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Prugnolle, F.

Publications and source records attributed to Prugnolle, F..

18 recordsLinked to original sources

Genomic signatures of selection and putative adaptive introgression during the African expansion of the house mouse

How species adapt to novel environments following biological invasion remains a central question in evolutionary biology. The recent human-mediated expansion of the western house mouse (Mus musculus domesticus) across Africa provides an opportunity to investigate the genomic basis of these rapid evolutionary responses. Using whole-genome data from 218 wild mice sampled across Europe and Africa, we combined complementary genome-wide differentiation, genotype-environment association, haplotype-based selection, and localized introgression analyses to investigate genomic signatures of selection and assess the contribution of interspecific gene flow from the native congener Mus spretus to these patterns. Genome-wide differentiation analyses identified candidate regions enriched for immune and epithelial-barrier functions, chemosensory perception, and neural or developmental pathways. Genotype-environment association analyses recovered fewer candidates linked mainly to precipitation, whereas haplotype-based scans highlighted recent selective signals involving sensory, immune, and neural functions. Across analyses, candidate regions were dominated by non-coding variation, supporting a predominantly regulatory and likely polygenic genomic architecture. Although excess allele sharing with M. spretus varied among populations, overlap between introgression and selection candidates was limited but greater than expected by chance. Several overlapping regions were also present in European populations, indicating that introgressed variants likely predated African colonization. Overall, our results suggest that the genomic signatures accompanying the African expansion of house mice were driven mainly by selection on M. m. domesticus variation, whereas introgressed M. spretus alleles contributed to a smaller subset of candidate loci and may have played a role in adaptation in African populations.

evolutionary biology↗

Human footprints in the gut: how anthropogenic environments reshape the microbiome of chacma baboons

Anthropogenic pressures are increasingly reshaping wildlife habitats worldwide. These transformations reduce natural areas, but also create new ecological niches, food resources, and environmental stressors, with potential consequences for wildlife behavior, physiology, and morphology. These changes may affect the gut microbiome, a critical component of host health, yet such effects are often inconsistent across species, particularly in wild non-human primates, and remain poorly understood. Here, we investigated how the gut microbiome of chacma baboons (Papio ursinus ursinus), an ecologically flexible generalist, responds to an anthropization gradient. We analyzed 512 fecal samples collected from 33 wild troops across a broad range of anthropogenic environments in the Western Cape, South Africa. Using a multi-metric approach including the Human Footprint Index, land-use variables and dietary proxies derived from stable isotopes, we assessed gut microbial diversity and composition based on 16S rRNA gene (V4) sequencing. Human-altered environments characterized by high Human Footprint and built-up areas were associated with reduced microbial diversity, and compositional and functional shifts, including decline in fiber-degrading taxa and increase in bacteria associated with simple carbohydrate and dairy metabolism. In contrast, highly cultivated areas showed no diversity difference and distinct microbial assemblages, while dietary variation had weaker effects, primarily altering rare taxa. Our results demonstrate that different components of anthropogenic pressure exert contrasting effects on the baboon gut microbiome, reflecting multiple ecological pathways extending beyond diet alone. Microbiome shifts may have implications for host health, potentially increasing susceptibility to pathogens or inflammatory diseases, with consequences for wildlife populations.

ecology↗

The Balancing Act: Olive baboon (Papio anubis) occupancy is associated with resource-related environmental variables rather than relative abundance of predators.

