Influenza A virus reassortment is strain dependent.

RNA viruses can exchange genetic material during coinfection, an interaction that creates novel strains with implications for viral evolution and public health. Influenza A viral genetic exchange can occur when genome segments from distinct strains reassort in coinfected cells. Predicting potential genomic reassortment between influenza strains has been a long-standing goal. Experimental coinfection studies have shed light on factors that limit or promote reassortment. However, determining the reassortment potential between diverse Influenza A strains has remained elusive. To address this challenge, we developed a high throughput genotyping approach to quantify reassortment among a diverse panel of human influenza virus strains encompassing two pandemics (swine and avian origin), three specific epidemics, and both circulating human subtypes A/H1N1 and A/H3N2. We found that reassortment frequency (the proportion of reassortants generated) is an emergent property of specific pairs of strains where strain identity is a predictor of reassortment frequency. We detect little evidence that antigenic subtype drives reassortment as intersubtype (H1N1xH3N2) and intrasubtype reassortment frequencies were, on average, similar. Instead, our data suggest that certain strains bias the reassortment frequency up or down, independently of the coinfecting partner. We observe that viral productivity is also an emergent property of coinfections, but uncorrelated to reassortment frequency; thus viral productivity is a separate factor affecting the total number of reassortants produced. Assortment of individual segments among progeny and pairwise segment combinations within progeny generally favored homologous combinations. These outcomes were not related to strain similarity or shared subtype but reassortment frequency was closely correlated to the proportion of both unique genotypes and of progeny with heterologous pairwise segment combinations. We provide experimental evidence that viral genetic exchange is potentially an individual social trait subject to natural selection, which implies the propensity for reassortment is not evenly shared among strains. This study highlights the need for research incorporating diverse strains to discover the traits that shift the reassortment potential to realize the goal of predicting influenza virus evolution resulting from segment exchange.

Open questions in the social lives of viruses.

Social interactions among viruses occur whenever multiple viral genomes infect the same cells, hosts, or populations of hosts. Viral social interactions range from cooperation to conflict, occur throughout the viral world, and affect every stage of the viral lifecycle. The ubiquity of these social interactions means that they can determine the population dynamics, evolutionary trajectory, and clinical progression of viral infections. At the same time, social interactions in viruses raise new questions for evolutionary theory, providing opportunities to test and extend existing frameworks within social evolution. Many opportunities exist at this interface: Insights into the evolution of viral social interactions have immediate implications for our understanding of the fundamental biology and clinical manifestation of viral diseases. However, these opportunities are currently limited because evolutionary biologists only rarely study social evolution in viruses. Here, we bridge this gap by (1) summarizing the ways in which viruses can interact socially, including consequences for social evolution and evolvability; (2) outlining some open questions raised by viruses that could challenge concepts within social evolution theory; and (3) providing some illustrative examples, data sources, and conceptual questions, for studying the natural history of social viruses.

Evaluating expert-based habitat suitability information of terrestrial mammals with GPS-tracking data.

Aim: Macroecological studies that require habitat suitability data for many species often derive this information from expert opinion. However, expert-based information is inherently subjective and thus prone to errors. The increasing availability of GPS tracking data offers opportunities to evaluate and supplement expert-based information with detailed empirical evidence. Here, we compared expert-based habitat suitability information from the International Union for Conservation of Nature (IUCN) with habitat suitability information derived from GPS-tracking data of 1,498 individuals from 49 mammal species. Location: Worldwide. Time period: 1998-2021. Major taxa studied: Forty-nine terrestrial mammal species. Methods: Using GPS data, we estimated two measures of habitat suitability for each individual animal: proportional habitat use (proportion of GPS locations within a habitat type), and selection ratio (habitat use relative to its availability). For each individual we then evaluated whether the GPS-based habitat suitability measures were in agreement with the IUCN data. To that end, we calculated the probability that the ranking of empirical habitat suitability measures was in agreement with IUCN's classification into suitable, marginal and unsuitable habitat types. Results: IUCN habitat suitability data were in accordance with the GPS data (> 95% probability of agreement) for 33 out of 49 species based on proportional habitat use estimates and for 25 out of 49 species based on selection ratios. In addition, 37 and 34 species had a > 50% probability of agreement based on proportional habitat use and selection ratios, respectively. Main conclusions: We show how GPS-tracking data can be used to evaluate IUCN habitat suitability data. Our findings indicate that for the majority of species included in this study, it is appropriate to use IUCN habitat suitability data in macroecological studies. Furthermore, we show that GPS-tracking data can be used to identify and prioritize species and habitat types for re-evaluation of IUCN habitat suitability data.

