Collective retention and transmission of chemical signals in a social insect

Social insect colonies exhibit highly coordinated responses to ecological challenges by acquiring information that is disseminated throughout the colony. Some responses are coordinated directly from the signals produced by individuals that acquired the information. Other responses may require information to be transferred indirectly through a third party, thereby requiring colony-wide retention of information. Social insects use colony signature odours to distinguish between nestmates and non-nestmates, and the level of aggression between non-nestmates typically varies according to the distance between colonies and thus their history of interactions. Such coordinated, colony-specific responses may require information about particular odours to be disseminated and retained across the colony. Our field experiments with weaver ants reveal colony-wide, indirect acquisition and retention of the signature odours of a different colony with which they had experienced aggression. These data highlight the significance of interaction history and suggest the presence of a collective memory.     

Multilevel selection and social evolution of insect societies

How sterile, altruistic worker castes have evolved in social insects and how they are maintained have long been central topics in evolutionary biology. With the advance of kin selection theory, insect societies, in particular those of haplodiploid bees, ants, and wasps, have become highly suitable model systems for investigating the details of social evolution and recently also how within-group conflicts are resolved. Because insect societies typically do not consist of clones, conflicts among nestmates arise, for example about the partitioning of reproduction and the allocation of resources towards male and female sexuals. Variation in relatedness among group members therefore appears to have a profound influence on the social structure of groups. However, insect societies appear to be remarkably robust against such variation: division of labor and task allocation are often organized in more or less the same way in societies with high as in those with very low nestmate relatedness. To explain the discrepancy between predictions from kin structure and empirical data, it was suggested that constraints—such as the lack of power or information—prevent individuals from pursuing their own selfish interests. Applying a multilevel selection approach shows that these constraints are in fact group-level adaptation preventing or resolving intracolonial conflict. The mechanisms of conflict resolution in insect societies are similar to those at other levels in the biological hierarchy (e.g., in the genome or multicellular organisms): alignment of interests, fair lottery, and social control. Insect societies can thus be regarded as a level of selection with novelties that provide benefits beyond the scope of a solitary life. Therefore, relatedness is less important for the maintenance of insect societies, although it played a fundamental role in their evolution.Dedicated to Prof. Ernst Mayr     

A survey of DNA methylation across social insect species, life stages, and castes reveals abundant and caste-associated methylation in a primitively social wasp

DNA methylation plays an important role in the epigenetic control of developmental and behavioral plasticity, with connections to the generation of striking phenotypic differences between castes (larger, reproductive queens and smaller, non-reproductive workers) in honeybees and ants. Here, we provide the first comparative investigation of caste- and life stage-associated DNA methylation in several species of bees and vespid wasps displaying different levels of social organization. Our results reveal moderate levels of DNA methylation in most bees and wasps, with no clear relationship to the level of sociality. Strikingly, primitively social Polistes dominula paper wasps show unusually high overall DNA methylation and caste-related differences in site-specific methylation. These results suggest DNA methylation may play a role in the regulation of behavioral and physiological differences in primitively social species with more flexible caste differences.     

Variation of foraging rate and wing loading, but not resting metabolic rate scaling, of insect pollinators

Morphological, physiological and behavioural variation with body size (i.e. scaling) may affect costs of living in a particular environment for insects and, ultimately, pollination or foraging success. However, few studies have directly assessed the scaling of these traits at the species level. Using two similar-sized pollinator species (the hawkmoth Macroglossum trochilus and the fly Moegistorhynchus longirostrus), we compare intraspecific scaling relationships of resting metabolic rate (RMR), foraging rate (FR) and wing loading (WL) to address this paucity of data. Scaling of RMR was similar for both taxa although the intercepts for the relationships differed. However, these two species showed variation in WL scaling relationships and fundamentally different FR scaling. For M. longirostrus, FR scaling was positive but non-significantly related to body mass while for M. trochilus FR scaling was negative. This suggests that variation in FR and WL, but not RMR scaling, among these flies and hawkmoths may impose significant energetic costs which could affect animal–plant interactions in the wild.     

