ancestral functions in males and females, and raise new questions on the nature of selection for sex-biased dispersal.

Queen and king recognition in the subterranean termite, Reticulitermes flavipes: Evidence for royal recognition pheromones.

Royal recognition is a central feature of insect societies, allowing them to maintain the reproductive division of labor and regulate colony demography. Queen recognition has been broadly demonstrated and queen recognition pheromones have been identified in social hymenopterans, and in one termite species. Here we describe behaviors that are elicited in workers and soldiers by neotenic queens and kings of the subterranean termite, Reticulitermes flavipes, and demonstrate the chemical basis for the behavior. Workers and soldiers readily perform a lateral or longitudinal shaking behavior upon antennal contact with queens and kings. When royal cuticular chemicals are transferred to live workers or inert glass dummies, they elicit antennation and shaking in a dose-dependent manner. The striking response to reproductives and their cuticular extracts suggests that royal-specific cuticular compounds act as recognition pheromones and that shaking behavior is a clear and measurable queen and king recognition response in this termite species.

Particulate matter collection by honey bees (Apis mellifera, L.) near to a cement factory in Italy.

Industrial activities play a key role in the economic well-being of a country but they usually involve processes with a more or less profound environmental impact, including emission of pollutants. Among them, much attention has been given to airborne particulate matter (PM) whose exposure is ubiquitous and linked with several adverse health effects mainly due to its size and chemical composition. Therefore, there is a strong need to exploit monitoring systems for airborne PM able to provide accurate information on the potential health hazards and the specific emission sources for the implementation of adequate control strategies. The honey bee (Apis mellifera, L.) is widely used as an indicator of environmental pollution: this social hymenopteran strongly interacts with vegetables, air, soil, and water surrounding the hive and, as a consequence, pollutants from these sources are translated to the insect and to the hive products. During the wide-ranging foraging activity, the forager bee is known to collect samples of the main airborne PM pollutants emitted from different sources and therefore it can be used as an efficient PM sampler. In the present research, PM contaminating forager bees living nearby a cement factory and several kilometers away from it has been analysed and characterised morphologically, dimensionally and chemically through SEM/EDX. This provided detailed information on the role of both the cement manufacturing activities and the vehicular traffic as sources of airborne PM. This may indeed help the implementation of appropriate preventive and corrective actions that would effectively minimize the environmental spread of pollutant PM not only in areas close to the plant, but also in more distant areas.

How do animals find their way back home? A brief overview of homing behavior with special reference to social Hymenoptera

Performing efficient homing, i.e., returning to a previously known place, is crucial for the survival of any motile animal. Animals perform homing across different spatial scales and environments, employing various mechanisms with the aid of different sensorimotor systems molded by their varied evolutionary histories and ecological constraints. Despite these differences, most of the homing mechanisms across different taxa can be explained by some general basic mechanisms. Studies from social hymenopterans contribute substantially to the knowledge base of this study field and are, especially, interesting—they show excellent homing capabilities while possessing relatively simple neural architectures, and hence, their homing mechanisms are considered as economic solutions to a complex problem. Moreover, many of their homing mechanisms have also been observed in other taxa including vertebrates. With the advent of new technologies and increased research, our understanding of the hymenopteran homing is improving faster than ever—and therefore, a regular contemporary update might be of much help. In this review, I present a brief synthesis of previous and current understanding of homing mechanisms in social hymenopterans, with descriptions of the cues that they exploit for homing, and a comparative discussion on terminologies frequently used in social Hymenoptera with analogous terminologies used to describe similar phenomena in other taxa. I conclude with a note on the potential of applying the knowledge from homing studies in other fields of research like neurobiology and robotics, and possible future directions.

TGFβ signaling related genes are involved in hormonal mediation during termite soldier differentiation.

