Co-founding ant queens prevent disease by performing prophylactic undertaking behaviour

Abstract Background Social insects form densely crowded societies in environments with high pathogen loads, but have evolved collective defences that mitigate the impact of disease. However, colony-founding queens lack this protection and suffer high rates of mortality. The impact of pathogens may be exacerbated in species where queens found colonies together, as healthy individuals may contract pathogens from infectious co-founders. Therefore, we tested whether ant queens avoid founding colonies with pathogen-exposed conspecifics and how they might limit disease transmission from infectious individuals. Results Using Lasius niger queens and a naturally infecting fungal pathogen Metarhizium brunneum, we observed that queens were equally likely to found colonies with another pathogen-exposed or sham-treated queen. However, when one queen died, the surviving individual performed biting, burial and removal of the corpse. These undertaking behaviours were performed prophylactically, i.e. targeted equally towards non-infected and infected corpses, as well as carried out before infected corpses became infectious. Biting and burial reduced the risk of the queens contracting and dying from disease from an infectious corpse of a dead co-foundress. Conclusions We show that co-founding ant queens express undertaking behaviours that, in mature colonies, are performed exclusively by workers. Such infection avoidance behaviours act before the queens can contract the disease and will therefore improve the overall chance of colony founding success in ant queens

Environmental risk factors for Toxoplasma gondii infections and the impact of latent infections on allostatic load in residents of Central North Carolina

Abstract Background Toxoplasma gondii infection can be acquired through ingestion of infectious tissue cysts in undercooked meat or environmental oocysts excreted by cats. This cross-sectional study assessed environmental risk factors for T. gondii infections and an association between latent infections and a measure of physiologic dysregulation known as allostatic load. Methods Serum samples from 206 adults in the Durham-Chapel Hill, North Carolina area were tested for immunoglobulin (IgG) responses to T. gondii using commercial ELISA kits. Allostatic load was estimated as a sum of 15 serum biomarkers of metabolic, neuroendocrine and immune functions dichotomized at distribution-based cutoffs. Vegetated land cover within 500 m of residences was estimated using 1 m resolution data from US EPA’s EnviroAtlas. Results Handling soil with bare hands at least weekly and currently owning a cat were associated with 5.3 (95% confidence limits 1.4; 20.7) and 10.0 (2.0; 50.6) adjusted odds ratios (aOR) of T. gondii seropositivity, respectively. There was also a significant positive interaction effect of handling soil and owning cats on seropositivity. An interquartile range increase in weighted mean vegetated land cover within 500 m of residence was associated with 3.7 (1.5; 9.1) aOR of T. gondii seropositivity. Greater age and consumption of undercooked pork were other significant predictors of seropositivity. In turn, T. gondii seropositivity was associated with 61% (13%; 130%) greater adjusted mean allostatic load compared to seronegative individuals. In contrast, greater vegetated land cover around residence was associated with significantly reduced allostatic load in both seronegative (p < 0.0001) and seropositive (p = 0.004) individuals. Conclusions Residents of greener areas may be at a higher risk of acquiring T. gondii infections through inadvertent ingestion of soil contaminated with cat feces. T. gondii infections may partially offset health benefits of exposure to the natural living environment

