Social network position is a major predictor of ant behavior, microbiota composition, and brain gene expression.

The physiology and behavior of social organisms correlate with their social environments. However, because social environments are typically confounded by age and physical environments (i.e., spatial location and associated abiotic factors), these correlations are usually difficult to interpret. For example, associations between an individual's social environment and its gene expression patterns may result from both factors being driven by age or behavior. Simultaneous measurement of pertinent variables and quantification of the correlations between these variables can indicate whether relationships are direct (and possibly causal) or indirect. Here, we combine demographic and automated behavioral tracking with a multiomic approach to dissect the correlation structure among the social and physical environment, age, behavior, brain gene expression, and microbiota composition in the carpenter ant Camponotus fellah. Variations in physiology and behavior were most strongly correlated with the social environment. Moreover, seemingly strong correlations between brain gene expression and microbiota composition, physical environment, age, and behavior became weak when controlling for the social environment. Consistent with this, a machine learning analysis revealed that from brain gene expression data, an individual's social environment can be more accurately predicted than any other behavioral metric. These results indicate that social environment is a key regulator of behavior and physiology.

An evidence map of polychlorinated biphenyl exposure and health outcome studies among residents of the Akwesasne Mohawk Nation.

From the 1950s to the 1970s, three Superfund sites discharged polychlorinated biphenyl (PCB)-contaminated waste upstream of the Mohawk Nation at Akwesasne, resulting in PCB contamination of groundwater, soil, and sediment in the surrounding area. Given the persistence of PCBs in the environment and in human tissues, there are continued concerns regarding PCB exposures and the potential for adverse health effects in the community. We developed an evidence map of PCB research at Akwesasne in order to characterize the available data and to highlight potential research needs. Human health and exposure biomarker studies were identified from a literature search based on population, exposure, comparator, and outcome (PECO) criteria. Data extracted from references that met the inclusion criteria after full-text review included study characteristics (e.g., sample size, study design, sampling years), details on PCB measurements (e.g., analytical method, number of congeners analyzed, method detection limits), and results (e.g., PCB levels and summary of study conclusions). We identified 33 studies, conducted between 1986 and 2013, that examined PCB exposure characteristics and health effects in residents of the Akwesasne Mohawk Nation. Organizing this literature into an evidence map including information on study cohort, congener groupings, exposure biomarker characteristics, and health effects allowed us to identify research gaps and to suggest future research priorities for the community. We identified current PCB exposure levels and PCB source characterization as major uncertainties, both of which could be addressed by new studies of PCB concentrations in environmental media.

A Comparison of Pollen and Syrup Exposure Routes in Bombus impatiens (Hymenoptera: Apidae) Microcolonies: Implications for Pesticide Risk Assessment.

Bumble bees are important pollinators for both native plants and managed agricultural systems. Accumulating evidence has shown that pesticides, including neonicotinoids, can have a range of adverse effects on bumble bee health. Most laboratory studies that assess the effects of chronic neonicotinoid exposure on bumble bees use syrup as the delivery vehicle, rather than pollen. However, in the field, it is likely that bumble bees are exposed to neonicotinoids in both nectar (syrup) and pollen. To examine the potential for different effects based on the vehicle, we compared two studies of chronic exposure to the neonicotinoid acetamiprid in Bombus impatiens microcolonies. We examined correlations between microcolony endpoints and identified associations between the timing of colony pollen and syrup consumption and drone production. Furthermore, in line with previous results, we found that average drone weight was affected at a range of doses only when microcolonies were exposed to acetamiprid via pollen. In general, our analyses point to the importance of the treatment vehicle and suggest that critical effects on developing brood could be missed when neonicotinoid exposure occurs only through syrup.

Effects of air pollution exposure on social behavior: a synthesis and call for research.

