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.

A modeling framework for adaptive collective defense: crisis response in social-insect colonies.

Living systems, from cells to superorganismic insect colonies, have an organizational boundary between inside and outside and allocate resources to defend it. Whereas the micro-scale dynamics of cell walls can be difficult to study, the adaptive allocation of workers to defense in social-insect colonies is more conspicuous. This is particularly the case for Tetragonisca angustula stingless bees, which combine different defensive mechanisms found across other colonial animals: (1) morphological specialization (distinct soldiers (majors) are produced over weeks); (2) age-based polyethism (young majors transition to guarding tasks over days); and (3) task switching (small workers (minors) replace soldiers within minutes under crisis). To better understand how these timescales of reproduction, development, and behavior integrate to balance defensive demands with other colony needs, we developed a demographic Filippov ODE system to study the effect of these processes on task allocation and colony size. Our results show that colony size peaks at low proportions of majors, but colonies die if minors are too plastic or defensive demands are too high or if there is a high proportion of quickly developing majors. For fast maturation, increasing major production may decrease defenses. This model elucidates the demographic factors constraining collective defense regulation in social insects while also suggesting new explanations for variation in defensive allocation at smaller scales where the mechanisms underlying defensive processes are not easily observable. Moreover, our work helps to establish social insects as model organisms for understanding other systems where the transaction costs for component turnover are nontrivial, as in manufacturing systems and just-in-time supply chains.

Impacts of seasonality and parasitism on honey bee population dynamics.

The honeybee plays an extremely important role in ecosystem stability and diversity and in the production of bee pollinated crops. Honey bees and other pollinators are under threat from the combined effects of nutritional stress, parasitism, pesticides, and climate change that impact the timing, duration, and variability of seasonal events. To understand how parasitism and seasonality influence honey bee colonies separately and interactively, we developed a non-autonomous nonlinear honeybee-parasite interaction differential equation model that incorporates seasonality into the egg-laying rate of the queen. Our theoretical results show that parasitism negatively impacts the honey bee population either by decreasing colony size or destabilizing population dynamics through supercritical or subcritical Hopf-bifurcations depending on conditions. Our bifurcation analysis and simulations suggest that seasonality alone may have positive or negative impacts on the survival of honey bee colonies. More specifically, our study indicates that (1) the timing of the maximum egg-laying rate seems to determine when seasonality has positive or negative impacts; and (2) when the period of seasonality is large it can lead to the colony collapsing. Our study further suggests that the synergistic influences of parasitism and seasonality can lead to complicated dynamics that may positively and negatively impact the honey bee colony's survival. Our work partially uncovers the intrinsic effects of climate change and parasites, which potentially provide essential insights into how best to maintain or improve a honey bee colony's health.

Body mass and cuticular hydrocarbon profiles, but not queen number, underlie worker desiccation resistance in a facultatively polygynous harvester ant (Pogonomyrmex californicus).

As small-bodied terrestrial organisms, insects face severe desiccation risks in arid environments, and these risks are increasing under climate change. Here, we investigate the physiological, chemical, and behavioral mechanisms by which harvester ants, one of the most abundant arid-adapted insect groups, cope with desiccating environmental conditions. We aimed to understand how body size, cuticular hydrocarbon profiles, and queen number impact worker desiccation resistance in the facultatively polygynous harvester ant, Pogonomyrmex californicus. We measured survival at 0% humidity of field-collected worker ants sourced from three closely situated populations within a semi-arid region of southern California. These populations vary in queen number, with one population dominated by multi-queen colonies (primary polygyny), one population dominated by single-queen colonies, and one containing an even mix of single- and multi-queen colonies. We found no effect of population on worker survival in desiccation assays, suggesting that queen number does not influence colony desiccation resistance. Across populations, however, body mass and cuticular hydrocarbon profiles significantly predicted desiccation resistance. Larger-bodied workers survived longer in desiccation assays, emphasizing the importance of reduced surface area-to-volume ratios in maintaining water balance. Additionally, we observed a positive relationship between desiccation resistance and the abundance of n-alkanes, supporting previous work that has linked these high-melting point compounds to improved body water conservation. Together, these results contribute to an emerging model explaining the physiological mechanisms of desiccation resistance in insects.

