Social life results in social stress protection: a novel concept to explain individual life-history patterns in social insects.

Resistance to and avoidance of stress slow aging and confer increased longevity in numerous organisms. Honey bees and other superorganismal social insects have two main advantages over solitary species to avoid or resist stress: individuals can directly help each other by resource or information transfer, and they can cooperatively control their environment. These benefits have been recognised in the context of pathogen and parasite stress as the concept of social immunity, which has been extensively studied. However, we argue that social immunity is only a special case of a general concept that we define here as social stress protection to include group-level defences against all biotic and abiotic stressors. We reason that social stress protection may have allowed the evolution of reduced individual-level defences and individual life-history optimization, including the exceptional aging plasticity of many social insects. We describe major categories of stress and how a colonial lifestyle may protect social insects, particularly against temporary peaks of extreme stress. We use the honey bee (Apis mellifera L.) to illustrate how patterns of life expectancy may be explained by social stress protection and how modern beekeeping practices can disrupt social stress protection. We conclude that the broad concept of social stress protection requires rigorous empirical testing because it may have implications for our general understanding of social evolution and specifically for improving honey bee health.

How honeybees respond to heat stress from the individual to colony level.

A honey bee colony functions as an integrated collective, with individuals coordinating their behaviour to adapt and respond to unexpected disturbances. Nest homeostasis is critical for colony function; when ambient temperatures increase, individuals switch to thermoregulatory roles to cool the nest, such as fanning and water collection. While prior work has focused on bees engaged in specific behaviours, less is known about how responses are coordinated at the colony level, and how previous tasks predict behavioural changes during a heat stress. Using BeesBook automated tracking, we follow thousands of individuals during an experimentally induced heat stress, and analyse their behavioural changes from the individual to colony level. We show that heat stress causes an overall increase in activity levels and a spatial reorganization of bees away from the brood area. Using a generalized framework to analyse individual behaviour, we find that individuals differ in their response to heat stress, which depends on their prior behaviour and correlates with age. Examining the correlation of behavioural metrics over time suggests that heat stress perturbation does not have a long-lasting effect on an individual's future behaviour. These results demonstrate how thousands of individuals within a colony change their behaviour to achieve a coordinated response to an environmental disturbance.

Selective enrichment of founding reproductive microbiomes allows extensive vertical transmission in a fungus-farming termite.

Mutualistic coevolution can be mediated by vertical transmission of symbionts between host generations. Termites host complex gut bacterial communities with evolutionary histories indicative of mixed-mode transmission. Here, we document that vertical transmission of gut bacterial strains is congruent across parent to offspring colonies in four pedigrees of the fungus-farming termite Macrotermes natalensis. We show that 44% of the offspring colony microbiome, including more than 80 bacterial genera and pedigree-specific strains, are consistently inherited. We go on to demonstrate that this is achieved because colony-founding reproductives are selectively enriched with a set of non-random, environmentally sensitive and termite-specific gut microbes from their colonies of origin. These symbionts transfer to offspring colony workers with high fidelity, after which priority effects appear to influence the composition of the establishing microbiome. Termite reproductives thus secure transmission of complex communities of specific, co-evolved microbes that are critical to their offspring colonies. Extensive yet imperfect inheritance implies that the maturing colony benefits from acquiring environmental microbes to complement combinations of termite, fungus and vertically transmitted microbes; a mode of transmission that is emerging as a prevailing strategy for hosts to assemble complex adaptive microbiomes.

Manipulating nest architecture reveals three-dimensional building strategies and colony resilience in honeybees.

Form follows function throughout the development of an organism. This principle should apply beyond the organism to the nests they build, but empirical studies are lacking. Honeybees provide a uniquely suited system to study nest form and function throughout development because we can image the three-dimensional structure repeatedly and non-destructively. Here, we tracked nest-wide comb growth in six colonies over 45 days (control colonies) and found that colonies have a stereotypical process of development that maintains a spheroid nest shape. To experimentally test if nest structure is important for colony function, we shuffled the nests of an additional six colonies, weekly rearranging the comb positions and orientations (shuffled colonies). Surprisingly, we found no differences between control and shuffled colonies in multiple colony performance metrics-worker population, comb area, hive weight and nest temperature. However, using predictive modelling to examine how workers allocate comb to expand their nests, we show that shuffled colonies compensate for these disruptions by accounting for the three-dimensional structure to reconnect their nest. This suggests that nest architecture is more flexible than previously thought, and that superorganisms have mechanisms to compensate for drastic architectural perturbations and maintain colony function.

