Evolution, Medicine, and Public Health

Parasitism is one of the key, structural, interspecific interactions in ecology. One remarkable parasitic strategy that has been documented in multiple systems is the behavioral manipulation of hosts to increase parasite fitness. While not yet documented in humans, we propose that a ubiquitous zoonotic parasite - Toxoplasma gondii - may change human behavior to favor the parasite by increasing the fitness of the parasites definitive host - cats. Specifically, we assess the possibility that human behavioral changes resulting from chronic, latent T. gondii infection lead to measurable changes in attitudes, actions and dopaminergic responses towards cats that function to increase domestic cat fitness. We assessed the potential role of humans in the T. gondii lifecycle by identifying and testing behavioral changes in humans that benefit the parasite; specifically, human affection for cats. We assessed T. gondii infection status in 68 participants using T. gondii serum antibody testing, and assessed their attitudes towards cats in three ways: i) surveys, ii) participant behavior in the presence of domestic cats, and iii) participant oxytocin levels before and after interactions with cats to assess dopaminergic changes. Only 2 of 68 participants were positive for T. gondii antibodies, limiting statistical power. However, our results indicated that T. gondii-positive participants both reported a greater affection for cats in surveys, and spent more time engaged with cats during behavioral trials than T. gondii-negative participants (87% of study time engaging with cats vs 75%). Oxytocin results were inconclusive.

Aging induces cognitive decline in humans and some other animals. For species that rely on learning and memory for reproduction, impaired cognitive functions may incur severe fitness costs. Here we report age-related cognitive decline in a solitary parasitoid wasp, Venturia canescens, that uses olfactory memories for host seeking and selection. We trained individual wasps to associate an odour with an oviposition reward, and compared their learning and memory performances at different stages of the reproductive life. Wasps between 6- and 14-day-old showed consistently poorer learning and reduced memory retention than young conspecifics, and this tendency increased with age. In this parasitoid insect, aging induces a precocious cognitive decline in reproductive females, which could severely impact their fitness through altered abilities to identify high quality hosts.

BackgroundOlder age is widely considered a risk factor for post-acute sequelae of SARS-CoV-2 infection (PASC), typically attributed to immunosenescence and inflammaging. However, whether this association reflects intrinsic biological ageing or accumulated comorbidity burden remains unclear, with implications for clinical risk stratification. MethodsWe conducted a retrospective cohort study using the Precision PASC Research Cohort (P2RC) from Mass General Brigham, comprising 133,792 COVID-19 patients from 12 hospitals and 20 community health centres in Massachusetts (March 2020-May 2024). PASC was ascertained using a validated computational phenotyping algorithm. We used generalised estimating equations with cluster-robust variance to model PASC risk, causal mediation analysis to decompose age effects through comorbidity burden and acute severity, and specification curve analysis across 768 analytical specifications to assess robustness. FindingsAfter adjustment for comorbidity burden, each decade of age was associated with 6% lower odds of PASC (OR 0.94; 95% CI 0.93-0.95). Causal mediation analysis revealed that comorbidities accounted for 145% of the total age effect, indicating inconsistent mediation wherein ages direct protective effect was masked by its indirect harm through chronic disease accumulation. This protection was age-dependent: adults younger than 65 years retained robust resilience independent of comorbidities (ADE:-0.0042, p<0.001), whereas adults 65 years and older showed complete loss of this protection (ADE: +0.0020, p=0.14). InterpretationLong COVID susceptibility is driven by physiological reserve rather than chronological age until approximately age 65, beyond which age-related protective mechanisms become exhausted. Risk stratification should prioritise comorbidity burden over birth year in younger adults. FundingNational Institute of Allergy and Infectious Diseases (NIAID).

