Social Insects Research Articles

Stingless bee foragers experience more thermally stressful microclimates and have wider thermal tolerance breadths than other worker subcastes

IntroductionThe current state of anthropogenic climate change is particularly concerning for tropical insects, species predicted to be the most negatively affected. Researching climatic tolerance in social insects is challenging because adaptations exist at both individual and societal levels. Division of labor research helps to bridge the gap between our understanding of these adaptations at different scales, which is important because social insects comprise a tremendous portion of global animal biomass, biodiversity, and ecosystem services. Considering how individual physiologies construct group-level adaptations can improve climate change impact assessments for social species. Tetragonisca angustula is a neotropical stingless bee species that exhibits high worker subcaste specialization with a morphologically distinct soldier caste.MethodsWe used this species to investigate 1) whether age- and size-differentiated subcastes differ in thermal tolerance, 2) which worker subcaste operates closest to their thermal limits, and 3) the extent to which this species selects active foraging times to offset thermal stress. We measured the thermal tolerance (CTmax and CTmin) of small-bodied foragers and two soldier subcastes (hovering guards and standing guards) in T. angustula.Results and discussionDespite body size differences between foragers and guards, no differences in the upper or lower thermal limits were observed. However, the average thermal tolerance breadth of foragers was significantly larger than that of guards, and foraging sites were more thermally variable than nest sites, supporting the Climatic Variability Hypothesis at a microclimate scale and in the context of division of labor. Warming tolerance was significantly lower among small-bodied foragers compared to hovering and standing guards. The magnitude of warming tolerances indicated low risk of imminent climate change impacts in this environment but suggests that increasing temperatures and heatwave prevalence may cause foragers to meet their upper thermal limits before other subcastes. Foraging occurred at a narrower range of temperatures than would challenge critical temperatures, with higher morning activity. Directionally increasing temperatures will likely confine these preferred foraging temperatures to a narrower time window. Further study is needed to elucidate how foragers may shift times of activity in response to anthropogenic warming, but changing climates may impact plant pollination rates in natural and agricultural systems.

HIVE TEMPERATURE REGULATION BY HONEYBEES IN RESPONSE TO EXTREME CONDITIONS

Honeybees are considered the primary pollinators of agricultural crops. However, climate change, pesticide use, disease transmission and pests all have an impact on their survival. Temperature is an important consideration, especially when bees are subjected to harsh conditions as a result of the effort required to regulate them within their hives. The brood chamber should be kept between 33 and 35 °C. The recognized temperature thresholds are 6 and 38 °C; deviations above or below these values cause metabolic damage in honeybees; the larger the difference, the greater the stress. These eusocial insects have developed thermoregulating mechanisms in response to adverse environmental conditions; the colony compensates for this difference by either fanning their wings to create air circulation and cause evaporative cooling or raising the temperature by generating endothermic heat to raise the temperature of the breeding chamber. This review brings together the most important and updated references on how to improve colony thermoregulation and its relationship to climate change.

Colony identity clues for Syntermes grandis (Blattodea: Termitidae) individuals using near-infrared spectroscopy and PLS-DA approach.

Termites are social insects with high species diversity in tropical ecosystems. Multivariate analysis with near-infrared spectroscopy (NIRS) and data interpretation can separate social insects belonging to different colonies of the same species. The objective of this study was to propose the use of discriminant analysis by partial least squares (PLS-DA) combined with NIRS to identify the colonial origin of the Syntermes grandis (Rambur, 1842) (Blattodea: Termitidae) in 2 castes. Six ground S. grandis colonies were identified and mapped; 30 workers and 30 soldier termites in each colony were submitted to spectral measurement with NIRS. PLS-DA applied to the termites' spectral absorbance was used to detect a spectral pattern per S. grandis colony by caste. PLS-DA regression with NIRS proved to be an approach with 99.9% accuracy for identifying the colonial origin of S. grandis workers and 98.3% for soldiers. The methodology showed the importance of qualitatively characterizing the colonial phenotypic response of this species. NIRS is a high-precision approach to identifying the colony origin of S. grandis workers and soldiers. The PLS-DA can be used to design ecological field studies to identify colony territorial competition and foraging behavior of subterranean termite species.