Complex cooperative breeders: Using infant care costs to explain variability in callitrichine social and reproductive behavior.

The influence of ecology on social behavior and mating strategies is one of the central questions in behavioral ecology and primatology. Callitrichines are New World primates that exhibit high behavioral variability, which is widely acknowledged, but not always systematically researched. Here, I examine the hypothesis that differences in the cost of infant care among genera help explain variation in reproductive traits. I present an integrative approach to generate and evaluate predictions from this hypothesis. I first identify callitrichine traits that vary minimally and traits that are more flexible (e.g., have greater variance or norm of reaction), including the number of males that mate with a breeding female, mechanisms of male reproductive competition, number of natal young retained, and the extent of female reproductive suppression. I outline how these more labile traits should vary along a continuum of infant care costs according to individual reproductive strategies. At one end of the spectrum, I predict that groups with higher infant care costs will show multiple adult males mating and providing infant care, high subordinate female reproductive suppression, few natal individuals delaying dispersal, and increased reproductive output by the dominant female -with opposite predictions under low infant costs. I derive an estimate of the differences in ecological and physiological infant care costs that suggest an order of ascending costs in the wild: Cebuella, Callithrix, Mico, Callimico, Saguinus, and Leontopithecus. I examine the literature on each genus for the most variable traits and evaluate a) where they fall along the continuum of infant care costs according to their reproductive strategies, and b) whether these costs correspond to the ecophysiological estimates of infant care costs. I conclude that infant care costs can provide a unifying explanation for the most variable reproductive traits among callitrichine genera. The approach presented can be used to generate predictions and motivate researchers to unravel complexity in callitrichine social and reproductive behavior.

"Monogamy" in Primates: Variability, Trends, and Synthesis: Introduction to special issue on Primate Monogamy.

This paper is the introduction to a special issue on "'Monogamy' in Primates: Variability, Trends, and Synthesis." The term "monogamy" has undergone redefinition over the years, and is now generally understood to refer to certain social characteristics rather than to genetic monogamy. However, even the term "social monogamy" is used loosely to refer to species which exhibit a spectrum of social structures, mating patterns, and breeding systems. Papers in this volume address key issues including whether or not our definitions of monogamy should change in order to better represent the social and mating behaviors that characterize wild primates; whether or not primate groups traditionally considered monogamous are actually so (by any definition); ways in which captive studies can contribute to our understanding of monogamy; and what selective pressures might have driven the evolution of monogamous and non-monogamous single female breeding systems.

Bacteria-phage interactions in natural environments.

Phages are considered the most abundant and diverse biological entities on Earth and are notable not only for their sheer abundance, but also for their influence on bacterial hosts. In nature, bacteria-phage relationships are complex and have far-reaching consequences beyond particular pairwise interactions, influencing everything from bacterial virulence to eukaryotic fitness to the carbon cycle. In this review, we examine bacteria and phage distributions in nature first by highlighting biogeographic patterns and nonhost environmental influences on phage distribution, then by considering the ways in which phages and bacteria interact, emphasizing phage life cycles, bacterial responses to phage infection, and the complex patterns of phage host specificity. Finally, we discuss phage impacts on bacterial abundance, genetics, and physiology, and further aim to clarify distinctions between current theoretical models and point out areas in need of future research.

Influenza A defective viral genome production is altered by metabolites, metabolic signaling molecules, and cyanobacteria extracts.