Understanding how the fear of predation acts as a driver of spatial distribution is fundamental to animal behaviour research, yet this relationship is not wholly understood in primates such as baboons. Olive baboons (Papio anubis) have evolved a diverse range of antipredator strategies that reduce, but do not eliminate, predation risk from the large carnivores they encounter across their broad geographic range. This raises a critical question: does the need to access essential resources outweigh the risk of predation when determining habitat selection? We addressed this question by examining the relative influence of three environmental factors and relative predator abundance on olive baboon occupancy patterns and detection probability in Serengeti National Park, Tanzania. Using data from 225 camera traps deployed by the Snapshot Safari program, we fitted three separate Bayesian occupancy models, each incorporating the same three environmental covariates (terrain ruggedness index, distance to nearest river, and Normalized Difference Vegetation Index, NDVI), together with the relative abundance of one of three principal predators (lion, leopard, or spotted hyena). This approach allowed us to assess whether environmental covariates associated with baboon occupancy remained consistent across different predator contexts. Baboon occupancy strongly increased with terrain ruggedness in all three models and consistently decreased with a greater distance to rivers. Vegetation greenness (NDVI) showed a positive association with baboon occupancy, though credible intervals narrowly overlapped zero. NDVI also showed a strong positive relationship with baboon detection probability. Associations between predator relative abundance and baboon occupancy varied between models: the relative abundance of lions and spotted hyenas showed no strong association with baboon occupancy, whereas the relative abundance of leopards was strongly correlated with baboon occupancy, consistent with shared habitat preferences. Our findings demonstrate that, independent of predator presence, olive baboon spatial distribution in the Serengeti is primarily and consistently associated with resource-related environmental features. This study expands our knowledge on the ecological factors that influence primate occupancy by showing that, for a behaviourally flexible species with diverse antipredator strategies, access to essential resources can outweigh spatial avoidance of predators in a multi-predator landscape.

ecology↗

Identification of two genomic cryptotypes of Plasmodium malariae in Africa

Plasmodium malariae is a neglected human malaria parasite that causes persistent, often asymptomatic infections and remains difficult to diagnose. Despite being generally associated with lower prevalence and severity than other malaria parasites, P. malariae represents a significant public health concern, particularly in Africa, but also as a zoonosis in South America with monkey-adapted Plasmodium brasilianum. Plasmodium malariae and P. brasilianum population genetic structure, evolutionary history, and adaptive potential remain poorly understood, largely due to the historical scarcity of whole-genome data. By screening 226 monkey samples from two Latin American countries, we identified 20 Plasmodium-positives across multiple primate species, highlighting the persistence of this parasite in sylvatic transmission cycles. We also investigated the evolutionary history and genetic diversity of P. malariae using whole-genome sequencing data. By combining 79 newly sequenced genomes with 248 publicly available genomes, we analyzed a filtered dataset comprising 179 P. malariae, two P. brasilianum, and two P. malariae-like genomes. Population structure analyses revealed the presence of two genetically distinct but recombining clusters across African P. malariae populations. These clusters occur across multiple African countries at varying frequencies, without clear geographic segregation. Genome-wide scans of genetic differentiation and selection further identified numerous cluster-specific signatures of adaptation, including loci putatively involved in interactions with human hosts and mosquito vectors. Our results provide the first evidence for fine-scale population substructure within African P. malariae and reveal ongoing adaptive processes that may contribute to its persistence and transmission. By uncovering previously unrecognized genetic diversity and selection patterns, this study highlights the importance of population genomic approaches for understanding the evolutionary dynamics of this neglected malaria parasite. Author summaryHuman malaria is most often associated with few well-studied parasites (Plasmodium falciparum and Plasmodium vivax), while other species have received far less attention. One such species is Plasmodium malariae, which often causes long-lasting infections with few or no symptoms. Because infections are difficult to detect, the true impact of this parasite is likely underestimated, particularly in Africa, where it is widespread. A closely related form, known as Plasmodium brasilianum, infects monkeys in South America with transmission between humans and wild animals. In our study, we analyzed the parasite genomes from infected people and monkeys to better understand the genetic diversity of these parasites, their population structure, and the molecular evidence of adaptation. We found evidence that P. brasilianum continues to circulate in several wild monkey species in South America. By analyzing nearly 300 genomes, we discovered that African P. malariae consists of two genetically distinct but recombining groups that coexist across the continent. These groups differ in specific regions of their genomes, including genes likely involved in interactions with human hosts and mosquito vectors. Our results reveal cryptic genetic diversity and structure with evidence of ongoing adaptation. These findings highlight the importance of including neglected parasites in malaria surveillance and control efforts.

genomics↗

Using social network analysis and non-invasive antibody detection to explore pathogen exposure in wildlife communities