Queens control caste allocation in the ant Cardiocondyla obscurior.

Social insect queens and workers can engage in conflict over reproductive allocation when they have different fitness optima. Here, we show that queens have control over queen-worker caste allocation in the ant Cardiocondyla obscurior, a species in which workers lack reproductive organs. We describe crystalline deposits that distinguish castes from the egg stage onwards, providing the first report of a discrete trait that can be used to identify ant caste throughout pre-imaginal development. The comparison of queen and worker-destined eggs and larvae revealed size and weight differences in late development, but no discernible differences in traits that may be used in social interactions, including hair morphology and cuticular odours. In line with a lack of caste-specific traits, adult workers treated developing queens and workers indiscriminately. Together with previous studies demonstrating queen control over sex allocation, these results show that queens control reproductive allocation in C. obscurior and suggest that the fitness interests of colony members are aligned to optimize resource allocation in this ant.

Testing the human superorganism approach to morality.

Current theories in moral psychology do not agree about the kinds and range of offenses that people should moralize. In this study, a new approach to defining the moral domain, Human Superorganism Theory (HSoT), is presented and tested. HSoT proposes that the primary function of moral action is the suppression of cheaters in the unusually large societies recently established by our species (i.e., human 'superorganisms'). It suggests that a broad range of moral concerns exist beyond traditional notions of harm and fairness, including actions that inhibit functions such as group-level social control, physical and social structuring, reproduction, communication, signaling and memory. Roughly 80,000 respondents completed a web-based experiment hosted by the British Broadcasting Corporation, which elicited a suite of responses to characteristics of a set of 33 short scenarios representing the areas identified by the HSoT perspective. Results indicate that all 13 superorganism functions are moralized, while violations of scenarios falling outside this area (social customs and individual decisions) are not. Several hypotheses derived specifically from HSoT were also supported. Given this evidence, we believe this new approach to defining a broader moral domain has implications for fields ranging from psychology to legal theory.

The economic superorganism in the complexity of evolution.

The transition to grain agriculture restructured human societies, creating a new whole, an economic superorganism. Homo sapiens became expansionary, structurally interdependent in material life, and a duality between them and Earth was created that had not previously existed. Yet H. sapiens are not the only species to make the transition to agriculture. Cross-species comparisons create an opening for a movement toward a focus on the universal and powerful agricultural system as a unique expression of the evolution of species cooperation. This shifts the focus around human social evolution away from culture and toward the formation and power of the economic system that took hold with the cultivation of annual grains. The basic structure and dynamic to economic life that began with grain agriculture has endured for 10 000 years and the duality between humans and Earth established therein is now reaching an apogee with the spectre of climate change and the mass extinction of other species on Earth. In this light, the questions emerge: Is the agricultural revolution an evolutionary transition adequately captured in existing frameworks of human social evolution? Is the human capacity for culture sufficient to override the power and dynamic of the economic superorganism? This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.

Phenoptosis and the Various Types of Natural Selection.

In the first description of evolution, the fundamental mechanism is the natural selection favoring the individuals best suited for survival and reproduction (selection at the individual level or classical Darwinian selection). However, this is a very reductive description of natural selection that does not consider or explain a long series of known phenomena, including those in which an individual sacrifices or jeopardizes his life on the basis of genetically determined mechanisms (i.e., phenoptosis). In fact, in addition to (i) selection at the individual level, it is essential to consider other types of natural selection such as those concerning: (ii) kin selection and some related forms of group selection; (iii) the interactions between the innumerable species that constitute a holobiont; (iv) the origin of the eukaryotic cell from prokaryotic organisms; (v) the origin of multicellular eukaryotic organisms from unicellular organisms; (vi) eusociality (e.g., in many species of ants, bees, termites); (vii) selection at the level of single genes, or groups of genes; (viii) the interactions between individuals (or more precisely their holobionts) of the innumerable species that make up an ecosystem. These forms of natural selection, which are all effects and not violations of the classical Darwinian selection, also show how concepts as life, species, individual, and phenoptosis are somewhat not entirely defined and somehow arbitrary. Furthermore, the idea of organisms selected on the basis of their survival and reproduction capabilities is intertwined with that of organisms also selected on the basis of their ability to cooperate and interact, even by losing their lives or their distinct identities.

Social complexity and brain evolution: insights from ant neuroarchitecture and genomics.

