Transcriptional and post-transcriptional control of odorant receptor choice in ants.

Insects and mammals have independently evolved odorant receptor genes that are arranged in large genomic tandem arrays. In mammals, each olfactory sensory neuron chooses to express a single receptor in a stochastic process that includes substantial chromatin rearrangements. Here, we show that ants, which have the largest odorant receptor repertoires among insects, employ a different mechanism to regulate gene expression from tandem arrays. Using single-nucleus RNA sequencing, we found that ant olfactory sensory neurons choose different transcription start sites along an array but then produce mRNA from many downstream genes. This can result in transcripts from dozens of receptors being present in a single nucleus. Such rampant receptor co-expression at first seems difficult to reconcile with the narrow tuning of the ant olfactory system. However, RNA fluorescence in situ hybridization showed that only mRNA from the most upstream transcribed odorant receptor seems to reach the cytoplasm where it can be translated into protein, whereas mRNA from downstream receptors gets sequestered in the nucleus. This implies that, despite the extensive co-expression of odorant receptor genes, each olfactory sensory neuron ultimately only produces one or very few functional receptors. Evolution has thus found different molecular solutions in insects and mammals to the convergent challenge of selecting small subsets of receptors from large odorant receptor repertoires.

Larger, more connected societies of ants have a higher prevalence of viruses.

The benefits of cooperative living for foraging, nesting, defence and buffering environmental challenges lead animals with the most highly social lifestyles to dominate many ecosystems. However, living in larger, more highly connected groups should also increase the risks of pathogen exposure and transmission. While over long timescales selective responses could buffer the impacts of potential higher pathogen prevalence, similar processes are unlikely over short timescales. The red fire ant Solenopsis invicta is ideal for measuring the effects of group size on pathogen prevalence because two types of society coexist in this species: smaller single-nest single-queen colonies that are highly aggressive to their neighbours and larger multiple-queen colonies that exchange resources with neighbouring nests. We compare the presence of viruses between these two colony types using metagenomic sequence classification of RNA-sequencing reads. We find that queens from multiple-queen colonies have 8.3-times higher viral load and 1.5-times higher viral diversity than queens from single-queen colonies. This finding characterizes a rarely considered cost of transitions to more highly social living. Furthermore, our results show that highly social invertebrates can harbour many viruses.

Getting older, getting smarter: ontogeny of foraging behaviour in the tropical social wasp Ropalidia marginata.

Desert ants and honey bees start foraging when they are a few days old, and subsequently increase their foraging effort and the amount of foraged food. This could be an optimal strategy for scavenger/gatherer animals inhabiting landscapes with fewer features. However, animals inhabiting cluttered landscapes, especially predatory animals, may require substantial familiarity with foraging landscapes to forage efficiently. They may acquire such spatial familiarity with increasing age/experience, and eventually reduce their foraging effort without compromising on foraging success/efficiency. To check whether this holds for the individually foraging predatory tropical paper-wasp Ropalidia marginata, we recorded the number and duration of all foraging trips, the identity of foraged materials, and the directions of outbound and inbound flights (with respect to the nest) of known-age wasps for three consecutive days from three naturally occurring colonies; thus, we measured behavioural profiles of wasps of various ages, and not from the same wasp throughout its lifespan. Wasps increased their foraging duration rapidly until about 4 weeks of age, during which they rarely brought food, although some wasps brought building material and water. Thereafter, their foraging duration started decreasing. Nevertheless, their foraging success/efficiency in bringing food kept on increasing. With age, wasps developed individual directional preferences for outbound and inbound flights, indicating the development of spatial memory for rewarding sites. Also, the angular difference between their outbound and subsequent inbound flights gradually increased, indicating older wasps may have followed tortuous foraging routes. High investment in early life to acquire familiarity with foraging landscapes and using that later to perform efficient foraging could be an optimal strategy for individually foraging animals inhabiting feature-rich landscapes.

Current indirect fitness and future direct fitness are not incompatible.

In primitively eusocial insects, many individuals function as workers despite being capable of independent reproduction. Such altruistic behaviour is usually explained by the argument that workers gain indirect fitness by helping close genetic relatives. The focus on indirect fitness has left open the question of whether workers are also capable of getting direct fitness in the future in spite of working towards indirect fitness in the present. To investigate this question, we recorded behavioural profiles of all wasps on six naturally occurring nests of Ropalidia marginata, and then isolated all wasps in individual plastic boxes, giving them an opportunity to initiate nests and lay eggs. We found that 41% of the wasps successfully did so. Compared to those that failed to initiate nests, those that did were significantly younger, had significantly higher frequency of self-feeding behaviour on their parent nests but were not different in the levels of work performed in the parent nests. Thus ageing and poor feeding, rather than working for their colonies, constrain individuals for future independent reproduction. Hence, future direct fitness and present work towards gaining indirect fitness are not incompatible, making it easier for worker behaviour to be selected by kin selection or multilevel selection.

Emergence of cooperation and division of labor in the primitively eusocial wasp Ropalidia marginata.

In most primitively eusocial wasps new nests are initiated by a single female or by small groups of females. To study the emergence of division of labor (DOL) among the nest foundresses and to determine its possible effect on nest productivity we maintained newly eclosed females of Ropalidia marginata in small boxes with one, two, or three nestmate wasps of the same age per box. Only one wasp developed her ovaries and laid eggs in each box, while the other wasp(s) built the nest, brought food, and fed larvae, demonstrating the spontaneous emergence of reproductive DOL in the presence of more than one wasp. In nests with three wasps there was also a strong negative correlation between intranidal and extranidal work performed by the two nonreproductive workers, suggesting the spontaneous emergence of nonreproductive DOL; such nonreproductive DOL was absent in nests with two wasps. Both reproductive and nonreproductive DOL were modulated by dominance behavior (DB). In nests with two wasps the egg layer showed significantly more DB than the non-egg layer before nest initiation; in nests with three wasps queens showed significantly more DB than intranidal workers, which in turn showed significantly more DB than extranidal workers. Productivities of nests (as measured by total brood on the day of eclosion of the first adult) initiated by one or two wasps were not different from each other but were significantly lower than that of three wasps. Thus, nonreproductive DOL, and not merely reproductive DOL, is necessary for increase in productivity.

Homing in a tropical social wasp: role of spatial familiarity, motivation and age.

We captured foragers of the tropical social wasp Ropalidia marginata from their nests and displaced them at different distances and directions. Wasps displaced within their probable foraging grounds returned to their nests on the day of release although they oriented randomly upon release; however, wasps fed before release returned sooner, displaying nest-ward orientation. When displaced to places far from their nests, thus expected to be unfamiliar, only a third returned on the day of release showing nest-ward orientation; others oriented randomly and either returned on subsequent days or never. When confined within mosquito-net tents since eclosion and later released to places close to their nests (but unfamiliar), even fed wasps oriented randomly, and only older wasps returned, taking longer time. Thus, contrary to insects inhabiting less-featured landscapes, R. marginata foragers appear to have thorough familiarity with their foraging grounds that enables them to orient and home efficiently after passive displacement. Their initial orientation is, however, determined by an interaction of the information acquired from surrounding landscape and their physiological motivation. With age, they develop skills to home from unfamiliar places. Homing behaviour in insects appears to be influenced by evolutionarily conserved mechanisms and the landscape in which they have evolved.