A working knowledge of the proximate factors intrinsic to sterile caste differentiation is necessary to understand the evolution of eusocial insects. Genomic and transcriptomic analyses in social hymenopteran insects have resulted in the hypothesis that sterile castes are generated by the novel function of co-opted or recruited universal gene networks found in solitary ancestors. However, transcriptome analysis during caste differentiation has not been tested in termites, and evolutionary processes associated with acquiring the caste are still unknown. Termites possess the soldier caste, which is regarded as the first acquired permanently sterile caste in the taxon. In this study, we performed a comparative transcriptome analysis in termite heads during 3 molting processes, i.e., worker, presoldier and soldier molts, under natural conditions in an incipient colony of the damp-wood termite Zootermopsis nevadensis. Although similar expression patterns were observed during each molting process, more than 50 genes were shown to be highly expressed before the presoldier (intermediate stage of soldier) molt. We then performed RNA interference (RNAi) of the candidate 13 genes, including transcription factors and uncharacterized protein genes, during presoldier differentiation induced by juvenile hormone (JH) analog treatment. Presoldiers induced after RNAi of two genes related to TGFβ (Transforming growth factor beta) signaling were extremely unusual and possessed soldier-like phenotypes. These individuals also displayed aggressive behaviors similar to natural soldiers when confronted with Formica ants as hypothetical enemies. These presoldiers never molted into the next instar, presumably due to the decreased expression levels of the molting hormone (20-hydroxyecdysone; 20E) signaling genes. These results suggest that TGFβ signaling was acquired for the novel function of regulating between JH and 20E signaling during soldier differentiation in termites.

Return of Drones: Flight Experience Improves Returning Performance in Honeybee Drones

The effect of experience on the behavior of worker bees has been extensively investigated; however, few such studies have been conducted on male bees. Honeybee (Apis mellifera) males (drones), unlike the males of other social hymenopterans, return to their nest after performing a mating flight and have, therefore, an opportunity to learn from their experiences. This provides a chance to understand the significance of experience in social hymenopteran males. Here, we investigated whether experience improves the returning performance in drones (rate and time of return to the hive). We compared the returning performance of “Experienced” drones that were allowed to fly freely and thus had an opportunity to learn the position of the hive before the experiment with “Naive” drones that were not allowed to fly and therefore, had no opportunity to learn. We found that Experienced drones returned to the hive after a displacement, whereas Naive drones did not. Furthermore, time to return decreased with the age of drones. These results suggest that flight experience improves the returning performance, which should increase the possibility of mating success and overall colony fitness.

Mutual intra- and interspecific social parasitism between parapatric sister species of Vespula wasps

Cooperative breeding of animals is vulnerable to social parasitism, in which parasites usurp the labors of the hosts. In social hymenopterans, social parasitism has evolved numerous times independently, and the process by which it has arisen is thus a major question in evolutionary biology. It is generally thought that parasites originate from their hosts via sympatric speciation, and some actual examples have been reported. On the other hand, an alternative hypothesis that allopatric speciation first occurred, and then one species subsequently evolved as the parasite of its sister species has been theoretically supported, but no actual cases have yet been reported. Here, we report that our observations suggest facultative, temporary, and mutual social parasitism that occurs in both an intra- and interspecific manner in two sister species of yellow jackets, Vespula flaviceps and V. shidai, in Japan. Considering their parapatric distribution, social structure, and parasitic behaviors, social parasitism between these two species does not follow the conventional sympatric speciation hypothesis (intraspecific hypothesis), but possibly supports the social deception hypothesis (interspecific hypothesis). The mutual social parasitism between parapatric sister species offers a good opportunity to study the evolution of social parasitism.

Male meliponine bees (Scaptotrigona aff. depilis) produce alarm pheromones to which workers respond with fight and males with flight.

In highly social hymenopteran societies, males mainly serve reproductive purposes. Semiochemicals enable the different hymenopteran sexes and castes to communicate with each other and to coordinate important functions within colonies. I hereby show that sexual dimorphism in meliponine bees incorporates the alarm and defence communication system. I chemically analysed the mandibular glands of Scaptotrigona aff. depilis using GCMS methods and conducted behavioural experiments in both males and female workers using cephalic and mandibular gland extracts. In addition, behaviour studies with male cephalic extracts were also conducted in Scaptotrigona bipunctata and Partamona cupira. Males and female worker bees showed differences in the content of the mandibular glands, which are responsible for alarm communication in meliponines. Males never attacked but usually fled when confronted with the mandibular gland extract content of other conspecific males or females. Interestingly, however, meliponine males were still able to raise alarm and to induce substantial amounts of aggression at nest entrances, which is different from the much better known and studied honey bees. Potential reasons are briefly discussed.

Reproductive concessions between related and unrelated members promote eusociality in bees.