RNA virus infections are composed of a diverse mix of viral genomes that arise from low fidelity in replication within cells. The interactions between "defective" and full-length viral genomes have been shown to shape pathogenesis, leading to intense research into employing these to develop novel antivirals. In particular, Influenza A defective viral genomes (DVGs) have been associated with milder clinical outcomes. Yet, the full potential of DVGs as broad-spectrum antivirals remains untapped due to the unknown mechanisms of their de novo production. Much of the research into the factors affecting defective viral genome production has focused on the virus, while the role of the host has been neglected. We recently showed that altering host cell metabolism away from pro-growth pathways using alpelisib increased the production of Influenza A defective viral genomes. To uncover other drugs that could induce infections to create more DVGs, we subjected active influenza infections of the two circulating human subtypes (A/H1N1 & A/H3N2) to a screen of metabolites, metabolic signaling molecules, and cyanobacteria-derived biologics, after which we quantified the defective viral genomes (specifically deletion-containing viral genomes, DelVGs) and total viral genomes using third generation long-read sequencing. Here we show that metabolites and signaling molecules of host cell central carbon metabolism can significantly alter DelVG production early in Influenza A infection. Adenosine, emerged as a potent inducer of defective viral genomes, significantly amplifying DelVG production across both subtypes. Insulin had similar effects, albeit subtype-specific, predominantly enhancing polymerase segment DVGs in TX12 infections. Tricarboxylic Acid (TCA) cycle inhibitors 4-octyl itaconate and UK5099, along with the purine analog favipiravir, increased total viral genome production across subtypes. Cyanobacterial extracts primarily affected DVG and total viral genome production in TX12, with a specific, almost complete shutdown of influenza antigenic segments. These results underscore the influence of host metabolic pathways on DVG production and suggest new avenues for antiviral intervention, including PI3K-AKT and Ras-MAPK signaling pathways, TCA cycle metabolism, purine-pyrimidine metabolism, polymerase inhibition, and cyanotherapeutic approaches. More broadly, our findings suggest that the social interactions observed between defective and full-length viral genomes, depend not only on the viral actors, but can be altered by the stage provided by the host. Our study advances our fundamental understanding of DVG production mechanisms and highlights the potential of targeting host metabolism to develop broad-spectrum influenza therapeutics.

Influenza A defective viral genomes and non-infectious particles are increased by host PI3K inhibition via anti-cancer drug alpelisib.

RNA viruses produce abundant defective viral genomes during replication, setting the stage for interactions between viral genomes that alter the course of pathogenesis. Harnessing these interactions to develop antivirals has become a recent goal of intense research focus. Despite decades of research, the mechanisms that regulate the production and interactions of Influenza A defective viral genomes are still unclear. The role of the host is essentially unexplored; specifically, it remains unknown whether host metabolism can influence the formation of defective viral genomes and the particles that house them. To address this question, we manipulated host cell anabolic signaling activity and monitored the production of defective viral genomes and particles by A/H1N1 and A/H3N2 strains, using a combination of single-cell immunofluorescence quantification, third-generation long-read sequencing, and the cluster-forming assay, a method we developed to titer defective and fully-infectious particles simultaneously. Here we show that alpelisib (Piqray), a highly selective inhibitor of mammalian Class 1a phosphoinositide-3 kinase (PI3K) receptors, significantly changed the proportion of defective particles and viral genomes (specifically deletion-containing viral genomes) in a strain-specific manner, under conditions that minimize multiple cycles of replication. Alpelisib pre-treatment of cells led to an increase in defective particles in the A/H3N2 strain, while the A/H1N1 strain showed a decrease in total viral particles. In the same infections, we found that defective viral genomes of polymerase and antigenic segments increased in the A/H1N1 strain, while the total particles decreased suggesting defective interference. We also found that the average deletion size in polymerase complex viral genomes increased in both the A/H3N2 and A/H1N1 strains. The A/H1N1 strain, additionally showed a dose-dependent increase in total number of defective viral genomes. In sum, we provide evidence that host cell metabolism can increase the production of defective viral genomes and particles at an early stage of infection, shifting the makeup of the infection and potential interactions among virions. Given that Influenza A defective viral genomes can inhibit pathogenesis, our study presents a new line of investigation into metabolic states associated with less severe flu infection and the potential induction of these states with metabolic drugs.

Electrophoretic mobility confirms reassortment bias among geographic isolates of segmented RNA phages.