Pervasive relaxed selection in termite genomes.

Genetic changes that enabled the evolution of eusociality have long captivated biologists. More recently, attention has focussed on the consequences of eusociality on genome evolution. Studies have reported higher molecular evolutionary rates in eusocial hymenopteran insects compared with their solitary relatives. To investigate the genomic consequences of eusociality in termites, we analysed nine genomes, including newly sequenced genomes from three non-eusocial cockroaches. Using a phylogenomic approach, we found that termite genomes have experienced lower rates of synonymous substitutions than those of cockroaches, possibly as a result of longer generation times. We identified higher rates of non-synonymous substitutions in termite genomes than in cockroach genomes, and identified pervasive relaxed selection in the former (24-31% of the genes analysed) compared with the latter (2-4%). We infer that this is due to reductions in effective population size, rather than gene-specific effects (e.g. indirect selection of caste-biased genes). We found no obvious signature of increased genetic load in termites, and postulate efficient purging of deleterious alleles at the colony level. Additionally, we identified genomic adaptations that may underpin caste differentiation, such as genes involved in post-translational modifications. Our results provide insights into the evolution of termites and the genomic consequences of eusociality more broadly.

Inter-clonal competition over queen succession imposes a cost of parthenogenesis on termite colonies.

In social insect colonies, selfish behaviour due to intracolonial conflict among members can result in colony-level costs despite close relatedness. In certain termite species, queens use asexual reproduction for within-colony queen succession but rely on sexual reproduction for worker and alate production, resulting in multiple half-clones of a single primary queen competing for personal reproduction. Our study demonstrates that competition over asexual queen succession among different clone types leads to the overproduction of parthenogenetic offspring, resulting in the production of dysfunctional parthenogenetic alates. By genotyping the queens of 23 field colonies of Reticulitermes speratus, we found that clone variation in the queen population reduces as colonies develop. Field sampling of alates and primary reproductives of incipient colonies showed that overproduced parthenogenetic offspring develop into alates that have significantly smaller body sizes and much lower survivorship than sexually produced alates. Our results indicate that while the production of earlier and more parthenogenetic eggs is advantageous for winning the competition for personal reproduction, it comes at a great cost to the colony. Thus, this study highlights the evolutionary interplay between individual-level and colony-level selection on parthenogenesis by queens.

Serial founder effects slow range expansion in an invasive social insect

Invasive populations often experience founder effects: a loss of genetic diversity relative to the source population, due to a small number of founders. Even where these founder effects do not impact colonization success, theory predicts they might affect the rate at which invasive populations expand. This is because secondary founder effects are generated at advancing population edges, further reducing local genetic diversity and elevating genetic load. We show that in an expanding invasive population of the Asian honey bee (Apis cerana), genetic diversity is indeed lowest at range edges, including at the complementary sex determiner, csd, a locus that is homozygous-lethal. Consistent with lower local csd diversity, range edge colonies had lower brood viability than colonies in the range centre. Further, simulations of a newly-founded and expanding honey bee population corroborate the spatial patterns in mean colony fitness observed in our empirical data and show that such genetic load at range edges will slow the rate of population expansion.

Using functional decomposition to bridge the design gap between desired emergent multi‐agent‐system resilience and individual agent design