Parasite avoidance strategies in a natural population of a social primate

Les pressions de sélection exercées par les parasites ont permis l’évolution de mécanismes complexes de défense chez les espèces hôtes qui limitent la transmission parasitaire. En complément de leur système immunitaire physiologique, les animaux ont développé un « système immunitaire comportemental » comprenant un ensemble sophistiqué de stratégies d’évitement parasitaire représentant une première ligne de défense pour diminuer la probabilité de rencontre avec différents parasites. Cependant, ces stratégies comportementales n’ont été que peu étudiées chez les espèces de mammifères vivant en milieu naturel. Au cours de ma thèse, j’ai donc étudié les stratégies d’évitement parasitaire dans une population sauvage de mandrills (Mandrillus sphinx), un primate de l’Ancien Monde vivant dans les forêts denses équatoriales d’Afrique et soumis à de forces pressions parasitaires. Je me suis en particulier intéressée aux différentes stratégies comportementales qui ont évolué en réponse au risque de contamination par deux types distincts de parasites gastro-intestinaux présentant des traits d’histoire de vie et des modes de transmission contrastés : les nématodes, transmis par l’environnement, et les protozoaires, transmis par contacts sociaux. A partir d’observations récoltées sur le long-terme, de test expérimentaux et d’analyses chimiques, mes études ont mis en évidence deux stratégies comportementales différentes, soulignant le lien étroit entre l’écologie des parasites et la réponse comportementale des hôtes. D’une part, les mandrills évitent les matières fécales lorsqu’ils fourragent et évitent également les habitats précédemment contaminés par des nématodes fécaux émis lors de la dernière visite de ces habitats. D’autre part, les mandrills évitent de toiletter leurs partenaires sociaux parasités par des protozoaires fécaux, particulièrement autour de la zone anale. Cette stratégie comportementale s’avère être efficace puisque les individus parasités présentent des kystes infectieux de protozoaires sur leurs corps, concentrés au niveau de la zone anale, et la richesse en protozoaire des individus augmente lorsqu’ils toilettent des congénères très parasités. De plus, nous avons montré que cet évitement des individus parasités était guidé par un mécanisme olfactif : les protozoaires influencent l’odeur des matières fécales et les individus discriminent et évitent l’odeur des matières fécales provenant d’individus parasités. Cette plasticité comportementale face au risque parasitaire pourrait constituer un des mécanismes majeurs permettant aux espèces sociales de diminuer le risque accru de contamination associé à la vie en groupe. L’ensemble de nos résultats permettent de mieux appréhender les conséquences évolutives des pressions de sélection exercées par les parasites sur différentes caractéristiques socio-écologiques des animaux, tels que l’utilisation de l’espace et les comportements sociaux.Parasite-mediated selection has driven the emergence of complex hosts’ defense mechanisms to limit the spread of parasites. In addition to their physiological immune system, animals have developed a “behavioral immune system” comprising a sophisticated set of parasite avoidance strategies that represents a first line of defense to decrease parasite encounter rates. However, behavioral adaptations to the threat of parasites have been poorly investigated in wild populations of mammals. In an attempt to fill this gap, during my PhD, I studied parasite avoidance strategies in a wild group of mandrills (Mandrillus sphinx), an Old World primate inhabiting dense equatorial rainforests of Africa and facing intensive parasite pressures in its natural habitat. In particular, I investigated the different behavioral strategies of defense that evolved to decrease contamination risk by two different classes of gastro-intestinal parasites exhibiting contrasted life-history traits and modes of transmission: environmentally transmitted nematodes and socially transmitted protozoa. Based on long-term observations, controlled experiments and chemical analyses, my studies document two distinct behavioral strategies emphasizing the close relationship between parasites’ ecology and hosts’ behavioral responses. On the one hand, mandrills exhibit fecal avoidance behavior when foraging and also avoid ranging in habitats previously contaminated with fecal nematodes released during the previous visit. On the other hand, mandrills avoid grooming social partners highly parasitized with fecal protozoa, particularly around the peri-anal area. This behavioral strategy appears to be operational because parasitized individuals harbor infectious protozoan cysts on their body, concentrated on the peri-anal region, and individual’s protozoan richness increases when grooming highly parasitized conspecifics. We further found that avoidance of parasitized individuals is guided by an olfactory mechanism, as protozoa influence the host’s fecal odor and mandrills discriminate and selectively avoid olfactory cues from individuals parasitized with protozoa. Such parasite-induced behavioral plasticity could be one of the major mechanisms allowing social species to cope with the increased risk of parasitism associated with group-living. Altogether, these findings shed light on the evolutionary consequences of parasite-mediated selection on several socioecological characteristics of animals, including space use and social behavior

Unconditional care from close maternal kin in the face of parasites

International audienceSeveral species mitigate relationships according to their conspecifics' parasite status. Yet, this defence strategy comes with the costs of depriving individuals from valuable social bonds. Animals therefore face a trade-off between the costs of pathogen exposure and the benefits of social relationships. According to the models of social evolution, social bonds are highly kin-biased. However, whether kinship mitigates social avoidance of contagious individuals has never been tested so far. Here, we build on previous research to demonstrate that mandrills (Mandrillus sphinx) modulate social avoidance of contagious individuals according to kinship: individuals do not avoid grooming their close maternal kin when contagious (parasitized with oro-faecally transmitted protozoa), although they do for more distant or non-kin. While individuals' parasite status has seldom been considered as a trait impacting social relationships in animals, this study goes a step beyond by showing that kinship balances the effect of health status on social behaviour in a non-human primate