BACKGROUND: There is a growing literature from both epidemiologic and experimental animal studies suggesting that exposure to air pollution can lead to neurodevelopmental and neuropsychiatric disorders. Here, we suggest that effects of air pollutant exposure on the brain may be even broader, with the potential to affect social decision-making in general. METHODS: We discuss how the neurobiological substrates of social behavior are vulnerable to air pollution, then briefly present studies that examine the effects of air pollutant exposure on social behavior-related outcomes. RESULTS: Few experimental studies have investigated the effects of air pollution on social behavior and those that have focus on standard laboratory tests in rodent model systems. Nonetheless, there is sufficient evidence to support a critical need for more research. CONCLUSION: For future research, we suggest a comparative approach that utilizes diverse model systems to probe the effects of air pollution on a wider range of social behaviors, brain regions, and neurochemical pathways.

An Examination of National Cancer Risk Based on Monitored Hazardous Air Pollutants.

BACKGROUND: Hazardous air pollutants, or air toxics, are pollutants known to cause cancer or other serious health effects. Nationwide cancer risk from these pollutants is estimated by the U.S. EPA National Air Toxics Assessment. However, these model estimates are limited to the totality of the emissions inventory used as inputs, and further, they cannot be used to examine spatial and temporal trends in cancer risk from hazardous air pollutants. OBJECTIVES: To complement model estimates of nationwide cancer risk, we examined trends in cancer risk using monitoring data from 2013 to 2017 across the 27 U.S. National Air Toxics Trends Stations. METHODS: For each monitoring site, we estimated cancer risk by multiplying the annual concentration for each monitored pollutant by its corresponding unit risk estimate. We examined the 5-y average (2013-2017) cancer risk across sites and the population levels and demographics within 1-mi of the monitors, as well as changes in estimated cancer risk over time. Finally, we examined changes in individual pollutant concentrations and their patterns of covariance. RESULTS: We found that the total estimated cancer risk is higher for urban vs. rural sites, with the risk at seven urban sites (of 21) above 75 in 1 million. Furthermore, while most pollutant concentrations have not changed over the time period explored, we found 38 site-pollutant combinations that significantly declined and 12 that significantly increased between 2013 and 2017. We also identified a positive correlation between estimated cancer risk and percent of the population within 1-mi of a monitor that is low income. DISCUSSION: Long-term trends show that annual mean concentrations of most measured air toxics have declined. Our evaluation of a more recent snapshot in time finds that most pollutant concentrations have not changed from 2013 to 2017. This analysis of cancer risk based on monitored values provides an important complement to modeled nationwide cancer risk estimates and can further inform future approaches to mitigate risk from exposure to hazardous air pollutants. https://doi.org/10.1289/EHP8044.

Monoassociation with bacterial isolates reveals the role of colonization, community complexity and abundance on locomotor behavior in larval zebrafish.

BACKGROUND: Across taxa, animals with depleted intestinal microbiomes show disrupted behavioral phenotypes. Axenic (i.e., microbe-free) mice, zebrafish, and fruit flies exhibit increased locomotor behavior, or hyperactivity. The mechanism through which bacteria interact with host cells to trigger normal neurobehavioral development in larval zebrafish is not well understood. Here, we monoassociated zebrafish with either one of six different zebrafish-associated bacteria, mixtures of these host-associates, or with an environmental bacterial isolate. RESULTS: As predicted, the axenic cohort was hyperactive. Monoassociation with three different host-associated bacterial species, as well as with the mixtures, resulted in control-like locomotor behavior. Monoassociation with one host-associate and the environmental isolate resulted in the hyperactive phenotype characteristic of axenic larvae, while monoassociation with two other host-associated bacteria partially blocked this phenotype. Furthermore, we found an inverse relationship between the total concentration of bacteria per larvae and locomotor behavior. Lastly, in the axenic and associated cohorts, but not in the larvae with complex communities, we detected unexpected bacteria, some of which may be present as facultative predators. CONCLUSIONS: These data support a growing body of evidence that individual species of bacteria can have different effects on host behavior, potentially related to their success at intestinal colonization. Specific to the zebrafish model, our results suggest that differences in the composition of microbes in fish facilities could affect the results of behavioral assays within pharmacological and toxicological studies.

A state-of-the-science review of polychlorinated biphenyl exposures at background levels: relative contributions of exposure routes.