Seasonal variability in physiology and behavior affect the impact of fungicide exposure on honey bee (Apis mellifera) health.

Honey bee pollination services are of tremendous agricultural and economic importance. Despite this, honey bees and other pollinators face ongoing perils, including population declines due to a variety of environmental stressors. Fungicides may be particularly insidious stressors for pollinators due to their environmental ubiquity and widespread approval for application during crop bloom. The mechanisms by which fungicides affect honey bees are poorly understood and any seasonal variations in their impact are unknown. Here we assess the effects on honey bee colonies of four-week exposure (the approximate duration of the almond pollination season) of a fungicide, Pristine® (25.2% boscalid, 12.8% pyraclostrobin), that has been commonly used for almonds. We exposed colonies to Pristine® in pollen patties placed into the hive, in either summer or fall, and assessed colony brood and worker populations, colony pollen collection and consumption, and worker age of first foraging and longevity. During the summer, Pristine® exposure induced precocious foraging, and reduced worker longevity resulting in smaller colonies. During the fall, Pristine® exposure induced precocious foraging but otherwise had no significant measured effects. During the fall, adult and brood population levels, and pollen consumption and collection, were all much lower, likely due to preparations for winter. Fungicides and other pesticides may often have reduced effects on honey bees during seasons of suppressed colony growth due to bees consuming less pollen and pesticide.

Social Factors in Heat Survival: Multiqueen Desert Ant Colonies Have Higher and More Uniform Heat Tolerance.

AbstractInvestigations of thermally adaptive behavioral phenotypes are critical for both understanding climate as a selective force and predicting global species distributions under climate change conditions. Cooperative nest founding is a common strategy in harsh environments for many species and can enhance growth and competitive advantage, but whether this social strategy has direct effects on thermal tolerance was previously unknown. We examined the effects of alternative social strategies on thermal tolerance in a facultatively polygynous (multiqueen) desert ant, Pogonomyrmex californicus, asking whether and how queen number affects worker thermal tolerances. We established and reared lab colonies with one to four queens, then quantified all colony member heat tolerances (maximum critical temperature [CTmax]). Workers from colonies with more queens had higher and less variant CTmax. Our findings resemble weak link patterns, in which colony group thermal performance is improved by reducing frequencies of the most temperature-vulnerable individuals. Using ambient temperatures from our collection site, we show that multiqueen colonies have thermal tolerance distributions that enable increased midday foraging in hot desert environments. Our results suggest advantages to polygyny under climate change scenarios and raise the question of whether improved thermal tolerance is a factor that has enabled the success of polygyne species in other climatically extreme environments.

Decoding alarm signal propagation of seed-harvester ants using automated movement tracking and supervised machine learning.

Alarm signal propagation through ant colonies provides an empirically tractable context for analysing information flow through a natural system, with useful insights for network dynamics in other social animals. Here, we develop a methodological approach to track alarm spread within a group of harvester ants, Pogonomyrmex californicus. We initially alarmed three ants and tracked subsequent signal transmission through the colony. Because there was no actual standing threat, the false alarm allowed us to assess amplification and adaptive damping of the collective alarm response. We trained a random forest regression model to quantify alarm behaviour of individual workers from multiple movement features. Our approach translates subjective categorical alarm scores into a reliable, continuous variable. We combined these assessments with automatically tracked proximity data to construct an alarm propagation network. This method enables analyses of spatio-temporal patterns in alarm signal propagation in a group of ants and provides an opportunity to integrate individual and collective alarm response. Using this system, alarm propagation can be manipulated and assessed to ask and answer a wide range of questions related to information and misinformation flow in social networks.

Soldier neural architecture is temporarily modality specialized but poorly predicted by repertoire size in the stingless bee Tetragonisca angustula.