Understanding the dynamics of infectious diseases in ecosystems shared with wildlife is a priority for preventing future threats to human, animal health and conservation. However, the collection of ecological and epidemiological data on wild populations has relied on invasive and costly methods which limited the capacity of investigation. Recent technological developments have changed this trend. In Hwange national park and its surrounding area in Zimbabwe, we combined camera trap-based ecological monitoring over a period of 12 months, covering 14 water holes with a fecal-based antibody survey in 16 large herbivore species. A survey involving 52,829 pictures as well as 629 faecal samples collected every 15 days, has shown Through the modelling of multispecies contact networks, the risk of infection exposure at species-level is predicted. Coupled with foot-and-mouth disease virus (FMDV) antibody information, the role of each species in the dynamics of infectious diseases is explored. This study highlights how community networks can provide valuable insights into the functional epidemiological role of wildlife populations. Rather than establishing transmission routes, our aim is to propose a scalable and non-invasive surveillance framework that identifies priority species and areas for epidemiological monitoring in complex ecological systems. Significance StatementMonitoring disease circulation in wildlife is often hindered by the difficulty of collecting epidemiological data. We propose a novel non-invasive approach that combines species interaction networks derived from camera-trap data with non-invasive antibody detection to explore the exposure patterns of large herbivore communities to foot-and-mouth disease virus (FMDV). By linking the position of species in contact networks with their immunological status, we demonstrate the potential of using ecological centrality as a proxy for identifying key hosts in transmission or indicator species for pathogen circulation. Beyond FMDV, this framework can be adapted to other pathogens for which non-invasive immunological assays are currently being developed, making it broadly relevant for wildlife disease surveillance in remote or protected areas.

ecology↗

Influence of anthropogenic environments on the activity patterns and vigilance of Cape chacma baboons (Papio ursinus ursinus) in the Garden Route, South Africa

Anthropogenic activities shape animals time allocation and risk perception, yet its immediate behavioural impacts on primate species remain poorly quantified. In the present study, variation in activity budgets and vigilance were analysed in three Cape chacma baboon (Papio ursinus ursinus) troops inhabiting contrasting anthropogenic environments in South Africas Garden Route: Madiba (in a peri-urban campus), North (in an intermediate area), and Outeniqua (in a more rural area). From March to June 2024, a total 84 h of observations were recorded yielding 343 scan samples, and modelled behaviour as a function of troop and environmental covariates (weather, habitat openness, car and human presence). Feeding dominated overall time allocation (35.4%), with no whole-budget differences among troops, but behaviour-specific contrasts emerged. Outeniqua troop inhabiting the more rural area relied significantly less on human-derived foods than Madiba and showed less running than both Madiba and North. In addition, level-3 vigilance (active/intense scanning) was higher in the troops frequenting more anthropogenic environments (Madiba, North) than in Outeniqua, suggesting that vigilance is a particularly sensitive response to human exposure. Finally, habitat openness was negatively associated with affiliative interactions, and car presence was negatively associated with resting. These results provide partial support for hypothesised disturbance effects, with shifts in behavioural sub-categories without overall budget change, clarifying how anthropogenic disturbance can restructure primate time allocation and risk perception. Such immediate behavioural responses should offer actionable insight for evidence-based conservation and human-baboon conflict mitigation.

animal behavior and cognition↗

Hidden hematological, biochemical and immune costs of asymptomatic malaria infections in semi-wild chimpanzees