Exposure to polychlorinated biphenyls (PCBs) can occur through multiple routes and sources, including dietary intake, inhalation, dermal contact, and ingestion of dust and soils. Dietary exposure to PCBs is often considered the primary exposure route for the general population; however, recent studies suggest an increasing contribution from indoor inhalation exposure. Here, we aim to estimate the relative contribution of different PCB exposure pathways for the general population, as well as for select age groups. We conducted a targeted literature review of PCB concentrations in environmental media, including indoor and outdoor air, indoor dust, and soils, as well as of total dietary intake. Using the average concentrations from the studies identified, we estimated PCB exposure through different routes for the general population. In addition, we assessed exposure via environmental media for select age groups. We identified a total of 70 studies, 64 that provided background PCB concentrations for one or more of the environmental media of interest and 6 studies that provided estimates of dietary intake. Using estimates from studies conducted worldwide, for the general population, dietary intake of PCBs was the major exposure pathway. In general, our review identifies important limitations in the data available to assess population exposures, highlighting the need for more current and population-based estimates of PCB exposure, particularly for indoor air and dietary intake.

A systematic review of the health effects associated with the inhalation of particle-filtered and whole diesel exhaust.

Background: Diesel exhaust is a complex mixture comprised of gases and particulate matter and is a contributor to ambient air pollution. To reduce health risks, recent changes in diesel engine technology have significantly altered the composition of diesel exhaust, primarily by lowering emissions of particulate matter. However, animal toxicological studies continue to report health effects following exposure to diesel exhaust from engines employing particulate filters. The cause of these effects remains unclear.Objective and methods: To gain an understanding of the role of both particle-filtered and whole diesel exhaust on specific health outcomes, we conducted a systematic review in which we examined animal toxicological and controlled human exposure studies that included a comparison between inhalation of particle-filtered and whole diesel exhaust on any health endpoint.Results: We identified 26 studies that met both the inclusion and study evaluation criteria. For most health outcomes, the particle filtration methods employed in the included studies did not appreciably attenuate the health effects associated with exposure to whole diesel exhaust. There were also several health endpoints for which significant effects were associated with exposure to either particle-filtered or whole diesel exhaust, but not to both.Conclusions: Overall, the results from this systematic review demonstrate that exposure to different components in diesel exhaust can have distinct and independent health effects. Thus, to better inform human health risk assessments, future studies aimed at elucidating the health effects from diesel exhaust should include exposure to both particle-filtered and whole diesel exhaust.

Health effects from freshly emitted versus oxidatively or photochemically aged air pollutants.

Epidemiology studies over the past five decades have provided convincing evidence that exposure to air pollution is associated with multiple adverse health outcomes, including increased mortality. Air pollution is a complex mixture of particles, vapors and gases emitted from natural and anthropogenic sources as well as formed through photochemical transformation processes. In metropolitan areas, air pollutants from combustion emissions feature a blend of emitted particles, oxides of carbon, sulfur and nitrogen, volatile organic compounds, and secondary reaction products, such as ozone, nitrogen dioxide, and secondary organic aerosols. Because many of the primary and transformed pollutants track together, their relative contributions to health outcomes are difficult to disentangle. Aside from the criteria pollutants ozone and nitrogen dioxide and some of the simpler aldehydes (e.g. formaldehyde and acrolein), other products from photochemical processes are a particularly vexing class of chemicals to investigate since they comprise a dynamic ill-defined complex mixture in both particulate and gas phases. The purpose of this review was to describe and compare health effects of freshly emitted versus oxidatively or photochemically aged air pollutants. In some cases, (e.g. single volatile organic compounds) photochemical transformation resulted in marked enhancements in toxicity through formation of both known and unidentified reaction products, while in other examples (e.g. aging of automobile emissions) the potentiation of effect was variable. The variation in experimental design, aging system employed, concentration and type of starting agent, and toxicity endpoints make comparisons between different studies exceedingly difficult. A more systematic approach with a greater emphasis on higher throughput screening and computational toxicology is needed to fully answer under what conditions oxidatively- or photochemically-transformed pollutants elicit greater health effects than primary emissions.

Triclosan-Selected Host-Associated Microbiota Perform Xenobiotic Biotransformations in Larval Zebrafish.