Animal societies exhibit remarkable variation in their breeding strategies. Individuals can maximize their fitness by either reproducing or by helping relatives. Social hymenopterans have been key taxa for the study of Hamilton’s inclusive fitness theory because the haplodiploid sex-determination system results in asymmetric relatedness among breeders producing conflict over the partitioning of reproduction. In small cooperative groups of insects, totipotent individuals may maximize their inclusive fitness by controlling reproduction despotically rather than helping their relatives. Here, we demonstrate that the dominant females of the primitively eusocial bee Euglossa melanotricha (Apidae: Euglossini) control reproduction, but concede part of the reproductive output with their related and unrelated subordinates. As expected, a dominant female capitalizes on the direct reproduction of related subordinates, according to her interests. We found that reproductive skew was positively correlated with relatedness. The concessions were highly reduced in mother-daughter and sibling nests (relatedness r ± s.d. = 0.54 ± 0.02 and 0.79 ± 0.02, respectively) but much more egalitarian in unrelated associations (r = −0.10 ± 0.01). We concluded that reproductive skew in these primitively eusocial bees is strongly related to the genetic structure of associations, and also that females are able to assess pairwise relatedness, either directly or indirectly, and use this information to mediate social contracts.

A comparative analysis of rapid antennation behavior in four species of Odontomachus trap-jaw ants

The exchange of rapid antennal strikes between individuals is a behavior exhibited by many social hymenopterans, largely in dominance contexts within the nest and in aggressive contexts towards non-nestmates. Despite being widely reported, the behavior itself has not been well described or compared between species for the majority of social insect groups. We first document how often rapid antennation is used as an aggressive response to non-nestmates for four species of Odontomachus ants. We then use high-speed videography to measure the rate of rapid antennation behavior for these species. We find that rates are neither conserved nor species-specific and average between 19.5 and 41.5 strikes/s. Next, with O. brunneus, we compare this behavior as it is performed between nestmates and non-nestmates. We find no context-specific differences in rate, bout length, or number of strikes. We conclude by discussing the evolution of this behavior and its potential utility as a model for understanding aggressive behaviors both inside and outside of the nest.

The Sensory Ecology of Ant Navigation: From Natural Environments to Neural Mechanisms.

Animals moving through the world are surrounded by potential information. But the components of this rich array that they extract will depend on current behavioral requirements and the animal's own sensory apparatus. Here, we consider the types of information available to social hymenopteran insects, with a specific focus on ants. This topic has a long history and much is known about how ants and other insects use idiothetic information, sky compasses, visual cues, and odor trails. Recent research has highlighted how insects use other sensory information for navigation, such as the olfactory cues provided by the environment. These cues are harder to understand because they submit less easily to anthropomorphic analysis. Here, we take an ecological approach, considering first what information is available to insects, then how different cues might interact, and finally we discuss potential neural correlates of these behaviors.

Changes in follicular cells architecture during vitellogenin transport in the ovary of social Hymenoptera.

Vitellogenins are the major yolk proteins, synthesized in the fat body, released into the hemolymph and captured by the developing oocytes, but the mechanisms by which these proteins cross the follicular cell layer are still poorly understood. This study describes the actin distribution in follicular cells during vitellogenin transport to the oocyte in social Hymenoptera represented by bees Apis mellifera and Melipona quadrifasciata, the wasp Mischocyttarus cassununga and the ant Pachycondyla curvinodis. In oocytic chambers of vitellogenic follicles, vitellogenin was found within the follicular cells, perivitelline space and oocyte, indicating a transcellular route from the hemolymph to the perivitelline space. The cortical actin cytoskeleton in follicular cells underwent reorganization during transport of vitellogenin across this epithelium suggesting that in the ovary of social hymenopterans, vitellogenin delivery to oocytes requires a dynamic cytoskeletal rearrangement of actin filaments in the follicular cells.

Searching behavior in social Hymenoptera

The movement pattern of a searching animal affects how it interacts with the environment, thus playing an important role in many environmental processes. Social hymenopteran foragers make good models for studying search patterns because their only role is to search for food and bring it back to the nest or hive. Search patterns in ants and bees, the most studied social hymenopterans, consist of loops around the origin of search that expand in size as the search goes on. Different factors influence search structure, including the type and distribution of the resource that is targeted, and the kind and amount of information available for navigation. In the distributions of the lengths of search segments, bees exhibit a Lévy walk pattern, which follows a power law in which occasional long segments are interspersed within many short segments, and yet longer segments are interspersed within the long segments. Such a scale-free and heavy-tailed distribution has been shown to be optimal in searching for sparse targets. Ants on the other hand show a composite Brownian search distribution, composed of two exponential distributions at different scales. We argue that such composite Brownian searches serve to approximate a Lévy walk. Both Lévy walks and composite Brownian searches are found in a range of other animals, including hunter–gatherer humans. These patterns may be ancient, as they have been found in fossils dating to at least 50 million years.