AbstractIncreasing the resilience of modern infrastructure systems is recognized as a priority by both the International Council on Systems Engineering and the National Academy of Engineering. Resilience answers the key stakeholder need for a stable and predictable system by withstanding, adapting to, and recovering from unexpected faults. Increasing resilience in multi‐agent systems is especially challenging because resilience is an emergent system‐level property rather than the sum of individual agent functions. This paper uses biological systems as a source of inspiration for resilient functions, examining the central question How can biologically inspired design be used to increase the emergent property of resilience in multi‐agent systems? The paper uses functional decomposition to break down the individual functions that result in resilience and transfer the properties to generalized systems. Accordingly, the central hypothesis examined in this article is If functional decomposition is performed on eusocial insect colonies, then generalizable approaches to increase the emergent property of multi‐agent system resilience can be identified. The results provide two contributions. The first contribution is the identification of six general functions based on eusocial insect behavior that influence resilience. The second contribution is a description of the process of identifying and transferring insect behaviors into generalized design‐for‐resilience guidance. To support these contributions, a case study applies biologically inspired functions to an emergency power service system and proposes tactics for the power system to improve its resilience. Thus, this article provides a key step towards our goal of using biologically inspired design to influence the emergent property of resilience in multi‐agent systems.

Unique spatially and temporary-regulated/sex-specific expression of a long ncRNA, Nb-1, suggesting its pleiotropic functions associated with honey bee lifecycle

Honey bees are social insects, and each colony member has unique morphological and physiological traits associated with their social tasks. Previously, we identified a long non-coding RNA from honey bees, termed Nb-1, whose expression in the brain decreases associated with the age-polyethism of workers and is detected in some neurosecretory cells and octopaminergic neurons, suggesting its role in the regulation of worker labor transition. Herein, we investigated its spatially and temporary-regulated/sex-specific expression. Nb-1 was expressed as an abundant maternal RNA during oogenesis and embryogenesis in both sexes. In addition, Nb-1 was expressed preferentially in the proliferating neuroblasts of the mushroom bodies (a higher-order center of the insect brain) in the pupal brains, suggesting its role in embryogenesis and mushroom body development. On the contrary, Nb-1 was expressed in a drone-specific manner in the pupal and adult retina, suggesting its role in the drone visual development and/or sense. Subcellular localization of Nb-1 in the brain during development differed depending on the cell type. Considering that Nb-1 is conserved only in Apidae, our findings suggest that Nb-1 potentially has pleiotropic functions in the expression of multiple developmental, behavioral, and physiological traits, which are closely associated with the honey bee lifecycle.

Optimal fissioning strategies of social insects with respect to colony dynamics and nest founding probability

Social insects demonstrate two fundamentally different modes of reproduction, independent colony foundation (ICF) by single fertilized queens or dependent colony foundation (DCF) by fissioning of existing colonies into two or several new colonies (swarms). In some species, both reproductive modes occur in parallel. The benefits and disadvantages of DCF vs. ICF have been widely discussed and been subject to empirical studies, but a formal theoretical treatment of the topic is still incomplete. Taking honey bees as example, we provide a resource allocation model of colony dynamics to analyze the ecological conditions under which DCF may be favored over ICF. Using mathematical and numerical methods, we show that it critically depends on the survivorship function linking swarm size to the probability of swarm establishment whether ICF or DCF results in a higher output of surviving new colonies. Because building larger swarms requires larger inter-swarm time intervals, DCF can only be a better strategy if this disadvantage is over-compensated for by a strong size-dependent swarm survivorship and survival of single queens is very low. Colony growth rate has no effect on this decision and the impact of maximum possible colony size is negligible. Further, there is a discontinuity in the optimal swarm size, so that either a swarm size of 1 (ICF) is the best strategy, or emitting swarms of considerable size (DCF). Consequently, a direct evolutionary transition from ICF to DCF appears unlikely and may have been triggered by selective pressures promoting movement of complete nests or distributing single colonies over several nests (polydomy).

Leptanillavoldemort sp. nov., a gracile new species of the hypogaeic ant genus Leptanilla (Hymenoptera, Formicidae) from the Pilbara, with a key to Australian Leptanilla.

The genus Leptanilla Emery, 1870 of the family Formicidae, subfamily Leptanillinae, comprises miniscule, pale, blind ants that are rarely collected and poorly understood due to their hypogaeic (i.e. underground) lifestyles. Here we describe a new Leptanilla species from two workers collected via subterranean scraping in the arid Pilbara region of Western Australia. Leptanillavoldemortsp. nov. is the second leptanilline species documented in Australia after the elusive Leptanillaswani Wheeler, 1932. Workers of L.voldemortsp. nov. display a remarkably gracile morphology characterised by elongated legs, antennae, and mandibles, and they are easily differentiated from other Leptanilla species. We also provide new measurements for L.swani from two workers found proximally to the type locality of L.voldemortsp. nov. A key to the worker caste of Leptanilla species of the Australian continent is presented.