Microbiota regulate important physiologic processes during early host development. They also biotransform xenobiotics and serve as key intermediaries for chemical exposure. Antimicrobial agents in the environment may disrupt these complex interactions and alter key metabolic functions provided by host-associated microbiota. To examine the role of microbiota in xenobiotic metabolism, we exposed zebrafish larvae to the antimicrobial agent triclosan. Conventionally colonized (CC), microbe-free axenic (AX), or axenic colonized on day 1 (AC1) zebrafish were exposed to 0.16-0.30 µM triclosan or vehicle on days 1, 6, 7, 8, and 9 days post fertilization (dpf). After 6 and 10 dpf, host-associated microbial community structure and putative function were assessed by 16S rRNA gene sequencing. At 10 dpf, triclosan exposure selected for bacterial taxa, including Rheinheimera. Triclosan-selected microbes were predicted to be enriched in pathways related to mechanisms of antibiotic resistance, sulfonation, oxidative stress, and drug metabolism. Furthermore, at 10 dpf, colonized zebrafish contained 2.5-3 times more triclosan relative to AX larvae. Nontargeted chemical analysis revealed that, relative to AX larvae, both cohorts of colonized larvae showed elevations in 23 chemical features, including parent triclosan and putative triclosan sulfate. Taken together, these data suggest that triclosan exposure selects for microbes that harbor the capacity to biotransform triclosan into chemical metabolites with unknown toxicity profiles. More broadly, these data support the concept that microbiota modify the toxicokinetics of xenobiotic exposure.

A comparison of hourly with annual air pollutant emissions: Implications for estimating acute exposure and public health risk.

Health risks from air pollutants are evaluated by comparing chronic (i.e., an average over 1 yr or greater) or acute (typically 1-hr) exposure estimates with chemical- and duration-specific reference values or standards. When estimating long-term pollutant concentrations via exposure modeling, facility-level annual average emission rates are readily available as model inputs for most air pollutants. In contrast, there are far fewer facility-level hour-by-hour emission rates available for many of these same pollutants. In this report, we first analyze hour-by-hour emission rates for total reduced sulfur (TRS) compounds from eight kraft pulp mill operations. This data set is used to demonstrate discrepancies between estimating exposure based on a single TRS emission rate that has been calculated as the mean of all operating hours of the year, as opposed to reported hourly emission rates. A similar analysis is then performed using reported hourly emission rates for sulfur dioxide (SO2) and oxides of nitrogen (NOx) from three power generating units from a U.S. power plant. Results demonstrate greater variability at kraft pulp mill operations, with ratios of reported hourly to average hourly TRS emissions ranging from less than 1 to greater than 160 during routine facility operations. Thus, if fluctuations in hourly emission rates are not accounted for, over- or underestimates of hourly exposure, and thus acute health risk, may occur. In addition to this analysis, we also demonstrate an additional challenge when assessing health risk based on hourly exposures: the lack of human health reference values based on 1-hr exposures. Implications: Largely due to the lack of reported hourly emission rate data for many air pollutants, an hourly average emission rate (calculated from an annual emission rate) is often used when modeling the potential for acute health risk. We calculated ratios between reported hourly and hourly average emission rates from pulp and paper mills and a U.S. power plant to demonstrate that if not considered, hourly fluctuations in emissions could result in an over- or underestimation of exposure and risk. We also demonstrate the lack of 1-hr human health reference values meant to be protective of the general population, including children.

Neural activity in the social decision-making network of the brown anole during reproductive and agonistic encounters.