BACKGROUND: Sex presents evolutionary costs and benefits, leading to the expectation that the amount of genetic exchange should vary in conditions with contrasting cost-benefit equations. Like eukaryotes, viruses also engage in sex, but the rate of genetic exchange is often assumed to be a relatively invariant property of a particular virus. However, the rates of genetic exchange can vary within one type of virus according to geography, as highlighted by phylogeographic studies of cystoviruses. Here we merge environmental microbiology with experimental evolution to examine sex in a diverse set of cystoviruses, consisting of the bacteriophage ϕ6 and its relatives. To quantify reassortment we manipulated - by experimental evolution - electrophoretic mobility of intact virus particles for use as a phenotypic marker to estimate genetic exchange. RESULTS: We generated descendants of ϕ6 that exhibited fast and slow mobility during gel electrophoresis. We identified mutations associated with slow and fast phenotypes using whole genome sequencing and used crosses to establish the production of hybrids of intermediate mobility. We documented natural variation in electrophoretic mobility among environmental isolates of cystoviruses and used crosses against a common fast mobility ϕ6 strain to monitor the production of hybrids with intermediate mobility, thus estimating the amount of genetic exchange. Cystoviruses from different geographic locations have very different reassortment rates when measured against ϕ6, with viruses isolated from California showing higher reassortment rates than those from the Northeastern US. CONCLUSIONS: The results confirm that cystoviruses from different geographic locations have remarkably different reassortment rates -despite similar genome structure and replication mechanisms- and that these differences are in large part due to sexual reproduction. This suggests that particular viruses may indeed exhibit diverse sexual behavior, but wide geographic sampling, across varying environmental conditions may be necessary to characterize the full repertoire. Variation in reassortment rates can assist in the delineation of viral populations and is likely to provide insight into important viral evolutionary dynamics including the rate of coinfection, virulence, and host range shifts. Electrophoretic mobility may be an indicator of important determinants of fitness and the techniques herein can be applied to the study of other viruses.

Black box of phage-bacterium interactions: exploring alternative phage infection strategies.

The canonical lytic-lysogenic binary has been challenged in recent years, as more evidence has emerged on alternative bacteriophage infection strategies. These infection modes are little studied, and yet they appear to be more abundant and ubiquitous in nature than previously recognized, and can play a significant role in the ecology and evolution of their bacterial hosts. In this review, we discuss the extent, causes and consequences of alternative phage lifestyles, and clarify conceptual and terminological confusion to facilitate research progress. We propose distinct definitions for the terms 'pseudolysogeny' and 'productive or non-productive chronic infection', and distinguish them from the carrier state life cycle, which describes a population-level phenomenon. Our review also finds that phages may change their infection modes in response to environmental conditions or the physiological state of the host cell. We outline known molecular mechanisms underlying the alternative phage-host interactions, including specific genetic pathways and their considerable biotechnological potential. Moreover, we discuss potential implications of the alternative phage lifestyles for microbial biology and ecosystem functioning, as well as applied topics such as phage therapy.

A comparison of amplification methods to detect Avian Influenza viruses in California wetlands targeted via remote sensing of waterfowl.

Migratory waterfowl, including geese and ducks, are indicated as the primary reservoir of avian influenza viruses (AIv) which can be subsequently spread to commercial poultry. The US Department of Agriculture's (USDA) surveillance efforts of waterfowl for AIv have been largely discontinued in the contiguous United States. Consequently, the use of technologies to identify areas of high waterfowl density and detect the presence of AIv in habitat such as wetlands has become imperative. Here we identified two high waterfowl density areas in California using processed NEXt generation RADar (NEXRAD) and collected water samples to test the efficacy of two tangential flow ultrafiltration methods and two nucleic acid based AIv detection assays. Whole-segment amplification and long-read sequencing yielded more positive samples than standard M-segment qPCR methods (57.6% versus 3.0%, p < .0001). We determined that this difference in positivity was due to mismatches in published primers to our samples and that these mismatches would result in failing to detect in the vast majority of currently sequenced AIv genomes in public databases. The whole segment sequences were subsequently used to provide subtype and potential host information of the AIv environmental reservoir. There was no statistically significant difference in sequencing reads recovered from the RexeedTM filtration compared to the unfiltered surface water. This overall approach combining remote sensing, filtration and sequencing provides a novel and potentially more effective, surveillance approach for AIv.

SARS-CoV-2 detection and genomic sequencing from hospital surface samples collected at UC Davis.

RATIONALE: There is little doubt that aerosols play a major role in the transmission of SARS-CoV-2. The significance of the presence and infectivity of this virus on environmental surfaces, especially in a hospital setting, remains less clear. OBJECTIVES: We aimed to analyze surface swabs for SARS-CoV-2 RNA and infectivity, and to determine their suitability for sequence analysis. METHODS: Samples were collected during two waves of COVID-19 at the University of California, Davis Medical Center, in COVID-19 patient serving and staff congregation areas. qRT-PCR positive samples were investigated in Vero cell cultures for cytopathic effects and phylogenetically assessed by whole genome sequencing. MEASUREMENTS AND MAIN RESULTS: Improved cleaning and patient management practices between April and August 2020 were associated with a substantial reduction of SARS-CoV-2 qRT-PCR positivity (from 11% to 2%) in hospital surface samples. Even though we recovered near-complete genome sequences in some, none of the positive samples (11 of 224 total) caused cytopathic effects in cultured cells suggesting this nucleic acid was either not associated with intact virions, or they were present in insufficient numbers for infectivity. Phylogenetic analysis suggested that the SARS-CoV-2 genomes of the positive samples were derived from hospitalized patients. Genomic sequences isolated from qRT-PCR negative samples indicate a superior sensitivity of viral detection by sequencing. CONCLUSIONS: This study confirms the low likelihood that SARS-CoV-2 contamination on hospital surfaces contains infectious virus, disputing the importance of fomites in COVID-19 transmission. Ours is the first report on recovering near-complete SARS-CoV-2 genome sequences directly from environmental surface swabs.