Dynamics of Information Flow and Task Allocation of Social Insect Colonies: Impacts of Spatial Interactions and Task Switching.

Models of social interaction dynamics have been powerful tools for understanding the efficiency of information spread and the robustness of task allocation in social insect colonies. How workers spatially distribute within the colony, or spatial heterogeneity degree (SHD), plays a vital role in contact dynamics, influencing information spread and task allocation. We used agent-based models to explore factors affecting spatial heterogeneity and information flow, including the number of task groups, variation in spatial arrangements, and levels of task switching, to study: (1) the impact of multiple task groups on SHD, contact dynamics, and information spread, and (2) the impact of task switching on SHD and contact dynamics. Both models show a strong linear relationship between the dynamics of SHD and contact dynamics, which exists for different initial conditions. The multiple-task-group model without task switching reveals the impacts of the number and spatial arrangements of task locations on information transmission. The task-switching model allows task-switching with a probability through contact between individuals. The model indicates that the task-switching mechanism enables a dynamical state of task-related spatial fidelity at the individual level. This spatial fidelity can assist the colony in redistributing their workforce, with consequent effects on the dynamics of spatial heterogeneity degree. The spatial fidelity of a task group is the proportion of workers who perform that task and have preferential walking styles toward their task location. Our analysis shows that the task switching rate between two tasks is an exponentially decreasing function of the spatial fidelity and contact rate. Higher spatial fidelity leads to more agents aggregating to task location, reducing contact between groups, thus making task switching more difficult. Our results provide important insights into the mechanisms that generate spatial heterogeneity and deepen our understanding of how spatial heterogeneity impacts task allocation, social interaction, and information spread.

Reproductive Ageing: Unlocking the secrets of reproductive longevity: the potential of social insects.

Social insect queens display both extraordinary longevity and fertility. In this point of view, we describe their distinctive traits that make them useful models for reproductive longevity, holding implications for human health discoveries. Social insects present an extraordinary opportunity as models for reproductive longevity because they challenge the conventional patterns of aging and reproduction seen in other model organisms. Their queens are simultaneously long-lived and highly fecund, and understanding how these traits co-occur may lead to discoveries with important implications for human health.

New Distributional Records of Ants of Genus <i>Crematogaster</i> Lund (Hymenoptera: Formicidae) from India

New locality records and illustrations for five known species viz., Crematogaster biroi Mayr, 1897, C. contemta Mayr, 1879, C. dohrni artifex Mayr, 1879, C. rothneyi Mayr, 1879, and C. subnuda Mayr, 1879 are provided from India. These records expand the area of occurrence and distribution of these species in India. In addition, Crematogaster travancorensis Forel (1902) is redescribed based on the worker caste collected from Pachmarhi, Madhya Pradesh and Ri Bhoi, Meghalaya, India.

Accessory gland protein regulates pairing process and oviposition in the subterranean termite Reticulitermes chinensis after swarming.

Swarming and pairing behaviors are significant to population dispersal of termites. Tandem running is a key process in pairing behavior of dealates to find a mate. Succinylation can lead to significant changes in protein structure and function, which is widely involved in metabolism and behavior regulation in many organisms. However, whether succinylation modification regulates termites' tandem running is currently unknown. In this research, we performed quantitative modified proteomics of the subterranean termite Reticulitermes chinensis Snyder before and after alate swarming. The succinylation levels of accessory gland protein (ACP) were significantly altered after alate swarming. We found that ACP is enriched in male accessory gland and female oocytes of termites. The acetylation and succinylation sites of ACP affected tandem running of dealates. The transcriptome and metabolome analyses of alates injected with ACP and its mutant proteins showed that β-alanine metabolism pathway was the major downstream pathway of ACP. Silencing the significantly differentially expressed genes in the β-alanine metabolic pathway (acyl-CoA dehydrogenase, enoyl-CoA hydratase, 3-hydroxyisobutyrate dehydrogenase, methylmalonate-semialdehyde dehydrogenase) suppressed tandem running and altered oviposition of paired dealates. These findings demonstrate that protein translation modification is an important regulator of tandem running behavior of termites, which implies that the succinylation and acetylation modification sites of ACP could be potential targets for insecticide action. Our research offers a potential approach for developing novel dispersal inhibitors against social insect pests.

