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de Thoisy, B.

Publications and source records attributed to de Thoisy, B..

8 recordsLinked to original sources

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↗

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↗

A DNA barcode library for Culex mosquitoes (Diptera: Culicidae) of South America with the description of two cryptic species of subgenus Melanoconion

The genus Culex is one of the most diverse in the world and includes numerous known vector species of parasites and viruses to humans. Morphological identification of Culex species is notoriously difficult and rely mostly on the examination of properly dissected male genitalia which largely prevents female and immature identification during entomological, ecological or arboviral surveys. The aims of this study were (i) to establish a DNA barcode library for Culex mosquitoes of French Guiana based on the mitochondrial gene cytochrome c oxidase I (COI) marker, (ii) to compare three approaches of molecular delimitation of species to morphological identification, and (iii) to test the effectiveness of the COI marker at a broader geographical scale across South America. Mosquitoes used in this study were sampled in French Guiana between 2013 and 2023. We provide 246 COI sequences for 90 morphologically identified species of Culex, including five new country records and two newly described species. Overall, congruence between morphological identification and molecular delimitations using the COI barcode were high. The Barcode of Life Data clustering approach into Barcode Index Numbers gives the best result in terms of species delimitation, followed by the muti-rate Poisson Tree Processes and the Assemble Species by Automatic Partitioning methods. Inconsistencies between morphological identification and molecular delimitation can be explained by introgression, incomplete lineage sorting, imperfect taxonomy or the effect of the geographical scale of sampling. This increases by almost two-fold the number of mosquito species for which a DNA barcode is available in French Guiana, including 75% of the species of Culex currently known in the territory. Finally, this study confirms the usefulness of the COI barcode in identifying Culex mosquitoes of South America, but also points the limits of this marker for some groups of species within the subgenera Culex and Melanoconion.

molecular biology↗

Metagenomics uncovers dietary adaptations for chitin digestion in the gut microbiota of convergent myrmecophagous mammals

In mammals, myrmecophagy (ant and termite consumption) represents a striking example of dietary convergence. This trait evolved independently at least five times in placentals with myrmecophagous species comprising aardvarks, anteaters, some armadillos, pangolins, and aardwolves. The gut microbiome plays an important role in dietary adaptation, and previous analyses of 16S rRNA metabarcoding data have revealed convergence in the composition of the gut microbiota among some myrmecophagous species. However, the functions performed by these gut bacterial symbionts and their potential role in the digestion of prey chitinous exoskeletons remain open questions. Using long- and short-read sequencing of fecal samples, we generated 29 gut metagenomes from nine myrmecophagous and closely related insectivorous species sampled in French Guiana, South Africa, and the USA. From these, we reconstructed 314 high-quality bacterial genome bins of which 132 carried chitinase genes, highlighting their potential role in insect prey digestion. These chitinolytic bacteria belonged mainly to the family Lachnospiraceae, and some were likely convergently recruited in the different myrmecophagous species as they were detected in several host orders (i.e., Enterococcus faecalis, Blautia sp), suggesting that they could be directly involved in the adaptation to myrmecophagy. Others were found to be more host-specific, possibly reflecting phylogenetic constraints and environmental influences. Overall, our results highlight the potential role of the gut microbiome in chitin digestion in myrmecophagous mammals and provide the basis for future comparative studies performed at the mammalian scale to further unravel the mechanisms underlying the convergent adaptation to myrmecophagy. ImportanceMyrmecophagous mammals are specialized in the consumption of ants and/or termites. They do not share a direct common ancestor and evolved convergently in five distinct placental orders raising questions about the underlying adaptive mechanisms involved and the relative contribution of natural selection and phylogenetic constraints. Understanding how these species digest their prey can help answer these questions. More specifically, the role of their gut microbial symbionts in the digestion of the insect chitinous exoskeleton has not been investigated in all myrmecophagous orders. We generated 29 new gut metagenomes from nine myrmecophagous species to reconstruct more than 300 bacterial genomes in which we identified chitin-degrading enzymes. Studying the distribution of these chitinolytic bacteria among hosts revealed both shared and specific bacteria between ant-eating species. Overall, our results highlight the potential role of gut symbionts in the convergent dietary adaptation of myrmecophagous mammals and the evolutionary mechanisms shaping their gut microbiota.

evolutionary biology↗

Comparative transcriptomics reveals divergent paths of chitinase evolution underlying dietary convergence in ant-eating mammals

Ant-eating mammals represent a textbook example of convergent evolution. Among them, anteaters and pangolins exhibit the most extreme convergent phenotypes with complete tooth loss, elongated skulls, protruding tongues, hypertrophied salivary glands producing large amounts of saliva, and powerful claws for ripping open ant and termite nests. However, comparative genomic analyses have shown that anteaters and pangolins differ in their chitinase acidic gene (CHIA) repertoires, which potentially degrade the chitinous exoskeletons of ingested ants and termites. While the southern tamandua (Tamandua tetradactyla) harbors four functional CHIA paralogs (CHIA1-4), Asian pangolins (Manis spp.) have only one functional paralog (CHIA5). Here, we performed a comparative transcriptomic analysis of salivary glands in 33 placental species, including 16 novel transcriptomes from ant-eating species and close relatives. Our results suggest that salivary glands play an important role in adaptation to an insect-based diet, as expression of different CHIA paralogs is observed in insectivorous species. Furthermore, convergently-evolved pangolins and anteaters express different chitinases in their digestive tracts. In the Malayan pangolin, CHIA5 is overexpressed in all major digestive organs, whereas in the southern tamandua, all four functional paralogs are expressed, at very high levels for CHIA1 and CHIA2 in the pancreas, and for CHIA3 and CHIA4 in the salivary glands, stomach, liver, and pancreas. Overall, our results demonstrate that divergent molecular mechanisms within the chitinase acidic gene family underlie convergent adaptation to the ant-eating diet in pangolins and anteaters. This study highlights the role of historical contingency and molecular tinkering of the chitin-digestive enzyme toolkit in this classic example of convergent evolution.