Brain evolution is hypothesized to be driven by requirements to adaptively respond to environmental cues and social signals. Diverse models describe how sociality may have influenced eusocial insect-brain evolution, but specific impacts of social organization and other selective forces on brain architecture have been difficult to distinguish. Here, we evaluate predictions derived from and/or inferences made by models of social organization concerning the effects of individual and collective behavior on brain size, structure, and function using results of neuroanatomical and genomic studies. In contrast to the predictions of some models, we find that worker brains in socially complex species have great behavioral and cognitive capacity. We also find that colony size, the evolution of worker physical castes, and task specialization affect brain size and mosaicism, supporting the idea that sensory, processing and motor requirements for behavioral performance select for adaptive allometries of functionally specialized brain centers. We review available transcriptomic and comparative genomic studies seeking to elucidate the molecular pathways functionally associated with social life and the genetic changes that occurred during the evolution of social complexity. We discuss ways forward, using comparative neuroanatomy, transcriptomics, and comparative genomics, to distinguish among multiple alternative explanations for the relationship between the evolution of neural systems and social complexity.

Positive Eusocial Impacts on Ants by Taurine Derivatives.

The present study is to investigate potential eusocial effects on ants from treatment of taurine or its derivatives: galactose-taurine (GT) or xylose-taurine (XT). Japanese carpenter ants (Camponotus japonicus) were maintained on taurine-supplemented diets, and their performance was evaluated according to arbitrary eusocial indexes. Four classes of criteria were employed: establishment of residence chambers, survival at severe conditions, cooperative defense index (CDI), and population size. Taurine or its derivatives were administered orally in 0.1 mM sucrose solution. When fed with taurine or taurine derivatives, ants built more chambers than the non-fed control. Among the taurine groups, the XT-fed group showed the highest number of chambers. Differences in survivorship were obvious between the control and taurine-fed groups at the extreme conditions of light exposure and high temperature. More ants survived when fed with taurine or its derivatives. The taurine-supplemented groups took less time to organize a defense form than the control. The XT-fed group showed a high level of CDI which refer to the willingness to participate in defense against a foreign queen. The taurine-fed group sustained higher total numbers of ants. The XT-fed groups showed a 15% increase in the number of workers and an 11% increase in the number of eggs. The taurine-fed ants positively responded according to the eusocial vitality indexes, especially when fed with XT. In summary, these results show that ants respond more like superorganisms when treated with XT among taurine or its two derivatives.

Low-cost sample preservation methods for high-throughput processing of rumen microbiomes.

BACKGROUND: The use of rumen microbial community (RMC) profiles to predict methane emissions has driven interest in ruminal DNA preservation and extraction protocols that can be processed cheaply while also maintaining or improving DNA quality for RMC profiling. Our standard approach for preserving rumen samples, as defined in the Global Rumen Census (GRC), requires time-consuming pre-processing steps of freeze drying and grinding prior to international transportation and DNA extraction. This impedes researchers unable to access sufficient funding or infrastructure. To circumvent these pre-processing steps, we investigated three methods of preserving rumen samples for subsequent DNA extraction, based on existing lysis buffers Tris-NaCl-EDTA-SDS (TNx2) and guanidine hydrochloride (GHx2), or 100% ethanol. RESULTS: Rumen samples were collected via stomach intubation from 151 sheep at two time-points 2 weeks apart. Each sample was separated into four subsamples and preserved using the three preservation methods and the GRC method (n = 4 × 302). DNA was extracted and sequenced using Restriction Enzyme-Reduced Representation Sequencing to generate RMC profiles. Differences in DNA yield, quality and integrity, and sequencing metrics were observed across the methods (p < 0.0001). Ethanol exhibited poorer quality DNA (A260/A230 < 2) and more failed samples compared to the other methods. Samples preserved using the GRC method had smaller relative abundances in gram-negative genera Anaerovibrio, Bacteroides, Prevotella, Selenomonas, and Succiniclasticum, but larger relative abundances in the majority of 56 additional genera compared to TNx2 and GHx2. However, log10 relative abundances across all genera and time-points for TNx2 and GHx2 were on average consistent (R2 > 0.99) but slightly more variable compared to the GRC method. Relative abundances were moderately to highly correlated (0.68 ± 0.13) between methods for samples collected within a time-point, which was greater than the average correlation (0.17 ± 0.11) between time-points within a preservation method. CONCLUSIONS: The two modified lysis buffers solutions (TNx2 and GHx2) proposed in this study were shown to be viable alternatives to the GRC method for RMC profiling in sheep. Use of these preservative solutions reduces cost and improves throughput associated with processing and sequencing ruminal samples. This development could significantly advance implementation of RMC profiles as a tool for breeding ruminant livestock.