Individual heterogeneity within societies provides opportunities to test hypotheses about adaptive neural investment in the context of group cooperation. Here, we explore neural investment in defense specialist soldiers of the eusocial stingless bee (Tetragonisca angustula) which are age subspecialized on distinct defense tasks and have an overall higher lifetime task repertoire than other sterile workers within the colony. Consistent with predicted behavioral demands, soldiers had higher relative visual (optic lobe) investment than nonsoldiers but only during the period when they were performing the most visually demanding defense task (hovering guarding). As soldiers aged into the less visually demanding task of standing guarding this difference disappeared. Neural investment was otherwise similar across all colony members. Despite having larger task repertoires, soldiers had similar absolute brain size and the smaller relative brain size compared to other workers, meaning that lifetime task repertoire size was a poor predictor of brain size. Both high behavioral specialization in stable environmental conditions and reassignment across task groups during a crisis occur in T. angustula. The differences in neurobiology we report here are consistent with these specialized but flexible defense strategies. This work broadens our understanding of how neurobiology mediates age and morphological task specialization in highly cooperative societies.

The active ingredients of a mitotoxic fungicide negatively affect pollen consumption and worker survival in laboratory-reared honey bees (Apis mellifera).

Recent observations of many sublethal effects of pesticides on pollinators have raised questions about whether standard short-term laboratory tests of pesticide effects on survival are sufficient for pollinator protection. The fungicide Pristine® and its active ingredients (25.2% boscalid, 12.8% pyraclostrobin) have been reported to have low acute toxicity to caged honey bee workers, but many sublethal effects at field-relevant doses have been reported and Pristine® was recently found to increase worker pollen consumption, reduce worker longevity and colony populations at field relevant concentrations (Fisher et al. 2021). To directly compare these whole-colony field results to more standard laboratory toxicology tests, the effects of Pristine®, at a range of field-relevant concentrations, were assessed on the survival and pollen consumption of honey bee workers 0-14 days of age. Also, to separate the effects of the inert and two active ingredients, bees were fed pollen containing boscalid, pyraclostrobin, or pyraclostrobin plus boscalid, at concentrations matching those in the Pristine® treatments. Pyraclostrobin significantly reduced pollen consumption across the duration of the experiment, and dose-dependently reduced pollen consumption on days 12-14. Pristine® and boscalid significantly reduced pollen feeding rate on days 12-14. Boscalid reduced survival in a dose-dependent manner. Consumption of Pristine® or pyraclostrobin plus boscalid did not affect survival, providing evidence against strong negative effects of the inert ingredients in Pristine® and against negative synergistic effects of boscalid and pyraclostrobin. The stronger toxic effects of Pristine® observed in field colonies compared to this laboratory test, and the opposite responses of pollen consumption in the laboratory and field to Pristine®, show that standard laboratory toxicology tests can fail to predict responses of pollinators to pesticides and to provide protection.

A common fungicide, Pristine®, impairs olfactory associative learning performance in honey bees (Apis mellifera).

Although fungicides were previously considered to be safe for important agricultural pollinators such as honey bees, recent evidence has shown that they can cause a number of behavioral and physiological sublethal effects. Here, we focus on the fungicide Pristine® (active ingredients: 25.2% boscalid, 12.8% pyraclostrobin), which is sprayed during the blooming period on a variety of crops and is known to affect honey bee mitochondria at field-relevant levels. To date, no study has tested the effects of a field-relevant concentration of a fungicide on associative learning ability in honey bees. We tested whether chronic, colony-level exposure at field-relevant and higher concentrations of Pristine® impairs performance on the proboscis extension reflex (PER) paradigm, an associative learning task. Learning performance was reduced at higher field-relevant concentrations of Pristine®. The reductions in learning performance could not be explained by effects on hunger or motivation, as sucrose responsiveness was not affected by Pristine® exposure. To determine whether Pristine®'s negative effects on learning performance were mediated at a specific life stage, we conducted a cross-fostering experiment that exposed bees to the fungicide either only as larvae, only as adults, or during both stages. We found that exposure across the entire life was necessary to significantly reduce learning performance, although non-significant reductions occurred when bees were exposed during just one stage. Our study provides strong evidence that Pristine® has significant sublethal effects on learning performance. As associative learning is a necessary ability for foraging, our results raise concerns that Pristine® could impair foraging abilities and substantially weaken colony health.

Cooperation among unrelated ant queens provides persistent growth and survival benefits during colony ontogeny.