Tandem carrying,a new foraging strategy in ants: description,function, and adaptive significance relative to other described foraging strategies

An important aspect of social insect biology lies in the expression of collective foraging strategies developed to exploit food. In ants, four main types of foraging strategies are typically recognized based on the intensity of recruitment and the importance of chemical communication. Here, we describe a new type of foraging strategy, “tandem carrying”, which is also one of the most simple recruitment strategies, observed in the Ponerinae species Pachycondyla chinensis. Within this strategy, workers are directly carried individually and then released on the food resource by a successful scout. We demonstrate that this recruitment is context dependent and based on the type of food discovered and can be quickly adjusted as food quality changes. We did not detect trail marking by tandem-carrying workers. We conclude by discussing the importance of tandem carrying in an evolutionary context relative to other modes of recruitment in foraging and nest emigration.     

Optimal web investment in sub-optimal foraging conditions

Orb web spiders sit at the centre of their approximately circular webs when waiting for prey and so face many of the same challenges as central-place foragers. Prey value decreases with distance from the hub as a function of prey escape time. The further from the hub that prey are intercepted, the longer it takes a spider to reach them and the greater chance they have of escaping. Several species of orb web spiders build vertically elongated ladder-like orb webs against tree trunks, rather than circular orb webs in the open. As ladder web spiders invest disproportionately more web area further from the hub, it is expected they will experience reduced prey gain per unit area of web investment compared to spiders that build circular webs. We developed a model to investigate how building webs in the space-limited microhabitat on tree trunks influences the optimal size, shape and net prey gain of arboricolous ladder webs. The model suggests that as horizontal space becomes more limited, optimal web shape becomes more elongated, and optimal web area decreases. This change in web geometry results in decreased net prey gain compared to webs built without space constraints. However, when space is limited, spiders can achieve higher net prey gain compared to building typical circular webs in the same limited space. Our model shows how spiders optimise web investment in sub-optimal conditions and can be used to understand foraging investment trade-offs in other central-place foragers faced with constrained foraging arenas.     

Multicomponent floral signals elicit selective foraging in bumblebees

Flower constancy, or the tendency of individual pollinators to visit sequentially a single flower type even when other equally rewarding types are available, has important implications for animal-pollinated plants. Yet, the proximal reason for the behaviour still remains poorly understood. Here I show that bumblebees visiting equally rewarding flowers that differ in size and odour are more flower constant and less efficient (visited fewer flowers per minute) than bees visiting flowers that differ in size only and odour only. These results are consistent with the view that flower constancy in pollinators is related to their inability to perceive, process or recall multicomponent floral signals. I discuss these findings in the context of pollinator behavioural mechanisms and the evolution of floral diversity.     

Prenatal cannibalism in an insect

Host selection and infection strategies of parasitoids often correlate with high parental investment and low numbers of progeny. In this study, we investigate how additional internal mechanisms might shape brood size and fitness of the offspring. Emblemasoma auditrix is a parasitoid fly in which about 38 larvae hatch simultaneously in utero. After host location, a single larva is deposited into the host, where it rapidly develops and pupates after about 5 days. The search for hosts can take several weeks, and during that time, the larvae arrest their development and remain in the first larval instar. Nevertheless, the larvae increase in weight within the uterus, and this growth correlates to a decrease in the number of larvae, although no larvae are deposited. Thus, our data indicate a first case of prenatal cannibalism in an invertebrate with larvae feeding on each other within the uterus of the adult.     

Geographical variation in parasitism shapes larval immune function in a phytophagous insect

Two of the central goals of immunoecology are to understand natural variation in the immune system among populations and to identify those selection pressures that shape immune traits. Maintenance of the immune system can be costly, and both food quality and parasitism selection pressure are factors potentially driving immunocompetence. In tritrophic interactions involving phytophagous insects, host plants, and natural enemies, the immunocompetence of phytophagous insects is constrained by selective forces from both the host plants and the natural enemies. Here, we assessed the roles of host plants and natural enemies as selective pressures on immune variation among natural populations of Lobesia botrana. Our results showed marked geographical variation in immune defenses and parasitism among different natural populations. Larval immune functions were dependent of the host plant quality and were positively correlated to parasitism, suggesting that parasitoids select for greater investment into immunity in moth. Furthermore, investment in immune defense was negatively correlated with body size, suggesting that it is metabolically expensive. The findings emphasize the roles of host plants and parasitoids as selective forces shaping host immune functions in natural conditions. We argue that kinds of study are central to understanding natural variations in immune functions, and the selective forces beyond.     