Aging was tracked in a cohort of 99 "retired" sled dogs over four years to characterize the latent dynamics of physiological decline. Animals were randomized to receive either placebo or the reverse transcriptase inhibitor lamivudine for [~]30 months. We employed a variational autoregressive model to integrate longitudinal blood parameters and DNA methylation (DNAm) profiles. The model defines Biological Age (BA) as a signature of irreversible damage with Poissonian statistics, a feature conserved across mammalian scales. Lamivudine modulated age-independent latent variables and temporarily decelerated the DNAm clock in females, but these effects were reversible upon treatment discontinuation and did not alter the long-term BA trajectory. Critically, we show that physiological fluctuations are governed by a single systemic factor - an effective or phenotypic temperature representing an emergent (macroscopic) property. We show that while the rate of damage accumulation (the BA slope) is independent of this temperature, actuarial aging parameters (initial mortality and the Gompertz exponent) are strongly temperature dependent. This supports a model where mortality arises from effective activation across a protective free energy barrier that erodes with age. These findings identify phenotypic temperature as an important control variable governing the kinetics of organism-level failure, offering a compelling target for interventions aimed at extending healthspan by "squaring" the survival curve.

Parental rejection of apparently healthy newborns is widely classified as a behavioural abnormality in captive primate colonies, yet its biological significance remains unclear. In owl monkeys (Aotus nancymaae), parental rejection, defined here as cessation of nursing leading to rescue nursery rearing, is typically lethal for offspring and is transmitted across generations despite reducing offspring survival. Here, we tested whether parental rejection is associated with lifespan and reproductive differences in parents and their surviving offspring. We analysed long-term demographic records from a captive colony of 962 individuals and compared survival and reproductive outcomes between rejector and non-rejector parents using survival analyses and regression-based models. Parents who rejected offspring lived significantly longer than non-rejectors, with an average lifespan advantage of approximately 4-4.5 years in both males and females. This survival difference was concentrated during the prime reproductive period (6-20 years). Well-reared offspring of rejector parents also lived longer than offspring of non-rejectors, with a mean lifespan difference of 1.26 years. Rejector parents produced more offspring overall, but this difference was explained by extended lifespan rather than higher reproductive output per year. Analyses stratified by rejection timing showed no longevity advantage in first-birth rejectors, whereas parents rejecting later-born offspring exhibited longer survival. Together, these findings show that parental rejection is associated with longer lifespan in parents and in their well-reared offspring under captive conditions. These patterns are consistent with altered allocation of parental investment under energetic or environmental stress.

Sex differences in behaviour and life-history trajectories are widespread across species, yet the mechanisms through which mothers shape these differences remain poorly understood. Classic theories emphasize sex-biased allocation at birth or differential energetic investment, but how maternal effects might operate instead through postnatal investment remains understudied. Using long-term demographic and behavioural data from female-philopatric vervet monkeys (Chlorocebus pygerythrus), we examined how maternal age and dominance rank influence offspring sex ratios at birth, survival to adulthood, maternal investment, and offspring social integration in both sons and daughters. Maternal age, but not rank, influenced offspring sex ratios, with older females producing more daughters. Maternal rank was positively associated with daughters survival and social engagement, with estimated effects consistently stronger in daughters than in sons. While both sexes were highly vulnerable to maternal loss, post-hoc trends suggested a potentially steeper effect on sons. Sons received more maternal proximity (under some maternal conditions) and maternal grooming, whereas daughters seemed to gain earlier and greater engagement with other group members and appeared to derive indirect advantages from maternal rank through social exposure. Together, these findings indicate that maternal investment in this species differs in form rather than in magnitude, primarily through postnatal developmental pathways rather than biased allocation at birth. By demonstrating how maternal age and social status shape divergent early-life trajectories, our study highlights the role of early social environments in generating sex-specific life histories. HighlightsO_LISex differences in life-history trajectories can arise through postnatal social development, not only sex allocation at birth; C_LIO_LIIn wild female-philopatric vervets, maternal age (not rank) predicts offspring sex ratios, with older females producing more daughters; C_LIO_LIMaternal rank shows stronger associations with daughters survival and social engagement, while sons were potentially more dependent on maternal presence; C_LIO_LIMaternal investment differs in form rather than magnitude, consistent with role-specific developmental preparation. C_LI