Uncovering Virus-Virus Interactions by Unifying Approaches and Harnessing High-Throughput Tools.

Virus-host interactions have received much attention in virology. Virus-virus interactions can occur when >1 virus infects a host and can be deemed social when one virus affects the fitness of another virus, as in the well-known case of superinfection exclusion. Coinfection and subsequent social interactions can change viral pathogenicity, host range, and genetic composition, with implications for human health and viral evolution. I propose that this field can be advanced by bringing new perspectives into virology (e.g., social evolution theory) and uniting disciplinary divides within virology (classical, host-focused, and ecoevolutionary). The development of novel high-throughput tools that meld molecular and evolutionary approaches can harness viral diversity as an experimental asset to understand complex viral social interactions. A greater knowledge of virus-virus interactions will lead to the reformulation of basic concepts of virology and advances in applied virology, with new treatments that harness interactions between viruses to fight viral and bacterial infections.

Next-generation sequencing of dsRNA is greatly improved by treatment with the inexpensive denaturing reagent DMSO.

dsRNA is the genetic material of important viruses and a key component of RNA interference-based immunity in eukaryotes. Previous studies have noted difficulties in determining the sequence of dsRNA molecules that have affected studies of immune function and estimates of viral diversity in nature. DMSO has been used to denature dsRNA prior to the reverse-transcription stage to improve reverse transcriptase PCR and Sanger sequencing. We systematically tested the utility of DMSO to improve the sequencing yield of a dsRNA virus (Φ6) in a short-read next-generation sequencing platform. DMSO treatment improved sequencing read recovery by over two orders of magnitude, even when RNA and cDNA concentrations were below the limit of detection. We also tested the effects of DMSO on a mock eukaryotic viral community and found that dsRNA virus reads increased with DMSO treatment. Furthermore, we provide evidence that DMSO treatment does not adversely affect recovery of reads from a ssRNA viral genome (influenza A/California/07/2009). We suggest that up to 50 % DMSO treatment be used prior to cDNA synthesis when samples of interest are composed of or may contain dsRNA.

Global phylogeography and ancient evolution of the widespread human gut virus crAssphage.

Microbiomes are vast communities of microorganisms and viruses that populate all natural ecosystems. Viruses have been considered to be the most variable component of microbiomes, as supported by virome surveys and examples of high genomic mosaicism. However, recent evidence suggests that the human gut virome is remarkably stable compared with that of other environments. Here, we investigate the origin, evolution and epidemiology of crAssphage, a widespread human gut virus. Through a global collaboration, we obtained DNA sequences of crAssphage from more than one-third of the world's countries and showed that the phylogeography of crAssphage is locally clustered within countries, cities and individuals. We also found fully colinear crAssphage-like genomes in both Old-World and New-World primates, suggesting that the association of crAssphage with primates may be millions of years old. Finally, by exploiting a large cohort of more than 1,000 individuals, we tested whether crAssphage is associated with bacterial taxonomic groups of the gut microbiome, diverse human health parameters and a wide range of dietary factors. We identified strong correlations with different clades of bacteria that are related to Bacteroidetes and weak associations with several diet categories, but no significant association with health or disease. We conclude that crAssphage is a benign cosmopolitan virus that may have coevolved with the human lineage and is an integral part of the normal human gut virome.

Viral coinfection is shaped by host ecology and virus-virus interactions across diverse microbial taxa and environments.