Chemical compounds of the foraging recruitment pheromone in bumblebees

When the frenzied and irregular food-recruitment dances of bumblebees were first discovered, it was thought that they might represent an evolutionary prototype to the honeybee waggle dance. It later emerged that the primary function of the bumblebee dance was the distribution of an alerting pheromone. Here, we identify the chemical compounds of the bumblebee recruitment pheromone and their behaviour effects. The presence of two monoterpenes and one sesquiterpene (eucalyptol, ocimene and farnesol) in the nest airspace and in the tergal glands increases strongly during foraging. Of these, eucalyptol has the strongest recruitment effect when a bee nest is experimentally exposed to it. Since honeybees use terpenes for marking food sources rather than recruiting foragers inside the nest, this suggests independent evolutionary roots of food recruitment in these two groups of bees.     

Social learning of an associative foraging task in zebrafish

The zebrafish (Danio rerio) is increasingly becoming an important model species for studies on the genetic and neural mechanisms controlling behaviour and cognition. Here, we utilized a conditioned place preference (CPP) paradigm to study social learning in zebrafish. We tested whether social interactions with conditioned demonstrators enhance the ability of focal naïve individuals to learn an associative foraging task. We found that the presence of conditioned demonstrators improved focal fish foraging behaviour through the process of social transmission, whereas the presence of inexperienced demonstrators interfered with the learning of the control focal fish. Our results indicate that zebrafish use social learning for finding food and that this CPP paradigm is an efficient assay to study social learning and memory in zebrafish.     

Self body-size perception in an insect

Animals negotiating complex environments encounter a wide range of obstacles of different shapes and sizes. It is greatly beneficial for the animal to react to such obstacles in a precise, context-specific manner, in order to avoid harm or even simply to minimize energy expenditure. An essential key challenge is, therefore, an estimation of the animal’s own physical characteristics, such as body size. A further important aspect of self body-size perception (or SBSP) is the need to update it in accordance with changes in the animal’s size and proportions. Despite the major role of SBSP in functional behavior, little is known about if and how it is mediated. Here, we demonstrate that insects are also capable of self perception of body size and that this is a vital factor in allowing them to adjust their behavior following the sudden and dramatic growth associated with periodic molting. We reveal that locusts’ SBSP is strongly correlated with their body size. However, we show that the dramatic change in size accompanying adult emergence is not sufficient to create a new and updated SBSP. Rather, this is created and then consolidated only following the individuals’ experience and interaction with the physical environment. Behavioral or pharmacological manipulations can both result in maintenance of the old larval SBSP. Our results emphasize the importance of learning and memory-related processes in the development and update of SBSP, and highlight the advantage of insects as good models for a detailed study on the neurobiological and molecular aspects of SBSP.     

Growth and social behavior in a cichlid fish are affected by social rearing environment and kinship

Living in groups is a widespread phenomenon in many animal taxa. The reduction of predation risk is thought to be an important cause for the formation of groups. Consequently, grouping behavior is particularly pronounced during vulnerable life stages, i.e., as juveniles. However, group living does not only provide benefits but also imposes costs on group members, e.g., increased competition for food. Thus, benefits of grouping behavior might not be evident when predation risk is absent. The adaptive significance of living and also developing in a group independent from predation risk has received relatively little attention although this might have important implications on the evolution and maintenance of group living. The first aim of the present study was to examine whether the social environment affects juvenile performance in the cichlid fish Pelvicachromis taeniatus and, secondly, whether kinship affects social behavior. Kin selection theory predicts benefits from grouping with kin. Here, we demonstrate that juveniles reared in a group grow on average faster compared to juveniles reared in isolation under standardized laboratory conditions without predation risk. Furthermore, we found significant differences in social behavior between juveniles reared in a group and reared in isolation. Fish reared in isolation were significantly more aggressive and less willing to shoal than group-reared fish. As expected, genetic relatedness influenced social behavior in group-reared fish as well: dyads of juveniles consisting of kin showed increased group cohesiveness compared to non-kin dyads. We discuss the potential benefits of group living in general and living with kin in particular.