Vertebrate adaptive immunity has long been considered uniquely advantageous for its capacity to recognise and remember a wide diversity of molecular targets, potentially conferring lasting defence from any threatening microbe. However, over the last two decades, results from comparative immunology have called into question the evolutionary benefits of vertebrate adaptive immunity as a defence mechanism, raising the possibility of alternative evolutionary explanations. For instance, the hypothesis that managing the complex and often beneficial host-microbiota associations characteristic of the vertebrate gut may have favoured the evolution of adaptive immunity. Here, we use individual-based simulations to investigate co-evolutionary interactions between hosts and their microbiota and the implication for the evolution of adaptive immunity. We focus on the capacity of adaptive immunity to produce and modify a diverse repertoire of immune receptors by using somatic variation and selective clonal reinforcement, in combination with a reinforcement bias from the innate immune system. Strikingly, we find that a high diversity of rapidly evolving parasites is insufficient to favour the evolution of adaptive immunity. Instead, our findings suggest that neutral and beneficial microbes can play a crucial role in weakening selection on innate immune defence against parasites in favour of the exploitation of beneficial microbes. In turn, this facilitates the emergence of adaptive immunity as a mechanism reducing the risk associated with infrequent parasite infections while exploiting beneficial microbes. In addition, we show that adaptive immunity can subsequently alter selection affecting both innate immune defence and microbe evolution, such that its loss becomes increasingly unlikely with evolutionary time. Together, these results suggest that simultaneous interactions with diverse mutualists and parasites is a compelling selective explanation for the emergence and maintenance of adaptive immunity.

Bats have attracted considerable recent interest for their extraordinary longevity and ability to withstand infection by a range of pathogens without major harm. However, few studies have examined immune responses as a function of age, sex, or social status. We investigated sources of individual immune variation by comparing whole-blood transcriptomes of wild greater spear-nosed bats, Phyllostomus hastatus, before and after ex vivo exposure to lipopolysaccharide, a membrane component of gram-negative bacteria. This species exhibits an extreme harem-polygynous mating system, which has pervasive consequences on life history traits, including male-biased mortality. We observe clear differences in immune responses, with males and older bats each mounting stronger inflammatory responses. Males also show steeper patterns of age-related variation in immune profiles, suggesting their earlier mortality is associated with accelerated immunosenescence. We did not detect largescale differences in immune responses between males of different social status, suggesting that--unlike in many primates--immune variation is not strongly influenced by social adversity. Our findings support recent calls for a more nuanced approach to understanding immune adaptations in bats that considers the diverse ways in which species and individuals differ in ecology, resource allocation, and selection.

The apolipoprotein {varepsilon}4 (APOE {varepsilon}4) isoform directly alters cholesterol and immune biology and is associated with an increased risk of neurodegenerative and cardiometabolic disease in industrialized settings; nevertheless, APOE {varepsilon}4--which is ancestral in humans--has persisted over evolutionary time. One potential explanation is that the costs and benefits of APOE {varepsilon}4 were significantly different in the environments in which humans evolved compared to those we experience today. In support, previous work has suggested that living in a high pathogen environment, engaging in high levels of physical activity, or eating a low fat diet can dampen the detrimental effects of APOE {varepsilon}4, and has revealed positive effects for fertility. However, direct tests of whether APOE isoforms are associated with different biological outcomes in non-industrial versus industrialized contexts are lacking. Working with the Turkana of Kenya and the Orang Asli of Peninsular Malaysia--two Indigenous groups in which individuals of shared ancestry span a continuum of subsistence, non-industrial to urban, industrialized lifestyles--we investigated how APOE genotypes impact cholesterol, immunological, and reproductive traits and tested for genotype x environment (GxE) interactions. First, we confirmed established genotype effects across lifestyles, showing that more APOE {varepsilon}4 alleles are associated with higher total cholesterol, higher LDL cholesterol, and lower HDL cholesterol. Second, we tested for lifestyle interactions, finding lifestyle-dependent effects of genotype on innate immune biomarkers in the Orang Asli but not Turkana. Finally, we show that more APOE {varepsilon}4 alleles are correlated with an extended reproductive lifespan, however this effect is relatively weak, is not consistent across populations, and does not correspond with a higher reproductive output. Together, our study provides evidence that industrialized environments can modify the biology of APOE {varepsilon}4; however, we find that APOE {varepsilon}4 is not universally beneficial in non-industrial contexts, highlighting the role of local environmental variation in determining its specific costs and benefits.