evolutionary biology↗

Evidence of backcross inviability and mitochondrial DNA paternal leakage in sea turtle hybrids

Hybridization is known to be part of many species evolutionary history. Sea turtles have a fascinating hybridization system in which species separated by as much as 43 million years are still capable of hybridizing. Indeed, the largest nesting populations in Brazil of loggerheads (Caretta caretta) and hawksbills (Eretmochelys imbricata) have a high incidence of hybrids between these two species. A third species, olive ridleys (Lepidochelys olivacea), is also known to hybridize although at a smaller scale. Here we used restriction site-associated DNA sequencing (RAD-Seq) markers, mitogenomes, and satellite-telemetry to investigate the patterns of hybridization and introgression in the Brazilian sea turtle population and their relationship with the migratory behaviors between feeding and nesting aggregations. We also explicitly test if the mixing of two divergent genomes in sea turtle hybrids causes mitochondrial paternal leakage. We developed a new species-specific PCR-assay capable of detecting mitochondrial DNA (mtDNA) inheritance from both parental species and performed ultra-deep sequencing to estimate the abundance of each mtDNA type. Our results show that all adult hybrids are first generation (F1) and most display a loggerhead migratory behavior. We detected paternal leakage in F1 hybrids and different proportions of mitochondria from maternal and paternal species. Although previous studies showed no significant fitness decrease in hatchlings, our results support genetically-related hybrid breakdown possibly caused by cytonuclear incompatibility. Further research on hybrids from other populations besides Brazil and between different species will show if backcross inviability and mitochondrial paternal leakage is observed across sea turtle species.

evolutionary biology↗

Optimization of ddRAD-like data leads to high quality sets of reduced representation single copy orthologs (R2SCOs) in a sea turtle multi-species analysis.

Reduced representation libraries (RRS) allow large scale studies on non-model species to be performed without the need for a reference genome, by building a pseudo-reference locus catalog directly from the data. However, using closely-related high-quality genomes can help maximize nucleotide variation identified from RRS libraries. While chromosome-level genomes remain unavailable for most species, researchers can still invest in building high-quality and project-specific de novo locus catalogs. Among methods that use restriction enzymes (RADSeq), those including fragment size selection to help obtain the desired number of loci - such as double-digest RAD (ddRAD) - are highly flexible but can present important technical issues. Inconsistent size selection reproducibility across libraries and variable coverage across fragment lengths can affect genotyping confidence, number of identified single nucleotide polymorphisms (SNPs), and quality and completeness of the de novo reference catalog. We have developed a strategy to optimize locus catalog building from ddRAD-like data by sequencing overlapping reads that recreate original fragments and add information about coverage per fragment size. Further in silico size selection and digestion steps limit the filtered dataset to well-covered sets of loci and identity thresholds are estimated based on sequence pairwise comparisons. We have developed a full workflow that identifies a set of reduced-representation single-copy orthologs (R2SCOs) for any given species and that includes estimating and evaluating allelic variation in comparison with SNP calling results. We also show how to use our concept in an established RADSeq pipeline - Stacks - and confirm that our approach increases average coverage and number of SNPs called per locus in the final catalog. We have demonstrated our full workflow using newly generated data from five sea turtle species and provided further proof-of-principle using published hybrid sea turtle and primate datasets. Finally, we showed that a project-specific set of R2SCOs perform better than a draft genome as a reference.

evolutionary biology↗

Manatee genomics supports a special conservation area in the Guianas coastline under the influence of the Amazon River plume

The West Indian manatee (Trichechus manatus) occurs along the Atlantic coastline and adjacent freshwater systems of South, Central and North America, from Alagoas (Brazil) to Florida (USA) and Greater Antilles. The Amazonian manatee (Trichechus inunguis) is the only Sirenian adapted exclusively to freshwater and endemic to the Amazon River basin. Previous studies have reported hybrids between T. inunguis and T. manatus close to the mouth of the Amazon River, composing a likely extensive hybrid zone along the Guianas coast of South America under the influence of the Amazon River plume. We have used ddRAD SNP data, and sequences of nuclear and mtDNA loci to characterize the genomic composition of manatees along the French Guiana coastline. We found this population to be formed by introgressed or later generation interspecific hybrids, and also describe the first T. inunguis found outside the Amazon River basin. Our results indicate that T. inunguis can survive in the Amazon River plume and have colonized independent water streams of the Guianas coastline where they likely hybridize with T. manatus. This hypothesis offers a plausible explanation for the known extension of the hybrid zone between the two species along the Guianas coastline. It also reinforces the importance of the Amazon plume, which flows westwards to the Guianas coastline and favors the dispersion of the freshwater species. This habitat functions as a large estuary-like system that provides an ecological continuum from Amazon River mouth to the disconnected waterflows of the Guianas, which deserves a status of special conservation area.

genomics↗