Odorant Receptors Expressing and Antennal Lobes Architecture Are Linked to Caste Dimorphism in Asian Honeybee, Apis cerana (Hymenoptera: Apidae).

Insects heavily rely on the olfactory system for food, mating, and predator evasion. However, the caste-related olfactory differences in Apis cerana, a eusocial insect, remain unclear. To explore the peripheral and primary center of the olfactory system link to the caste dimorphism in A. cerana, transcriptome and immunohistochemistry studies on the odorant receptors (ORs) and architecture of antennal lobes (ALs) were performed on different castes. Through transcriptomesis, we found more olfactory receptor genes in queens and workers than in drones, which were further validated by RT-qPCR, indicating caste dimorphism. Meanwhile, ALs structure, including volume, surface area, and the number of glomeruli, demonstrated a close association with caste dimorphism. Particularly, drones had more macroglomeruli possibly for pheromone recognition. Interestingly, we found that the number of ORs and glomeruli ratio was nearly 1:1. Also, the ORs expression distribution pattern was very similar to the distribution of glomeruli volume. Our results suggest the existence of concurrent plasticity in both the peripheral olfactory system and ALs among different castes of A. cerana, highlighting the role of the olfactory system in labor division in insects.

Highly diverse cuticular hydrocarbon profiles but no evidence for aggression towards non-kin in the ambrosia beetle Xyleborinus saxesenii.

Animal societies use nestmate recognition to protect against social cheaters and parasites. In most social insect societies, individuals recognize and exclude any non-nestmates and the roles of cuticular hydrocarbons as recognition cues are well documented. Some ambrosia beetles live in cooperatively breeding societies with farmed fungus cultures that are challenging to establish, but of very high value once established. Hence, social cheaters that sneak into a nest without paying the costs of nest foundation may be selected. Therefore, nestmate recognition is also expected to exist in ambrosia beetles, but so far nobody has investigated this behavior and its underlying mechanisms. Here we studied the ability for nestmate recognition in the cooperatively breeding ambrosia beetle Xyleborinus saxesenii, combining behavioural observations and cuticular hydrocarbon analyses. Laboratory nests of X. saxesenii were exposed to foreign adult females from the same population, another population and another species. Survival as well as the behaviours of the foreign female were observed. The behaviours of the receiving individuals were also observed. We expected that increasing genetic distance would cause increasing distance in chemical profiles and increasing levels of behavioural exclusion and possibly mortality. Chemical profiles differed between populations and appeared as variable as in other highly social insects. However, we found only very little evidence for the behavioural exclusion of foreign individuals. Interpopulation donors left nests at a higher rate than control donors, but neither their behaviours nor the behaviours of receiver individuals within the nest showed any response to the foreign individual in either of the treatments. These results suggest that cuticular hydrocarbon profiles might be used for communication and nestmate recognition, but that behavioural exclusion of non-nestmates is either absent in X. saxesenii or that agonistic encounters are so rare or subtle that they could not be detected by our method. Additional studies are needed to investigate this further.