Hosts have evolved a variety of innate immune responses to pathogens. In many cases, hosts directly detect pathogen-associated molecular patterns (PAMPs) or pathogen effectors to trigger an immune response. However, hosts may also detect pathogens indirectly through guarding, whereby immune receptors monitor the effects of pathogens rather than the pathogens themselves. Guarding likely represents a more difficult evolutionary challenge for pathogens than direct recognition of PAMPs, as infection may require modifying or disrupting guarded host proteins. Recently, self-guarding has been discovered, in which the host target functions as both guard and guardee. Self-guarding appears to present an intractable problem for pathogens: modification of the host target may benefit replication, but also triggers an immune response. If self-guarding creates an apparently inescapable detection mechanism, why are most guarding systems composed of separate guards and guardees? Here, we use mathematical models of within-host pathogen and immune dynamics to compare guarding and self-guarding architectures. We show that self-guarding leads to a more rapid immune response and faster pathogen suppression, but is also more prone to false-positive immune responses, likely imposing greater costs through autoimmunity. We therefore hypothesise that the greater potential for false-positive immune responses may explain the relative scarcity of self-guarding.

Across social species, strong social bonds are linked to health benefits, including reduced disease risk and increased survival. Chronic glucocorticoid exposure, frequently associated with negative health outcomes, may mediate this relationship, as bonds may reduce stressor exposure or buffer physiological responses. Among primates, these relationships have mostly been studied in female-bonded species, where kinship shapes cooperation and access to resources. Whether bonds confer simsilar benefits in species with different social structures - especially bonds between non-kin - remains unclear. We tested whether strong affiliative bonds were associated with glucocorticoid production in wild adult chimpanzees using 22 years of behavioural and urinary cortisol data. Bonds were quantified for same-sex adult dyads using an index of party association, proximity, and grooming. Bond strength was measured by averaging each individuals top three bonds per year. Stronger bonds predicted lower cortisol in females but higher cortisol in males, a pattern that persisted after accounting for dominance rank, aggression, and contextual stressors. In this male-bonded species, stronger male bonds predicted higher physiological costs, while stronger female bonds, though weaker, appeared to attenuate stress. Our results challenge the assumption that social bonds are universally health-promoting, and suggest their physiological consequences vary with sex and social organization.

Evolution of drug resistance to one drug can alter the minimum inhibitory concentration to another drug. This phenomenon, known as a collateral effect, can manifest as either cross-resistance or collateral sensitivity. Various patterns of collateral effects have been observed experimentally. Repeated adaptation from the same parental strain may result in variable collateral effects; this is non-repeatability. Additionally, adaptation of a pathogen to one drug may produce a specific collateral effect to a second drug, while altering the order of drug exposure can result in a different, or even absent, collateral effect. This phenomenon is termed unidirectionality. The genetic and evolutionary mechanisms underlying these patterns remain incompletely characterised. Here, we propose a frame-work that integrates pharmacodynamics and population genetics and provide minimal examples to explain these patterns and their combinations. Furthermore, we demonstrate that drug concentration and selection regime strongly influence patterns of collateral effects, including repeatability, directionality, and their temporal dynamics.

Influenza infection results from tightly coupled interactions between viral replication, host immune responses, and the emergence of clinical symptoms. While mathematical models have extensively characterized viral and immune dynamics, the mechanistic link between immune activity and disease severity remains poorly understood. Here, we develop an integrative within-host modeling framework that explicitly connects infection dynamics, immune responses, and symptom manifestation through a unified dynamical system. Using murine influenza data, we incorporate key immune components alongside a mechanistic representation of symptom progression, quantified via host weight loss. Our analysis identifies inflammatory signaling, particularly TNF--mediated pathways, as a central driver linking immune activity to symptom severity. Importantly, we demonstrate that age-dependent alterations in immune regulation reshape this coupling: aged hosts exhibit prolonged inflammatory responses that amplify and sustain symptom burden despite comparable viral kinetics. These results highlight that disease severity cannot be inferred from viral load alone, but instead emerges from the dynamical interplay between immune regulation and host physiology. This framework provides a quantitative basis for understanding age-specific morbidity and offers a foundation for designing interventions that target immune-mediated pathology rather than viral replication alone.