The fitness consequences of cooperation can vary across an organism's lifespan. For non-kin groups, especially, social advantages must balance intrinsic costs of cooperating with non-relatives. In this study, we asked how challenging life history stages can promote stable, long-term alliances among unrelated ant queens. We reared single- and multi-queen colonies of the primary polygynous harvester ant, Pogonomyrmex californicus, from founding through the first ten months of colony growth, when groups face high mortality risks. We found that colonies founded by multiple, unrelated queens experienced significant survival and growth advantages that outlasted the colony founding period. Multi-queen colonies experienced lower mortality than single-queen colonies, and queens in groups experienced lower mortality than solitary queens. Further, multi-queen colonies produced workers at a faster rate than did single-queen colonies, even while experiencing lower per-queen worker production costs. Additionally, we characterized ontogenetic changes in the organization of labor, and observed increasing and decreasing task performance diversity by workers and queens, respectively, as colonies grew. This dynamic task allocation likely reflects a response to the changing role of queens as they are increasingly able to delegate risky and costly tasks to an expanding workforce. Faster worker production in multi-queen colonies may beneficially accelerate this behavioral transition from a vulnerable parent-offspring group to a stable, growing colony. These combined benefits of cooperation may facilitate the retention of multiple unrelated queens in mature colonies despite direct fitness costs, providing insight into the evolutionary drivers of stable associations between unrelated individuals.

Field cross-fostering and in vitro rearing demonstrate negative effects of both larval and adult exposure to a widely used fungicide in honey bees (Apis mellifera).

Pollinators and other insects are experiencing an ongoing worldwide decline. While various environmental stressors have been implicated, including pesticide exposure, the causes of these declines are complex and highly debated. Fungicides may constitute a particularly prevalent threat to pollinator health due to their application on many crops during bloom, and because pollinators such as bees may consume fungicide-tainted pollen or nectar. In a previous study, consumption of pollen containing the fungicide Pristine® at field-relevant concentrations by honey bee colonies increased pollen foraging, caused earlier foraging, lowered worker survival, and reduced colony population size. Because most pollen is consumed by young adults, we hypothesized that Pristine® (25.2% boscalid, 12.8% pyraclostrobin) in pollen exerts its negative effects on honey bee colonies primarily on the adult stage. To rigorously test this hypothesis, we used a cross-fostering experimental design, with bees reared in colonies provided Pristine® incorporated into pollen patties at a supra-field concentration (230 mg/kg), only in the larvae, only in the adult, or both stages. In contrast to our predictions, exposure to Pristine® in either the larval or adult stage reduced survival relative to control bees not exposed to Pristine®, and exposure to the fungicide at both larval and adult stages further reduced survival. Adult exposure caused precocious foraging, while larval exposure increased the tendency to forage for pollen. These results demonstrate that pollen containing Pristine® can induce significant negative effects on both larvae and adults in a hive, though the magnitude of such effects may be smaller at field-realistic doses. To further test the potential negative effects of direct consumption of Pristine® on larvae, we reared them in vitro on food containing Pristine® at a range of concentrations. Consumption of Pristine® reduced survival rates of larvae at all concentrations tested. Larval and adult weights were only reduced at a supra-field concentration. We conclude that consumption of pollen containing Pristine® by field honey bee colonies likely exerts impacts on colony population size and foraging behavior by affecting both larvae and adults.

Social consequences of energetically costly nest construction in a facultatively social bee.

Social groups form when the costs of breeding independently exceed fitness costs imposed by group living. The costs of independent breeding can often be energetic, especially for animals performing expensive behaviours, such as nest construction. To test the hypothesis that nesting costs can drive sociality by disincentivizing independent nest founding, we measured the energetics of nest construction and inheritance in a facultatively social carpenter bee (Xylocopa sonorina Smith), which bores tunnel nests in wood. We measured metabolic rates of bees excavating wood and used computerized tomography images of nesting logs to measure excavation volumes. From these data, we demonstrate costly energetic investments in nest excavation of a minimum 4.3 kJ per offspring provisioned, an expense equivalent to nearly 7 h of flight. This high, potentially prohibitive cost of nest founding may explain why females compete for existing nests rather than constructing new ones, often leading to the formation of social groups. Further, we found that nest inheritors varied considerably in their investment in nest renovation, with costs ranging more than 12-fold (from 7.08 to 89.1 kJ energy), probably reflecting differences in inherited nest quality. On average, renovation costs were lower than estimated new nest construction costs, with some nests providing major savings. These results suggest that females may join social groups to avoid steep energetic costs, but that the benefits of this strategy are not experienced equally.