Animals have evolved flexible strategies that allow them to evaluate and respond to their social environment by integrating the salience of external stimuli with internal physiological cues into adaptive behavioral responses. A highly conserved social decision-making network (SDMN), consisting of interconnected social behavior and mesolimbic reward networks, has been proposed to underlie such adaptive behaviors across all vertebrates, although our understanding of this system in reptiles is very limited. Here we measure neural activation across the SDMN and associated regions in the male brown anole (Anolis sagrei), within both reproductive and agonistic contexts, by quantifying the expression density of the immediate early gene product Fos. We then relate this neural activity measure to social context, behavioral expression, and activation (as measured by colocalization with Fos) of different phenotypes of 'source' node neurons that produce neurotransmitters and neuropeptides known to modulate SDMN 'target' node activity. Our results demonstrate that measures of neural activation across the SDMN network are generally independent of specific behavioral output, although Fos induction in a few select nodes of the social behavior network component of the SDMN does vary with social environment and behavioral output. Under control conditions, the mesolimbic reward nodes of the SDMN actually correlate little with the social behavior nodes, but the interconnectivity of these SDMN components increases dramatically within a reproductive context. When relating behavioral output to specific source node activation profiles, we found that catecholaminergic activation is associated with the frequency and intensity of reproductive behavior output, as well as with aggression intensity. Finally, in terms of the effects of source node activation on SDMN activity, we found that Ile8-oxytocin (mesotocin) populations correlate positively, while Ile3-vasopressin (vasotocin), catecholamine, and serotonin populations correlate negatively with SDMN activity. Taken together, our findings present evidence for a highly dynamic SDMN in reptiles that is responsive to salient cues in a social context-dependent manner.

Arginine Vasotocin Preprohormone Is Expressed in Surprising Regions of the Teleost Forebrain.

Nonapeptides play a fundamental role in the regulation of social behavior, among numerous other functions. In particular, arginine vasopressin and its non-mammalian homolog, arginine vasotocin (AVT), have been implicated in regulating affiliative, reproductive, and aggressive behavior in many vertebrate species. Where these nonapeptides are synthesized in the brain has been studied extensively in most vertebrate lineages. While several hypothalamic and forebrain populations of vasopressinergic neurons have been described in amniotes, the consensus suggests that the expression of AVT in the brain of teleost fish is limited to the hypothalamus, specifically the preoptic area (POA) and the anterior tuberal nucleus (putative homolog of the mammalian ventromedial hypothalamus). However, as most studies in teleosts have focused on the POA, there may be an ascertainment bias. Here, we revisit the distribution of AVT preprohormone mRNA across the dorsal and ventral telencephalon of a highly social African cichlid fish. We first use in situ hybridization to map the distribution of AVT preprohormone mRNA across the telencephalon. We then use quantitative real-time polymerase chain reaction to assay AVT expression in the dorsomedial telencephalon, the putative homolog of the mammalian basolateral amygdala. We find evidence for AVT preprohormone mRNA in regions previously not associated with the expression of this nonapeptide, including the putative homologs of the mammalian extended amygdala, hippocampus, striatum, and septum. In addition, AVT preprohormone mRNA expression within the basolateral amygdala homolog differs across social contexts, suggesting a possible role in behavioral regulation. We conclude that the surprising presence of AVT preprohormone mRNA within dorsal and medial telencephalic regions warrants a closer examination of possible AVT synthesis locations in teleost fish, and that these may be more similar to what is observed in mammals and birds.

Genetics and Evolution of Social Behavior in Insects.

The study of insect social behavior has offered tremendous insight into the molecular mechanisms mediating behavioral and phenotypic plasticity. Genomic applications to the study of eusocial insect species, in particular, have led to several hypotheses for the processes underlying the molecular evolution of behavior. Advances in understanding the genetic control of social organization have also been made, suggesting an important role for supergenes in the evolution of divergent behavioral phenotypes. Intensive study of social phenotypes across species has revealed that behavior and caste are controlled by an interaction between genetic and environmentally mediated effects and, further, that gene expression and regulation mediate plastic responses to environmental signals. However, several key methodological flaws that are hindering progress in the study of insect social behavior remain. After reviewing the current state of knowledge, we outline ongoing challenges in experimental design that remain to be overcome in order to advance the field.

Neuromolecular Regulation of Aggression Differs by Social Role during Joint Territory Defense.