Ageing is traditionally conceived as a continuous process of progressive physiological decline. Recent evidence across multiple species challenges this view, suggesting ageing may proceed through distinct phases. Here we present a rigorous statistical framework to test and refine the two-phase ageing model using longitudinal survival data from Drosophila melanogaster. We analyzed 1,159 individually tracked female flies from the Smurf assay, which identifies a transition from a non-Smurf state to a Smurf state characterized by increased intestinal permeability that precedes death. Using non-parametric hazard rate estimation followed by mechanistic modelling, we reveal three key findings. First, the Smurf transition rate follows a Gompertz-Makeham law, increasing exponentially with age. Second, contrary to previous constant-rate assumptions, newly transitioned Smurf flies exhibit remarkably high mortality - approximately 40% die within 24 hours - followed by an exponential decline in death rate. Third, we identified a subtle but statistically significant negative dependence between time spent non-Smurf and subsequent Smurf lifespan, though this relationship varies: flies transitioning before 200 hours show minimal dependence and higher early mortality. Our best-fit model captures the bimodal nature of mortality curves using simple, biologically interpretable functions. Validation using data from two mouse strains confirms the broader applicability of this framework. These results establish a quantitative foundation for the two-phase ageing paradigm and highlight a critical period of vulnerability immediately following the physiological transition to frailty.

Declining vaccine coverage across the United States has increased the risk of outbreaks of vaccine-preventable diseases. Even when vaccines have low primary failure rates, conventional epidemic theory predicts a strongly nonlinear, positive relationship between vaccine coverage and the fraction of breakthrough infections in vaccinated individuals. These breakthrough infections may generate misconceptions that vaccines are not working and accelerate declines in confidence and coverage. Here, we set out to test predictions of conventional epidemic theory that assumes random mixing between individuals irrespective of vaccine status. In contrast to expectations from random mixing models, we find a far lower fraction of breakthrough infections in measles outbreak data from seven states in the United States. To explore this discrepancy, we evaluate an alternative, compartmental disease model that accounts for preferential mixing ( assortativity) between people with the same vaccination status. The model predicts significantly lower fractions of breakthrough infections, consistent with observations from measlesoutbreak data. Next, we leverage the deviation between statewide and school-level vaccine MMR coverage across kindergartens in sixteen states, finding substantial assortativity in all cases. Our model accounting for preferential mixing predicts the total number of breakthrough infections is nonlinear, peaking at intermediate coverage below vaccine-derived herd immunity. Nationally, 94% of counties that report MMR coverage are above the model-predicted breakthrough-maximizing coverage, suggesting that they are at risk for increasing breakthrough infections if coverage declines. Vaccination outreach and monitoring campaigns should develop proactive strategies to contextualize breakthrough infections before low levels of primary failure contributes to population-scale increases in preventable disease. Significance StatementInfections among vaccinated people may exacerbate vaccine hesitancy. Despite reports of breakthrough infections within ongoing measles outbreaks, we show that the realized fraction of breakthrough infections is far lower than predicted by conventional epidemic theory that assumes random mixing. Combining epidemic models and school-level vaccine coverage data, we show that breakthrough infections may be partially limited via preferential mixing ( assortativity) based on vaccination status. Given current MMR coverage, most of the country is at risk for increasing breakthrough infections if vaccine coverage declines further. We conclude that enhanced vaccine monitoring and outreach campaigns are needed to confront a potential positive feedback loop between increasing breakthrough infections and declining vaccine coverage that could substantially increase the burden of vaccine-preventable disease.