Table S3. Groomed partners and top-groomed partners in common for each kin category (mother-daughter / maternal half-sisters / paternal half-sisters / unrelated females). from Mother-to-daughter transmission of hygienic anti-parasite behaviour in mandrills

For each dyad of females each year, we considered the total number of groomed partners and top-groomed partners in common between these two females over the total number of groomed partners for both females. We considered as top-groomed partners those that were groomed more than 10% of the time that female spent grooming that year. The sample sizes in brackets indicate the number of dyad.year

Table S2. Summary of the model investigating the effects of female traits (age, dominance rank, and sociality level; see methods) on female.annual hygienic index in females for whom few grooming events (10-19) were recorded. from Mother-to-daughter transmission of hygienic anti-parasite behaviour in mandrills

To test for significant differences between levels of female dominance rank, we changed the reference level sequentially

Figure S1. Repeatability of female.annual HI according to different thresholds of the minimum number of grooming events considered per female.year. from Mother-to-daughter transmission of hygienic anti-parasite behaviour in mandrills

The black line, grey area and blue line indicate, respectively, repeatability estimates, confidence intervals, and associated p-values according to different thresholds. The blue dotted line indicates the limit of significance (p = 0.05). Numbers in parentheses below threshold values indicate the associated sample sizes (number of female.years) along with the number of different females involved

Table S1. Summary of the model investigating the effect of female.annual PRG on females’ monthly protozoan richness in females for whom few grooming events (10-19) were recorded. from Mother-to-daughter transmission of hygienic anti-parasite behaviour in mandrills

Social animals are particularly exposed to infectious diseases. Pathogen-driven selection pressures have thus favoured the evolution of behavioural adaptations to decrease transmission risk such as the avoidance of contagious individuals. Yet, such strategies deprive individuals of valuable social interactions, generating a cost-benefit trade-off between pathogen avoidance and social opportunities. Recent studies revealed that hosts differ in these behavioural defences but the determinants driving such inter-individual variation remain understudied. Using 6 years of behavioural and parasite data on a large natural population of mandrills (Mandrillus sphinx), we showed that, when parasite prevalence was high in the population, females avoided grooming their conspecifics' peri-anal region (PAR), where contagious gastro-intestinal parasites accumulate. Females varied, however, in their propensity to avoid this risky body region: across years, some females consistently avoided grooming it, while others did not. Interestingly, hygienic females, i.e. those avoiding the PAR, were less parasitized than non-hygienic females. Finally, age, dominance rank and grooming frequency did not influence a female's hygiene but both mother–daughter and maternal half-sisters exhibited similar hygienic levels, whereas paternal half-sisters and non-kin dyads did not, suggesting a social transmission of this behaviour. Our study emphasizes that the social inheritance of hygiene may structure behavioural resistance to pathogens in host populations with potential consequences on the dynamics of infectious diseases

Appendix S1: from Mother-to-daughter transmission of hygienic anti-parasite behaviour in mandrills

This appendix provides supplementary materials and results

Faecal avoidance differs between the sexes but not with nematode infection risk in mandrills

International audienceAnimals have evolved a wide range of behaviours that act as barriers to decrease the risk of parasite infection. Faecal avoidance may, for example, limit contact with orofaecally transmitted parasites, such as gastrointestinal nematodes. When present in faeces, however, nematode eggs need to mature before reaching their infective stage. If strategies have evolved in hosts to specifically avoid nematodes, old faeces with infective larvae should elicit stronger avoidance behaviour than fresh faeces that contain noninfective stages. Here, we carried out two experiments to test the hypothesis that mandrills, Mandrillus sphinx, an Old-World primate, exhibit specific behavioural strategies to avoid nematode infection. Our results show that individuals did not avoid faeces in a nonfeeding context but did avoid eating food items contaminated with faecal material, females more so than males. However, neither the presence of nematodes nor the age of faeces influenced the level of avoidance observed, suggesting that mandrills avoid faecal material in general rather than nematodes specifically when foraging