Consumption of field-realistic doses of a widely used mito-toxic fungicide reduces thorax mass but does not negatively impact flight capacities of the honey bee (Apis mellifera).

Commercial beekeepers in many locations are experiencing increased annual colony losses of honey bees (Apis mellifera), but the causes, including the role of agrochemicals in colony losses, remain unclear. In this study, we investigated the effects of chronic consumption of pollen containing a widely-used fungicide (Pristine®), known to inhibit bee mitochondria in vitro, which has recently been shown to reduce honey bee worker lifespan when field-colonies are provided with pollen containing field-realistic levels of Pristine®. We fed field colonies pollen with a field-realistic concentration of Pristine® (2.3 ppm) and a concentration two orders of magnitude higher (230 ppm). To challenge flight behavior and elicit near-maximal metabolic rate, we measured flight quality and metabolic rates of bees in two lower-than-normal air densities. Chronic consumption of 230 but not 2.3 ppm Pristine® reduced maximal flight performance and metabolic rates, suggesting that the observed decrease in lifespans of workers reared on field-realistic doses of Pristine®-laced pollen is not due to inhibition of flight muscle mitochondria. However, consumption of either the 230 or 2.3 ppm dose reduced thorax mass (but not body mass), providing the first evidence of morphological effects of Pristine®, and supporting the hypothesis that Pristine® reduces forager longevity by negatively impacting digestive or nutritional processes.

Colony field test reveals dramatically higher toxicity of a widely-used mito-toxic fungicide on honey bees (Apis mellifera).

Honey bees (Apis mellifera) and other pollinator populations are declining worldwide, and the reasons remain controversial. Based on laboratory testing, fungicides have traditionally been considered bee-safe. However, there have been no experimental tests of the effects of fungicides on colony health under field conditions, and limited correlational data suggests there may be negative impacts on bees at levels experienced in the field. We tested the effects of one of the most commonly used fungicides on colony health by feeding honey bee colonies pollen containing Pristine® (active ingredients: 25.2% boscalid, 12.8% pyraclostrobin) at four levels that bracketed concentrations we measured for pollen collected by bees in almond orchards. We also developed a method for calculating per-bee and per-larva dose. Pristine® consumption significantly and dose-dependently reduced worker lifespan and colony population size, with negative health effects observed even at the lowest doses. The lowest concentration we tested caused a 15% reduction in the worker population at an estimated dosage that was three orders of magnitude below the estimated LD15 values for previous acute laboratory studies. The enhanced toxicity under field conditions is at least partially due to activation of colonial nutritional responses missed by lab tests. Pristine® causes colonies to respond to perceived protein malnutrition by increasing colony pollen collection. Additionally, Pristine induces much earlier transitioning to foraging in individual workers, which could be the cause of shortened lifespans. These findings demonstrate that Pristine® can negatively impact honey bee individual and colony health at concentrations relevant to what they experience from pollination behavior under current agricultural conditions.

Dynamics of social interactions, in the flow of information and disease spreading in social insects colonies: Effects of environmental events and spatial heterogeneity.

The relationship between division of labor and individuals' spatial behavior in social insect colonies provides a useful context to study how social interactions influence the spreading of elements (which could be information, virus or food) across distributed agent systems. In social insect colonies, spatial heterogeneity associated with variations of individual task roles, affects social contacts, and thus the way in which agent moves through social contact networks. We used an Agent Based Model (ABM) to mimic three realistic scenarios of elements' transmission, such as information, food or pathogens, via physical contact in social insect colonies. Our model suggests that individuals within a specific task interact more with consequences that elements could potentially spread rapidly within that group, while elements spread slower between task groups. Our simulations show a strong linear relationship between the degree of spatial heterogeneity and social contact rates, and that the spreading dynamics of elements follow a modified nonlinear logistic growth model with varied transmission rates for different scenarios. Our work provides important insights on the dual-functionality of physical contacts. This dual-functionality is often driven via variations of individual spatial behavior, and can have both inhibiting and facilitating effects on elements' transmission rates depending on environment. The results from our proposed model not only provide important insights on mechanisms that generate spatial heterogeneity, but also deepen our understanding of how social insect colonies balance the benefit and cost of physical contacts on the elements' transmission under varied environmental conditions.