Parasite defense is the ability of a host to minimize fitness loss to parasites, and it is among the most variable phenotypes in natural populations. We expect this variation in defense to facilitate rapid adaptation under parasite-mediated selection. What we do not know is what traits are most likely to evolve in response to this selection. A common assumption is that the most defended hosts are the most resistant, meaning they limit the establishment and growth of infecting parasites. Under this assumption, resistance traits should evolve readily under parasite selection. Resistance is, however, just one of many strategies hosts use to defend against parasites, and it does not consistently covary with parasite defense. We accordingly ask: which host traits covary with parasite defense and are thus likely to respond to parasite selection? We use controlled exposures to characterize genetic variation in defense of the nematode Caenorhabditis elegans against its natural microsporidian parasites. We report extensive variation in parasite defense among wild strains of C. elegans: some strains lost 60% of fecundity under parasite exposure, while others were unaffected. We then tested the covariance of defense with two prominent host traits, resistance and reproductive timing. Our results did not support the hypothesis that resistance covaries with defense: strains with lower parasite burden did not have higher relative fecundity under exposure. Our results instead supported the hypothesis that life history covaries with defense: host strains that reproduced quickly had higher relative fecundity under exposure, consistent with the idea that parasites diminish future reproductive opportunities. Moreover, we detected substantial heritability of fecundity traits but low heritability of resistance traits. Together, these findings indicate significant potential for adaptation of wild C. elegans populations to defend against their natural parasites. They further predict that life history traits will evolve rapidly in response to parasite selection. AUTHOR SUMMARYSome hosts fare much better than others in the face of parasite infection. What traits differentiate defended hosts from undefended hosts? The answer to this question is critical for identifying the strategies that best protect hosts from their parasites. It also allows us to predict and interpret the evolution of host populations over the course of epidemics. To address this question, we surveyed wild strains of a tractable model host, the nematode Caenorhabditis elegans, for their response to two species of microsporidian parasites. We found that, on average, parasite exposure substantially impaired the ability of hosts to reproduce. Host strains, however, varied widely: some experienced major losses in fecundity with exposure, while others were highly defended, showing little to no change. We identified reproductive timing as the trait that differentiated defended hosts from undefended hosts. Our results indicate that reproducing quickly was protective, because hosts were able to make most of their offspring before parasites impaired reproduction. We did not find evidence that resistance was protective - hosts with lower parasite burdens did not reproduce better than those with high parasite burdens. These findings give added weight to life history as a major component of host defense against parasites.

HighlightsO_LIDNA damage-induced selection is the underlying cause of ageing. C_LIO_LIFaster metabolising cells naturally spread unless prevented by a deliberate process designed to prevent hyperfunctional diseases like cancer and fibrosis. C_LIO_LIAs a result, slow metabolising mutants reduce the metabolic rate of faster neighbours epigenetically, shifting energy homeostasis to induce insulin resistance, weight gain, inflammation, metabolic syndrome and age-related disease. C_LIO_LIIn post-mitotic tissues, mitochondria are undergoing similar selection and counterselection, contributing to the same metabolic slowdown. C_LIO_LIThe four process model defined by these selection processes explains all major anti-ageing therapies and connects the hallmarks into a mechanistic framework. C_LI Although ageing can be understood in terms of associated hallmarks and biomarkers, the processes which connect and cause these phenotypes are ill-defined. Here we suggest a unifying model of ageing as four distinct processes which connect the major observations and evidence into a single framework. It explains, from a single initial cause to the ultimate outcomes and diseases, why we age and die. We suggest that although DNA damage is crucial to shift homeostasis, ageing itself is not caused by simple DNA damage accumulation. Instead, only specific sites of damage are relevant when they affect selection and the resulting ageing processes. For clarity, each process is given a name. The first process, celerisis, results from the natural course of tissue-level selection for cells with elevated metabolic and proliferative rate. If the damaged DNA site gives the cell a selective advantage, it can spread within the tissue causing hyperfunctional diseases including cancer and fibrosis. However, many ageing phenotypes are more associated with hypofunction. Therefore, we suggest that our tissues have a mechanism to prevent the spread of hyperfunctional cells. In proliferative tissues, a second process, intrinsic ageing, is the result of this defence mechanism induced through cell communication via Notch. Slower metabolising mutants induce epigenetic changes in faster cells, and then epigenetically slowed cells slow other cells, causing gradual metabolic slowdown across tissues. The third process, extrinsic ageing, could then result directly from metabolic slowdown as body cells use less ATP. Mitochondria reduce catabolism, restoring ATP levels by burning less glucose and lipid. Build-up of these fuels in the cytoplasm reduces import, restoring equilibrium but inducing insulin resistance (IR), while the excess fuel is diverted to the adipose, causing weight gain, chronic inflammation, and metabolic syndrome. These outcomes could then combine with intrinsic ageing to induce age-related disease. The final process of mitochondrial selection induces intrinsic ageing of single celled life as well as post-mitotic tissues and organisms. Together, the four processes produce a detailed mechanistic map that explains the evolutionary significance of ageing, removing old paradoxes, and connecting the hallmarks into a causal framework that furthers our understanding. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=176 SRC="FIGDIR/small/701154v1_ufig1.gif" ALT="Figure 1"> View larger version (51K): org.highwire.dtl.DTLVardef@2873e3org.highwire.dtl.DTLVardef@1d05f0aorg.highwire.dtl.DTLVardef@10fa833org.highwire.dtl.DTLVardef@ebe435_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOGraphical abstractC_FLOATNO C_FIG