Eusociality and the Evolution of Aging in Superorganisms.

AbstractEusocial insects-ants, bees, wasps, and termites-are being recognized as model organisms to unravel the evolutionary paradox of aging for two reasons: (1) queens (and kings, in termites) of social insects outlive similarly sized solitary insects by up to several orders of magnitude and (2) all eusocial taxa show a divergence of long queen and shorter worker life spans, despite their shared genomes and even under risk-free laboratory environments. Traditionally, these observations have been explained by invoking the classical evolutionary aging theory: well-protected inside their nests, queens are much less exposed to external hazards than foraging workers, and this provides natural selection the opportunity to favor queens that perform well at advanced ages. Although quite plausible, these verbal arguments have not been backed up by mathematical analysis. Here, for the first time, we provide quantitative models for the evolution of caste-specific aging patterns. We show that caste-specific mortality risks are in general neither sufficient nor necessary to explain the evolutionary divergence in life span between queens and workers and the extraordinary queen life spans. Reproductive monopolization and the delayed production of sexual offspring in highly social colonies lead natural selection to inherently favor queens that live much longer than workers, even when exposed to the same external hazards. Factors that reduce a colony's reproductive skew, such as polygyny and worker reproduction, tend to reduce the evolutionary divergence in life span between queens and workers. Caste-specific extrinsic hazards also affect life span divergence, but to a much smaller extent than reproductive monopolization.

Gaia as Solaris: An Alternative Default Evolutionary Trajectory.

Now that we know that Earth-like planets are ubiquitous in the universe, as well as that most of them are much older than the Earth, it is justified to ask to what extent evolutionary outcomes on other such planets are similar, or indeed commensurable, to the outcomes we perceive around us. In order to assess the degree of specialty or mediocrity of our trajectory of biospheric evolution, we need to take into account recent advances in theoretical astrobiology, in particular (i) establishing the history of habitable planets' formation in the Galaxy, and (ii) understanding the crucial importance of "Gaian" feedback loops and temporal windows for the interaction of early life with its physical environment. Hereby we consider an alternative macroevolutionary pathway that may result in tight functional integration of all sub-planetary ecosystems, eventually giving rise to a true superorganism at the biospheric level. The blueprint for a possible outcome of this scenario has been masterfully provided by the great Polish novelist Stanislaw Lem in his 1961 novel Solaris. In fact, Solaris offers such a persuasive and powerful case for an "extremely strong" Gaia hypothesis that it is, arguably, high time to investigate it in a discursive astrobiological and philosophical context. In addition to novel predictions in the domain of potentially detectable biosignatures, some additional cognitive and heuristic benefits of studying such extreme cases of functional integration are briefly discussed.

My road to the ants: A model clade for eco-evo-devo.

This chapter is the story of how I pioneered ants as a system for studying eco-evo-devo, a field that integrates developmental biology with ecology and evolutionary biology. One aim of eco-evo-devo is to understand how the interactions between genes and their environments during development facilitates the origin and evolution of novel phenotypes. In a series of six parts, I review some of the key discoveries from my lab on how novel worker caste systems in ants--soldiers and supersoldiers--originated and evolved. I also discuss some of the ideas that emerged from these discoveries, including the role that polyphenisms, hidden developmental potentials, and rudimentary organs play in facilitating developmental and evolutionary change. As superorganisms, I argue that ants are uniquely positioned to reveal types of variation that are often difficult to observe in nature. In doing so, they have the potential to transform our view of biology and provide new perspectives in medicine, agriculture, and biodiversity conservation. With my story I hope to inspire the next generation of biologists to continue exploring the unknown regions of phenotypic space to solve some of our most pressing societal challenges.

Responsiveness to inhibitory signals changes as a function of colony size in honeybees (Apis mellifera).

Biological collectives, like honeybee colonies, can make intelligent decisions and robustly adapt to changing conditions via intricate systems of excitatory and inhibitory signals. In this study, we explore the role of behavioural plasticity and its relationship to network size by manipulating honeybee colony exposure to an artificial inhibitory signal. As predicted, inhibition was strongest in large colonies and weakest in small colonies. This is ecologically relevant for honeybees, for which reduced inhibitory effects may increase robustness in small colonies that must maintain a minimum level of foraging and food stores. We discuss evidence for size-dependent plasticity in other types of biological networks.

Microbiome First Medicine in Health and Safety.