Foliar Substrate Affects Cuticular Hydrocarbon Profiles and Intraspecific Aggression in the Leafcutter Ant Atta sexdens.

Cuticular hydrocarbons (CHCs) are traditionally considered to be one of the most important chemical cues used in the nestmate recognition process of social hymenopterans. However, it has been suggested that in the leafcutter ant genus Atta, it is not the CHCs, but the alarm pheromone that is involved in the nestmate recognition process. In this study we used a laboratory population of Atta sexdens to explore the association between their CHC profile variation and intraspecific aggression. In the first part of the experiment, four colonies were divided into two groups with distinct diets to stimulate differentiation of their CHC profiles. In the second part of the experiment, all colonies received the same diet to examine resemblance of chemical profiles. At the end of each part of the experiment we extracted the CHCs from workers. The results demonstrated that colonies that shared the same food resource had similar cuticular hydrocarbon profiles. Furthermore, colonies were significantly more aggressive towards conspecifics that used a different foliar substrate and consequently had greater differences in their cuticular chemical composition. This study suggests that the CHC profiles of A. sexdens can be affected by the foliar substrates used, and that the CHCs are used in the nestmate recognition process of this species.

A new antigenic marker specifically labels a subpopulation of the class II Kenyon cells in the brain of the European honeybee Apis mellifera.

The mushroom bodies are the higher-order integration center in the insect brain and are involved in higher brain functions such as learning and memory. In the social hymenopteran insects such as honeybees, the mushroom bodies are the prominent brain structures. The mushroom bodies are composed of lobed neuropils formed by thousands of parallel-projecting axons of intrinsic neurons, and the lobes are divided into parallel subdivisions. In the present paper, we report a new antigenic marker to label a single layer in the vertical lobes of the European honeybee Apis mellifera. In the brain of A. mellifera, a monoclonal antibody (mAb) 15C3, which was originally developed against an insect ecdysone receptor (EcR) protein, immunolabels a single layer of the vertical lobes that correspond to the most dorsal layer of the γ-lobe. The 15C3 mAb recognizes a single ~200 kDa protein expressed in the adult honeybee brain. In addition, the 15C3 mAb immunoreactivity was also observed in the lobes of the developing pupal mushroom bodies. Since γ-lobe is well known to their extensive reorganization that occurs during metamorphosis in Drosophila, the novel antigenic marker for the honeybee γ-lobe allows us to investigate morphological changes of the mushroom bodies during metamorphosis.

Behavioral syndrome in a native and an invasive hymenoptera species.

Recent studies have focused on the role of behavior in biological invasions. Individuals may differ consistently in time for several behavioral traits (personality) which covary (behavioral syndrome) resulting in different behavioral types, some of them favoring invasion. Social hymenopterans have a strong potential to be invaders and their success depends primarily on the foundresses' ability to found viable colonies. They are expected to be active, explorative and bold for optimally establishing their nest. In Europe, 2 hornet species coexist: the native Vespa crabro and the invasive Vespa velutina. These 2 species may compete for nesting sites and we suggest that the initial success of V. velutina has been favored by its behavior in outperforming V. crabro for the traits involved in nest initiation. Here, we (i) defined the personality of V. crabro and V. velutina, (ii) tested for the existence of behavioral syndrome in these species, and (iii) compared their performances using an open-field test. Our results show that V. crabro foundresses behave consistently but not V. velutina; this lack of consistency being mainly due to reduced variance among individuals. This result questions the possibility of detecting consistent behavioral differences in species having recently undergone a strong bottleneck. Both species exhibit the same correlations between activity, boldness and exploration and V. velutina clearly outperforms V. crabro for all traits. Our results suggest that activity, boldness, and exploration are implicated in both hornet nest initiation and invasion process which contributed to explain why social hymenopterans are so successful at colonization.