The emergence of tolerance between distinct social groups is a central question in social evolution, with relevance to both nonhuman primates and early human societies. Ecological factors such as resource heterogeneity and social threats like bachelor male presence have each been proposed as drivers of intergroup proximity, but their combined effects remain unclear. We developed a spatially explicit agent-based model to examine how resource patchiness and bachelor threat jointly shape aggregation dynamics and intergroup tolerance among mixed-sex groups. In the model, groups forage across heterogeneous landscapes and expand their ranges with increasing patchiness. Bachelor males roam independently and pose localized threats, prompting groups to aggregate probabilistically according to threat intensity. Aggregation decisions follow a sigmoid response, and familiarity accumulates through repeated overlap or joint aggregation. Intergroup tolerance thus arises from encounter histories rather than being preprogrammed. Simulations show that resource heterogeneity promotes tolerance by increasing overlap and encounter frequency, while bachelor threat induces aggregation as a protective response. Tolerance can also emerge without consistent aggregation, provided that ecological conditions repeatedly bring groups together. When both heterogeneity and threat are high, aggregation and familiarity peak, indicating a synergistic effect. These outcomes are robust across a wide parameter space and do not require explicit coordination or cooperative intent. Our findings highlight how simple behavioral rules embedded in ecological and social contexts can yield complex intergroup outcomes, offering a general framework for understanding the evolution of intergroup tolerance in primates and humans.

Understanding the complex interplay between a host, its diet, and its microbiome is crucial for comprehending an organisms health and adaptability. Diet impacts both the host and microbiome, which then influence each other. We used black soldier fly larvae (Hermetia illucens) as a model to investigate this tripartite interaction due to its resilience and bioconversion capabilities. We analyzed life-history traits and metatranscriptomics in larvae fed three diets: carbohydrate-rich, protein-rich, and balanced. Our results showed that dietary macronutrients correlated with shifts in the microbial community and gene expression. The carbohydrate-rich diet, in particular, led to increased microbial diversity and carbohydrate metabolism transcripts. However, this diet also negatively affected larval weight and development, suggesting potential host control over the microbiome. Overall, black soldier fly performance was highest on the balanced diet. This study highlights the black soldier flys resilience and its value as a model for exploring host-diet-microbe interactions. Significance StatementUnderstanding the intricate interplay between an organism, its diet, and its microbiome is fundamental to health and adaptability. This complex tripartite relationship, where dietary macronutrients influence microbial communities and their gene expression, while the host maintains control, is crucial for addressing global challenges from sustainable food systems to personalized medicine. Using the black soldier fly as a resilience model, our metatranscriptomic study reveals how specific dietary shifts impact both host and microbial gene expression, providing mechanistic insights into nutrient utilization and adaptability with broad implications for diverse biological systems, including animals and humans.

The COVID-19 pandemic saw successive emergence and global spread of novel viral variants, exhibiting enhanced transmissibility or evasion of immunity. While the genotypic and phenotypic basis of SARS-CoV-2 variants have been extensively characterized, the evolutionary factors governing their patterns of emergence are less well understood. In this study we systematically investigated how the invasion dynamics of viral variants depend on variant phenotype (increased transmissibility or immune evasion), source (local evolution vs importation), the timing of introduction, the distribution of population susceptibility, and the contact network structure. Using a stochastic multi-strain epidemic model, we find that strains with only a transmission advantage are more likely to emerge earlier in the epidemic, and rapidly and predictably dominate the viral population. In contrast, immune-escape variants tend to linger at low prevalence for extended time periods after emergence, avoiding detection, until a critical amount of immunity has built up in the population and they begin to rapidly outcompete existing strains. We find that two common features of realistic human contact networks---heterogeneity in contacts (overdispersion) and clustering---lead to more punctuated evolutionary dynamics. This work provides insight into past dynamics of SARS-CoV-2 variants and can help define planning scenarios for future epidemic modeling efforts.