In response to a territory intrusion, neighboring males of the African cichlid fish Astatotilapia burtoni engage in aggressive joint territory defense in a manner that depends on their social role. Here, we examine the possible function of several neuroendocrine and neuromodulator pathways previously implicated in the regulation of complex social behavior. We find that the neuromolecular regulation of aggression during joint territory defense is very much dependent on an individual's role in this context. In neighbors but not in residents, aggression is correlated to gene expression in the medial part of the dorsal telencephalon (area Dm), the putative homolog to the mammalian basolateral amygdala. This correlation is strikingly high for expression of the serotonin receptor 5-HT2c, suggesting the serotonin system is important in regulating context-dependent behavior. Furthermore, by examining candidate gene expression co-variance patterns in area Dm and in the lateral part of the dorsal telencephalon (area Dl), the putative homolog to the mammalian hippocampus, we identify two main patterns: gene expression is co-regulated within, but not across, brain regions, and co-regulation is synergistic rather than antagonistic. Our results highlight the critical effect of social context on both behavior and its neuromolecular basis.

A Role for Oxytocin-Like Receptor in Social Habituation in a Teleost.

Oxytocin (OT) mediates social habituation in rodent model systems, but its role in mediating this effect in other vertebrates is unknown. We used males of the African cichlid fish, Astatotilapia burtoni, to investigate two aspects of isotocin (IT; an OT homolog) signaling in social habituation. First, we examined the expression of IT receptor 2 (ITR2) as well as two immediate early genes in brain regions implicated in social recognition. Next, we examined IT neuron activity using immunohistochemistry. Patterns of gene expression in homologs of the amygdala and hippocampus implicate IT signaling in these regions in social habituation to a territorial neighbor. In the preoptic area, the expression of the ITR2 subtype and IT neuron activity respond to the presence of a male, independent of familiarity. Our results implicate IT in mediating social habituation in a teleost.

Neuromolecular correlates of cooperation and conflict during territory defense in a cichlid fish.

Cooperative behavior is widespread among animals, yet the neural mechanisms have not been studied in detail. We examined cooperative territory defense behavior and associated neural activity in candidate forebrain regions in the cichlid fish, Astatotilapia burtoni. We find that a territorial male neighbor will engage in territory defense dependent on the perceived threat of the intruder. The resident male, on the other hand, engages in defense based on the size and behavior of his partner, the neighbor. In the neighbor, we find that an index of engagement correlates with neural activity in the putative homolog of the mammalian basolateral amygdala and in the preoptic area, as well as in preoptic dopaminergic neurons. In the resident, neighbor behavior is correlated with neural activity in the homolog of the mammalian hippocampus. Overall, we find distinct neural activity patterns between the neighbor and the resident, suggesting that an individual perceives and processes an intruder challenge differently during cooperative territory defense depending on its own behavioral role.

Evolutionary themes in the neurobiology of social cognition.

Remarkable examples of social cognition have been described across a diverse range of species, yet surprisingly little is known about the neurobiological underpinnings of these behaviors. Recent studies suggest that the molecular pathways and neural networks that mediate social behavior have been relatively conserved across vertebrate evolution, suggesting that shared mechanisms may drive adaptive behavioral responses to social stimuli. Here, we review recent advances in the neurobiology of flexible and context-dependent social behaviors across vertebrate taxa, focusing on female mate choice, pair-bonding, and aggressive behavior. Furthermore, we highlight the outstanding opportunities for uncovering the mechanisms mediating cooperative behavior, an exemplar of social cognition. We suggest a framework for investigating context-dependent neural organization and the evoked neural response to social stimuli.

Genetic variation and mating success in managed american plains bison.

The American plains bison (Bison bison) was pushed to the brink of extinction in the late 1800s but has since rebounded. Less than 5% of animals currently exist in conservation herds that are critical for maintaining genetic variability. Here, we use 25 microsatellite loci to assess genetic diversity and patterns of mating success over a 3-year period in a managed conservation herd at Konza Prairie Biological Station, Kansas (total number of individuals genotyped = 587). Heterozygosity was comparable to and allelic diversity higher than that in 11 other wild and managed herds for which similar estimates are available. Parentage analyses revealed that males within the oldest age classes (5-7 years) sired >90% of calves over the study period, consistent with a polygynous breeding system. Asymmetries in siring success also were observed within age classes, with the same males enjoying high siring success over multiple seasons. Empirical results of paternity will facilitate future modeling and empirical efforts to determine how demographic factors, population size, and variation in siring success interact to determine the retention (or loss) of genetic diversity in natural and managed herds, thus allowing informed recommendations for management practices and conservation efforts of this symbolic North American species.