Ontogeny of superorganisms: Social control of queen specialization in ants

Abstract The functioning of biological systems relies on the cooperation of specialized components and understanding the processes that produce such specialization is a major challenge in biology. Here, we study the ontogeny of biological systems at a new phenotypic level: the superorganisms (i.e. insect societies with specialized individuals). We investigate how founding queens, the earliest developmental stage of ant colonies, transition from expressing behavioural pluripotency to becoming strictly specialized in egg production. We demonstrate that the presence of workers both initiates and maintains this queen specialization, and propose that such a social control of queen behaviour is common in ants and regulated by ancestral mechanisms. These findings contradict the traditional view of social insect queens as being intrinsically specialized in egg production and may reshape our understanding of the division of labour in insect societies. Read the free Plain Language Summary for this article on the Journal blog.

N6-methyladenosine modification of RNA controls dopamine synthesis to influence labour division in ants.

The N6-methyladenosine (m6A) modification of RNA has been reported to remodel gene expression in response to environmental conditions; however, the biological role of m6A in social insects remains largely unknown. In this study, we explored the role of m6A in the division of labour by worker ants (Solenopsis invicta). We first determined the presence of m6A in RNAs from the brains of worker ants and found that m6A methylation dynamics differed between foragers and nurses. Depletion of m6A methyltransferase or chemical suppression of m6A methylation in foragers resulted in a shift to 'nurse-like' behaviours. Specifically, mRNAs of dopamine receptor 1 (Dop1) and dopamine transporter (DAT) were modified by m6A, and their expression increased dopamine levels to promote the behavioural transition from foragers to nurses. The abundance of Dop1 and DAT mRNAs and their stability were reduced by the inhibition of m6A modification caused by the silencing of Mettl3, suggesting that m6A modification in worker ants modulates dopamine synthesis, which regulates labour division. Collectively, our results provide the first example of the epitranscriptomic regulation of labour division in social insects and implicate m6A regulatory mechanism as a potential novel target for controlling red imported fire ants.

Structural variation of ant nests mediates the local distribution and abundance of an associate

AbstractSymbionts form intricate associations with their hosts. They can only establish when potential hosts are present, but in addition, their distribution is often influenced by microhabitat preferences, which may not overlap those of their hosts. This leads to a patchy local distribution of the symbiont, being present with some hosts and absent with others. We studied this effect of microhabitat preferences on symbiont distribution by examining the occurrence and density of the obligately ant‐associated springtail Cyphoderus albinus Nicolet (Collembola: Paronellidae) across a mosaic of ant nests. Nest structure strongly varied both within and between ant species and included sand, dead wood, arboreal and thatch mound nests. We hypothesized that the symbiotic springtail would show the strongest preference for thermoregulated and organic‐rich nests such as thatch mounds. The springtail was found in all thatch mound nests of red wood ants and in all arboreal nests of Lasius fuliginosus (Latreille). A high occurrence (75%) was recorded in the smaller thatch nests of Formica sanguinea Latreille. Lasius, Myrmica and Formica species exhibited variation in nest structures on the ground, establishing nests in both sand and wood. For each of these three host taxa, encountering the springtail was more likely in their wood nests (medium‐to‐high occurrence), than in their sand nests where the occurrence was low. Nest structure did not only impact springtail occurrence, but their densities as well. The densities within thatch nests were much higher than those in other nest types, achieving the highest densities (1148 individuals per litre of nest material) observed for a social insect symbiont. Our findings emphasize that host nests with wood structures and thatch material provide a more favourable habitat for the springtail compared with soil nests. Overall, this study underscores the role of microhabitat variation in the spatial distribution and density of a symbiotic species.

Two new ant species of the genus Leptogenys (Hymenoptera, Formicidae) from Hainan, China, with a key to the known Chinese species.

Two new species of ponerine ants from Hainan Province, China, Leptogenyshainanensissp. nov. and L.zhouisp. nov., are delineated and depicted based on the worker caste. Leptogenyshainanensissp. nov. belongs to the L.leleji species group, with mandibles elongate, slender and curved, lacking a distinct masticatory margin. On the other hand, L.zhouisp. nov. belongs to the L.crassicornis species group, distinguished by its square head, smooth body, mandibles with a dentate masticatory margin, and short antennae. A key to workers for the known species of Leptogenys in China are provided and a map is provided for the newly described species.