Ecological drivers and reproductive consequences of non-kin cooperation by ant queens.

The fitness consequences of joining a group are highly dependent on ecological context, especially for non-kin. To assess the relationships between cooperation and environment, we examined variation in colony reproductive success for a harvester ant species that nests either solitarily or with multiple, unrelated queens, a social strategy known as primary polygyny. We measured the reproductive investment of colonies of solitary versus social nesting types at two sites, one with primarily single-queen colonies, and the other with a majority of polygynous nests. Our results were consistent with the hypothesis that cooperative nesting by unrelated ant queens is likely a selection response to difficult environments, rather than a strategy to maximize reproduction under favorable conditions. Fewer colonies at the primarily polygynous site reproduced than at the site with primarily single queen nests, and those that did had lower reproductive investment, as measured by number and total mass of reproductives. Assessment of ecological conditions also support the harsh environment hypothesis. Colony density in the multi-queen population was higher, and nearest neighbor distances were lower for non-reproducing than reproducing colonies. To more directly test the hypothesis that colony reproduction was ecologically constrained, we experimentally supplemented food resources for a subset of colonies at the primary polygyny site. Supplemented colonies increased reproductive investment levels to equal that of colonies at the single-queen population, further indicating that environmental pressures are severe where primary polygyny is dominant, and may drive the evolution of non-kin cooperation in this context.

Differentiating causality and correlation in allometric scaling: ant colony size drives metabolic hypometry.

Metabolic rates of individual animals and social insect colonies generally scale hypometrically, with mass-specific metabolic rates decreasing with increasing size. Although this allometry has wide ranging effects on social behaviour, ecology and evolution, its causes remain controversial. Because it is difficult to experimentally manipulate body size of organisms, most studies of metabolic scaling depend on correlative data, limiting their ability to determine causation. To overcome this limitation, we experimentally reduced the size of harvester ant colonies (Pogonomyrmex californicus) and quantified the consequent increase in mass-specific metabolic rates. Our results clearly demonstrate a causal relationship between colony size and hypometric changes in metabolic rate that could not be explained by changes in physical density. These findings provide evidence against prominent models arguing that the hypometric scaling of metabolic rate is primarily driven by constraints on resource delivery or surface area/volume ratios, because colonies were provided with excess food and colony size does not affect individual oxygen or nutrient transport. We found that larger colonies had lower median walking speeds and relatively more stationary ants and including walking speed as a variable in the mass-scaling allometry greatly reduced the amount of residual variation in the model, reinforcing the role of behaviour in metabolic allometry. Following the experimental size reduction, however, the proportion of stationary ants increased, demonstrating that variation in locomotory activity cannot solely explain hypometric scaling of metabolic rates in these colonies. Based on prior studies of this species, the increase in metabolic rate in size-reduced colonies could be due to increased anabolic processes associated with brood care and colony growth.

The foundress's dilemma: group selection for cooperation among queens of the harvester ant, Pogonomyrmex californicus.

The evolution of cooperation is a fundamental problem in biology, especially for non-relatives, where indirect fitness benefits cannot counter within-group inequalities. Multilevel selection models show how cooperation can evolve if it generates a group-level advantage, even when cooperators are disadvantaged within their group. This allows the possibility of group selection, but few examples have been described in nature. Here we show that group selection can explain the evolution of cooperative nest founding in the harvester ant Pogonomyrmex californicus. Through most of this species' range, colonies are founded by single queens, but in some populations nests are instead founded by cooperative groups of unrelated queens. In mixed groups of cooperative and single-founding queens, we found that aggressive individuals had a survival advantage within their nest, but foundress groups with such non-cooperators died out more often than those with only cooperative members. An agent-based model shows that the between-group advantage of the cooperative phenotype drives it to fixation, despite its within-group disadvantage, but only when population density is high enough to make between-group competition intense. Field data show higher nest density in a population where cooperative founding is common, consistent with greater density driving the evolution of cooperative foundation through group selection.