Representación odotópica de la organización glomerular del lóbulo antenal en los cuerpos fungiformes de las hormigas (Hymenoptera: Formicidae): Comparaciones entre dos especies

In this work, the organization of the antennal lobes (ALs) and its topographic representation in the mushroom bodies (MBs) in soldiers of two species of ants has been compared. Morphologic comparison between these species suggests that ALs of A. mexicana could be more specialized than that of C. ocreatus at the expense of general capabilities. In both species the AL is organized in six groups of glomeruli, each of which innervated by its own tract. Glomeruli clusters are grouped in two regions, anterior and posterior, by the innervation of projection neurons (PNs) that connect AL with MBs via antennoprotocerebral tracts (APT). Calyces of MBs are layered and receive segregated olfactory information: PNs innervating anterior glomeruli clusters send axons through lateral-APT to the lateral horn (LH) and then to inner layer of the calyx, while PNs innervating posterior glomeruli clusters send axons through medial-APT to inner layers of the calyx and then to the LH. These results show that AL organization is topographically represented in the MB forming a coarse odotopic map. The two pathways connecting AL with MB could represent two channels for processing different kinds of odors or different properties of olfactory stimuli. The neuroanatomical results suggest a conserved functional organization in social hymenopterans.

Whole-Genome DNA Methylation Profile of the Jewel Wasp (Nasonia vitripennis)

The epigenetic mark of DNA methylation, the addition of a methyl (CH3) group to a cytosine residue, has been extensively studied in many mammalian genomes and, although it is commonly found at the promoter regions of genes, it is also involved in a number of different biological functions. In other complex animals, such as social insects, DNA methylation has been determined to be involved in caste differentiation and to occur primarily in gene bodies. The role of methylation in nonsocial insects, however, has not yet been explored thoroughly. Here, we present the whole-genome DNA methylation profile of the nonsocial hymenopteran, the jewel wasp (Nasonia vitripennis). From high-throughput sequencing of bisulfite-converted gDNA extracted from male Nasonia thoraces, we were able to determine which cytosine residues are methylated in the entire genome. We found that an overwhelming majority of methylated sites (99.7%) occur at cytosines followed by a guanine in the 3′ direction (CpG sites). Additionally, we found that a majority of methylation in Nasonia occurs within exonic regions of the genome (more than 62%). Overall, methylation is sparse in Nasonia, occurring only at 0.18% of all sites and at 0.63% of CpGs. Our analysis of the Nasonia methylome revealed that in contrast to the methylation profile typically seen in mammals, methylation is sparse and is constrained primarily to exons. This methylation profile is more similar to that of the social hymenopteran species, the honey bee (Apis mellifera). In presenting the Nasonia methylome, we hope to promote future investigation of the regulatory function of DNA methylation in both social and nonsocial hymenoptera.

A test of neuroecological predictions using paperwasp caste differences in brain structure (Hymenoptera: Vespidae)

Adaptive brain architecture hypotheses predict brain region investment matches the cognitive and sensory demands an individual confronts. Social hymenopteran queen and worker castes differ categorically in behavior and physiology leading to divergent sensory experiences. Queens in mature colonies are largely nest-bound while workers depart nests to forage. We predicted social paperwasp castes would differ in tissue allocation among brain regions. We expected workers to invest relatively more than queens in neural tissues that process visual input. As predicted, we found workers invested more in visual relative to antennal processing than queens both in peripheral sensory lobes and in central processing brain regions (mushroom bodies). Although we did not measure individual brain development changes, our comparative data provide a preliminary test of mechanisms of caste differences. Paperwasp species differ in the degree of caste differentiation (monomorphic versus polymorphic castes) and in colony structure (independent- versus swarm-founding); these differences could correspond to the magnitude of caste brain divergence. If caste differences resulted from divergent developmental programs (experience-expectant brain growth), we predicted species with morphologically distinct queens, and/or swarm-founders, would show greater caste divergence of brain architecture. Alternatively, if adult experience affected brain plasticity (experience-dependent brain growth), we predicted independent-founding species would show greater caste divergence of brain architecture. Caste polymorphism was not related to the magnitude of queen-worker brain differences, and independent-founder caste brain differences were greater than swarm-founder caste differences. Greater caste separation in independent-founder brain structure suggests a role for adult experience in the development of caste-specific brain anatomy.