Microbiome First Medicine is a suggested 21st century healthcare paradigm that prioritizes the entire human, the human superorganism, beginning with the microbiome. To date, much of medicine has protected and treated patients as if they were a single species. This has resulted in unintended damage to the microbiome and an epidemic of chronic disorders [e.g., noncommunicable diseases and conditions (NCDs)]. Along with NCDs came loss of colonization resistance, increased susceptibility to infectious diseases, and increasing multimorbidity and polypharmacy over the life course. To move toward sustainable healthcare, the human microbiome needs to be front and center. This paper presents microbiome-human physiology from the view of systems biology regulation. It also details the ongoing NCD epidemic including the role of existing drugs and other factors that damage the human microbiome. Examples are provided for two entryway NCDs, asthma and obesity, regarding their extensive network of comorbid NCDs. Finally, the challenges of ensuring safety for the microbiome are detailed. Under Microbiome-First Medicine and considering the importance of keystone bacteria and critical windows of development, changes in even a few microbiota-prioritized medical decisions could make a significant difference in health across the life course.

Interactive brains, social minds: Neural and physiological mechanisms of interpersonal action coordination.

It is now widely accepted that inter-brain synchronization is an important and inevitable mechanism of interpersonal action coordination and social interaction behavior. This review of the current literature focuses first on the forward model for interpersonal action coordination and functional system theory for biological systems, two broadly similar concepts for adaptive system behavior. Further, we review interacting-brain and/or hyper-brain dynamics studies, to show the interplay between intra- and inter-brain connectivity resulting in hyper-brain network structure and network topology dynamics, and consider the functioning of interacting brains as a superordinate system. The concept of a superordinate system, or superorganism, is then evaluated with respect to neuronal and physiological systems group dynamics, which show further accompanying mechanisms of interpersonal interaction. We note that fundamental problems need to be resolved to better understand the neural mechanisms of interpersonal action coordination.

Imperfect comb construction reveals the architectural abilities of honeybees.

Honeybees are renowned for their perfectly hexagonal honeycomb, hailed as the pinnacle of biological architecture for its ability to maximize storage area while minimizing building material. However, in natural nests, workers must regularly transition between different cell sizes, merge inconsistent combs, and optimize construction in constrained geometries. These spatial obstacles pose challenges to workers building perfect hexagons, but it is unknown to what extent workers act as architects versus simple automatons during these irregular building scenarios. Using automated image analysis to extract the irregularities in natural comb building, we show that some building configurations are more difficult for the bees than others, and that workers overcome these challenges using a combination of building techniques, such as: intermediate-sized cells, regular motifs of irregular shapes, and gradual modifications of cell tilt. Remarkably, by anticipating these building challenges, workers achieve high-quality merges using limited local sensing, on par with analytical models that require global optimization. Unlike automatons building perfectly replicated hexagons, these building irregularities showcase the active role that workers take in shaping their nest and the true architectural abilities of honeybees.

Groups as organisms: Implications for therapy and training.

The intellectual tradition of individualism treats the individual person as the fundamental unit of analysis and reduces all things social to the motives and actions of individuals. Most methods in clinical psychology are influenced by individualism and therefore treat the individual as the primary object of therapy/training, even when recognizing the importance of nurturing social relationships for individual wellbeing. Multilevel selection theory offers an alternative to individualism in which individuals become part of something larger than themselves that qualifies as an organism in its own right. Seeing individuals as parts of social organisms provides a new perspective with numerous implications for improving wellbeing at all scales, from individuals to the planet.

Emigrating Together but Not Establishing Together: A Cockroach Rides Ants and Leaves.

AbstractSymbionts of ant colonies can hitchhike on winged ant reproductives (alates) during colony nuptial flights. Attaphila fungicola Wheeler, a miniature cockroach that lives in the nests of Texas leaf-cutter ants (Atta texana Buckley), hitchhikes on female alates (winged queens). Hitchhiking roaches are presumably vertically transmitted from leaf-cutter parent colonies to daughter colonies, remaining with female alates as they transition into foundresses (workerless queens); however, foundresses have limited resources and high mortality rates. Rather than remaining with foundresses likely to die (vertical transmission), roaches might abandon them during dispersal to infect higher-quality later stages of colony development (female alate-vectored transmission). In field experiments, I find evidence for female alate-vectored transmission and discover that roaches use a second hitchhiking step (riding foraged plant material) to infect established colonies. This work reveals a novel relationship between host dispersal and symbiont transmission and shows that colony development can be an important selection pressure on transmission.