The health consequences of Plasmodium infections in wild great apes, particularly in asymptomatic animals, remain poorly understood. This study investigated the hematological and immune impacts of natural malaria infections in 27 semi-wild chimpanzees (Pan troglodytes troglodytes) from Gabon. Using MinION sequencing and species-specific PCR, results showed a 48.15% overall Plasmodium infection rate, with frequent multi-species co-infections involving Plasmodium gaboni, Plasmodium reichenowi, and Plasmodium vivax-like parasites. In addition, younger animals were significantly more infected and exhibited higher parasitemia levels, especially those with triple infections involving P. vivax-like. Profiling of 15 hematological markers and 8 cytokines/chemokines known to be associated with malarial infections in humans revealed significant alterations in infected chimpanzees, including elevated urea, reduced creatinine, and increased systemic concentrations of pro-inflammatory (TNF, IL-1{beta}, CCL3) and anti-inflammatory (IL-10) cytokines. Ex vivo PBMC stimulation yielded higher IL-10 in infected than non-infected individuals, indicating a regulatory-skewed cytokine response at the time of sampling. These results suggest that malaria in chimpanzees is associated with systemic immune modulation and accompanied by signs of physiological stress, including potential renal dysfunction. This study challenges the assumption that chronic Plasmodium infections are entirely benign in great apes and highlight the need to integrate immunological health indicators into conservation strategies. Broader immune profiling and longitudinal studies will be essential in the future to assess long-term health outcomes and resilience in these endangered populations.

evolutionary biology↗

Absence of reactive temporal response of baboons to the occurrence of predators

Predators exert strong selective pressure on prey species, shaping their behavioral adaptations. Prey species use proactive responses, such as site selection and the adjustment of daily activity patterns to anticipate and avoid predation exposure. In contrast, reactive responses, including fleeing, referential signaling and retaliation, occur after encountering a predator to mitigate the immediate predation risk. The presence of a predator in an area can also generate longer-term responses, such as reactive avoidance, defined here as the temporary avoidance of the area following the passage of a predator. Such a long-term reactive response remains understudied in primates. To investigate reactive avoidance, we analyzed an extensive camera trap data set of 3,042 detections (defined here as a motion-triggered event of three pictures per trigger during the day and one picture at night) of both chacma (Papio ursinus) and olive (Papio anubis) baboons, including 6,958 detections of their main predators, lions (Panthera leo), leopards (Panthera pardus) and spotted hyenas (Crocuta crocuta), in four savanna sites (Madikwe Game Reserve, Tswalu Kalahari Private Wildlife Reserve and the Associated Private Nature Reserves, South Africa; Serengeti National Park, Tanzania). We examined whether baboons display species-specific reactive avoidance towards predators up to 72 hours after the detection of a predator using randomization tests. We found no significant decrease in baboon presence (defined as the number of baboon detections) 0 to 24 hours, 24 to 48 hours and 48 to 72 hours after the detection of any predator species. These results suggest that baboons may not display reactive avoidance and rely on alternative predator-avoidance strategies, such as proactive avoidance or aggressive retaliation, to mitigate predation risk.

animal behavior and cognition↗

Genomic insights into Plasmodium vivax and Plasmodium simium host shifts in Latin America

Malaria in Latin America is largely caused by Plasmodium vivax, but its lesser-known sister species, Plasmodium simium, has recently emerged from monkeys to infect humans, thus raising new public health concerns. By analyzing 719 monkey samples and whole genome variations for 19 P. simium and 408 P. vivax isolates, we investigated the evolutionary history and population genetics of the two species. P. vivax, typically restricted to humans, was identified in three Colombian and one Brazilian monkeys, suggesting host niche expansion. Genetic analysis reveals recent genetic exchanges between both species and indicates that P. simium originated from a host jump approximately a century ago, possibly linked to P. vivax migration from Mexico to Brazil. Genome-wide scans revealed signals of positive selection in P. simium genes involved in interactions with primate hosts and mosquito vectors. These findings highlight P. simium evolutionary history and zoonotic malaria risks, and underscore the need to include monkeys in malaria prevention measures while ensuring human-wildlife coexistence.

evolutionary biology↗

Climate and predation drive variation of diel activity patterns in chacma baboons (Papio ursinus) across southern Africa

Understanding how animals adjust daily activity to environmental gradients reveals key drivers of behavioral plasticity. While diel activity is theorized to reflect trade-offs among thermoregulation, energy balance, and predation risk, few studies test these interactions at broad spatial scales within species. We investigated this in chacma baboons (Papio ursinus) using over a million camera-trap detections across 29 sites in six biomes (2016-2022) in South Africa and Zimbabwe. Activity declined by about 3% with latitude, consistent with lower resource predictability and increased with thermal stress, while sleep and wake times were similar across sites. Baboons avoided midday heat but increased dawn and night activity under predator pressure. These findings show how abiotic and biotic pressures shape diel schedules and highlight temporal flexibility as an adaptive strategy for generalist mammals in a changing world.