Infection of more than one virus in a host, coinfection, is common across taxa and environments. Viral coinfection can enable genetic exchange, alter the dynamics of infections, and change the course of viral evolution. Yet, a systematic test of the factors explaining variation in viral coinfection across different taxa and environments awaits completion. Here I employ three microbial data sets of virus-host interactions covering cross-infectivity, culture coinfection, and single-cell coinfection (total: 6,564 microbial hosts, 13,103 viruses) to provide a broad, comprehensive picture of the ecological and biological factors shaping viral coinfection. I found evidence that ecology and virus-virus interactions are recurrent factors shaping coinfection patterns. Host ecology was a consistent and strong predictor of coinfection across all three data sets: cross-infectivity, culture coinfection, and single-cell coinfection. Host phylogeny or taxonomy was a less consistent predictor, being weak or absent in the cross-infectivity and single-cell coinfection models, yet it was the strongest predictor in the culture coinfection model. Virus-virus interactions strongly affected coinfection. In the largest test of superinfection exclusion to date, prophage sequences reduced culture coinfection by other prophages, with a weaker effect on extrachromosomal virus coinfection. At the single-cell level, prophage sequences eliminated coinfection. Virus-virus interactions also increased culture coinfection with ssDNA-dsDNA coinfections >2× more likely than ssDNA-only coinfections. The presence of CRISPR spacers was associated with a ∼50% reduction in single-cell coinfection in a marine bacteria, despite the absence of exact spacer matches in any active infection. Collectively, these results suggest the environment bacteria inhabit and the interactions among surrounding viruses are two factors consistently shaping viral coinfection patterns. These findings highlight the role of virus-virus interactions in coinfection with implications for phage therapy, microbiome dynamics, and viral infection treatments.

Sociovirology: Conflict, Cooperation, and Communication among Viruses.

Viruses are involved in various interactions both within and between infected cells. Social evolution theory offers a conceptual framework for how virus-virus interactions, ranging from conflict to cooperation, have evolved. A critical examination of these interactions could expand our understanding of viruses and be exploited for epidemiological and medical interventions.

Contextual organismality: Beyond pattern to process in the emergence of organisms.

Biologists have taken the concept of organism largely for granted. However, advances in the study of chimerism, symbiosis, bacterial-eukaryote associations, and microbial behavior have prompted a redefinition of organisms as biological entities exhibiting low conflict and high cooperation among their parts. This expanded view identifies organisms in evolutionary time. However, the ecological processes, mechanisms, and traits that drive the formation of organisms remain poorly understood. Recognizing that organismality can be context dependent, we advocate elucidating the ecological contexts under which entities do or do not act as organisms. Here we develop a "contextual organismality" framework and provide examples of entities, such as honey bee colonies, tumors, and bacterial swarms, that can act as organisms under specific life history, resource, or other ecological circumstances. We suggest that context dependence may be a stepping stone to the development of increased organismal unification, as the most integrated biological entities generally show little context dependence. Recognizing that organismality is contextual can identify common patterns and testable hypotheses across different entities. The contextual organismality framework can illuminate timeless as well as pressing issues in biology, including topics as disparate as cancer emergence, genomic conflict, evolution of symbiosis, and the role of the microbiota in impacting host phenotype.

No sex-biased dispersal in a primate with an uncommon social system-cooperative polyandry.

An influential hypothesis proposed by Greenwood (1980) suggests that different mating systems result in female and male-biased dispersal, respectively, in birds and mammals. However, other aspects of social structure and behavior can also shape sex-biased dispersal. Although sex-specific patterns of kin cooperation are expected to affect the benefits of philopatry and dispersal patterns, empirical evidence is scarce. Unlike many mammals, Saguinus geoffroyi (Geoffroy's tamarin) has a breeding system in which typically multiple males mate with a single breeding female. Males typically form cooperative reproductive partnerships between relatives, whereas females generally compete for reproductive opportunities. This system of cooperative polyandry is predicted to result in female-biased dispersal, providing an opportunity to test the current hypotheses of sex-biased dispersal. Here we test for evidence of sex-biased dispersal in S. geoffroyi using demographic and genetic data from three populations. We find no sex bias in natal dispersal, contrary to the prediction based on the mating patterns. This pattern was consistent after controlling for the effects of historical population structure. Limited breeding opportunities within social groups likely drive both males and females to disperse, suggesting that dispersal is intimately related to the social context. The integration of genetic and field data revealed that tamarins are another exception to the presumed pattern of male-biased dispersal in mammals. A shift in focus from mating systems to social behavior, which plays a role in most all processes expected to influence sex-bias in dispersal, will be a fruitful target for research both within species and across taxa.