animal behavior and cognition↗

Genomic exploration of the complex journey of Plasmodium vivax in Latin America

Plasmodium vivax, the predominant malaria parasite in Latin America, has a rich and complex colonization history in the region, with debated hypotheses about its origin. Our study employed cutting-edge population genomic techniques, to collect whole genome sequencing data from 620 P. vivax isolates, including 107 newly sequenced samples, thus representing nearly all potential source populations worldwide. Analyses of the genetic structure, diversity, ancestry, and also, coalescent-based inferences and scenario testing using Approximate Bayesian Computation, have revealed a more complex evolutionary history than previously envisioned. Indeed, according to our analysis, the current American P. vivax populations predominantly stemmed from a now-extinct European lineage, with the potential contribution also from unsampled populations, most likely of West African origin, during post-colonial human migration waves in the late 19th-century. This study provides a fresh perspective on P. vivax intricate evolutionary journey and brings insights into the possible contribution of West African P. vivax populations to the colonization history of Latin America.

genomics↗

Population genomic evidence of adaptive response during the invasion history of Plasmodium falciparum in the Americas

Plasmodium falciparum, the most virulent agent of human malaria, spread from Africa to all continents following the out-of-Africa human migrations. During the transatlantic slave trade between the 16th and 19th centuries, it was introduced twice independently to the Americas where it adapted to new environmental conditions (new human populations and mosquito species). Here, we analyzed the genome-wide polymorphisms of 2,635 isolates across the current P. falciparum distribution range in Africa, Asia, Oceania, and the Americas to investigate its genetic structure, invasion history, and selective pressures associated with its adaptation to the American environment. We confirmed that American populations originated from Africa with at least two independent introductions that led to two genetically distinct clusters, one in the North (Haiti and Columbia) and one in the South (French Guiana and Brazil), and the admixed Peruvian group. Genome scans revealed recent and more ancient signals of positive selection in the American populations. Particularly, we detected positive selection signals in genes involved in interactions with host (human and mosquito) cells and in genes involved in resistance to malaria drugs in both clusters. We found that some genes were under selection in both clusters. Analyses suggested that for five genes, adaptive introgression between clusters or selection on standing variation was at the origin of this repeated evolution. This study provides new genetic evidence on P. falciparum colonization history and on its local adaptation in the Americas.

evolutionary biology↗

A unique Toxoplasma gondii haplotype under strong selection has accompanied domestic cats in their global expansion

Toxoplasma gondii is a cyst-forming apicomplexan parasite of virtually all warm-blooded species, with all true cats (Felidae) as definitive hosts. It is the etiologic agent of toxoplasmosis, a disease causing substantial public health burden worldwide. Its wide range of host species and its global occurrence probably complicate the study of its evolutionary history, and conflicting scenarios have been proposed to explain its current global distribution. In this study, we analyse a global set of 156 genomes (including 105 new genomes) and we provide the first direct estimate of T. gondii mutation rate and the first estimate of its generation time. We elucidate how the evolution of T. gondii populations is intimately linked to the major events that have punctuated the recent history of cats. We show that a unique haplotype --whose length represents only 0.16% of the whole T. gondii genome-- is common to all domestic T. gondii strains worldwide and has accompanied wild cats (Felis silvestris) during their emergence from the wild to domestic settlements, their dispersal in the Old World and their recent expansion to the Americas in the last six centuries. By combining environmental and functional data to selection inference tools, we show that selection of this domestic haplotype is most parsimoniously explained by its role in initiation of sexual reproduction of T. gondii in domestic cats.

genomics↗

Population genomic evidence of a Southeast Asian origin of Plasmodium vivax

Plasmodium vivax is the most prevalent and widespread human malaria parasite, with almost three billion people living at risk of infection. With the discovery of its closest genetic relatives in African great apes (Plasmodium vivax-like), the origin of P. vivax has been proposed to be located in the sub-Saharan African area. However, the limited number of genetic markers and samples investigated questioned the robustness of this result. Here, we examined the population genomic variation of 447 human P. vivax strains and 19 ape P. vivax-like strains originating from 24 different countries across the world. We identified 2,005,455 high quality single-nucleotide polymorphism loci allowing us to conduct an extensive characterization to date of P. vivax worldwide genetic variation. Phylogenetic relationships between human and ape Plasmodium revealed that P. vivax is a sister clade of P. vivax-like, not included within the radiation of P. vivax-like. By investigating a variety of aspects of P. vivax variation, we identified several striking geographical patterns in summary statistics as function of increasing geographic distance from Southeast Asia, suggesting that P. vivax may derived from serial founder effects from a single origin located in Asia.

evolutionary biology↗

Natural Wolbachia infections are common in the major malaria vectors in Central Africa

During the last decade, the endosymbiont bacterium Wolbachia has emerged as a biological tool for vector disease control. However, for long time, it was believed that Wolbachia was absent in natural populations of Anopheles. The recent discovery that species within the Anopheles gambiae complex hosts Wolbachia in natural conditions has opened new opportunities for malaria control research in Africa. Here, we investigated the prevalence and diversity of Wolbachia infection in 25 African Anopheles species in Gabon (Central Africa). Our results revealed the presence of Wolbachia in 16 of these species, including the major malaria vectors in this area. The infection prevalence varied greatly among species, confirming that sample size is a key factor to detect the infection. Moreover, our sequencing and phylogenetic analyses showed the important diversity of Wolbachia strains that infect Anopheles. Co-evolutionary analysis unveiled patterns of Wolbachia transmission within Anopheles species, suggesting that past independent acquisition events were followed by co-cladogenesis. The large diversity of Wolbachia strains that infect natural populations of Anopheles offers a promising opportunity to select suitable phenotypes for suppressing Plasmodium transmission and/or manipulating Anopheles reproduction, which in turn could be used to reduce the malaria burden in Africa.

ecology↗

Plasmodium vivax-like genome sequences shed new insights into Plasmodium vivax biology and evolution

Plasmodium vivax is responsible of the majority of malaria infections outside Africa. Its closer genetic relative, Plasmodium vivax-like, was discovered in African great apes and suggested to have given rise to P. vivax in humans. We generated two newly P. vivax-like reference genomes and 9 additional P. vivax-like genotypes, to unravel the evolutionary history of P. vivax. We showed a clear separation between the two clades, a higher genetic diversity of P. vivax-like parasites in comparison to the P. vivax ones, and the potential existence of two sub-clades of P. vivax-like. We dated the relative split between P. vivax and P. vivax-like as three times shorter than the split between P. ovale wallikeri and P. ovale curtesi and 1.5 times longer than the split between Plasmodium malariae. The sequencing of the P. vivax-like genomes is an undeniable advance in the understanding of P. vivax biology, evolution and emergence in human populations.

evolutionary biology↗

Genomes of an entire Plasmodium subgenus reveal paths to virulent human malaria

Plasmodium falciparum, the most virulent agent of human malaria, shares a recent common ancestor with the gorilla parasite P. praefalciparum. Little is known about the other gorilla and chimpanzee-infecting species in the same (Laverania) subgenus as P. falciparum but none of them are capable of establishing repeated infection and transmission in humans. To elucidate underlying mechanisms and the evolutionary history of this subgenus, we have generated multiple genomes from all known Laverania species. The completeness of our dataset allows us to conclude that interspecific gene transfers as well as convergent evolution were important in the evolution of these species. Striking copy number and structural variations were observed within gene families and one, stevor shows a host specific sequence pattern. The complete genome sequence of the closest ancestor of P. falciparum enables us to estimate confidently for the first time the timing of the beginning of speciation to be 40,000-60,000 years ago followed by a population bottleneck around 4,000-6,000 years ago. Our data allow us also to search in detail for the features of P. falciparum that made it the only member of the Laverania able to infect and spread in humans.

evolutionary biology↗