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Genetic sex determination (GSD) can evolve from environmental sex determination (ESD) via an intermediate state in which both coexist in the same population. Such mixed populations are found in the crustacean Daphnia magna, where non-male producers (NMP, genetically determined females) coexist with male producers (MP), in which male production is environmentally inducible and can also artificially be triggered by exposure to juvenile hormone. This makes Daphnia magna a rare model species for the study of evolutionary transitions from ESD to GSD. Although the chromosomal location of the NMP-determining mutation has been mapped, the actual genes and pathways involved in the evolution of GSD from ESD remain unknown. Here, we present a transcriptomic analysis of MP and NMP females under control (female producing) and under hormone exposure conditions. We found ∼100 differentially expressed genes between MP and NMP under control conditions. Genes in the NMP-determining chromosome region were especially likely to show such constitutive expression differences. Hormone exposure led to expression changes of an additional ∼100 (MP) to ∼600 (NMP) genes, with an almost systematic upregulation of those genes in NMP. These observations suggest that the NMP phenotype is not determined by a simple “loss-of-function” mutation. Rather, homeostasis of female offspring production under hormone exposure appears to be an active state, tightly regulated by complex mechanisms involving many genes. In a broader view, this illustrates that the evolution of GSD, while potentially initiated by a single mutation, likely leads to secondary integration involving many genes and pathways.

The breeding systems of many organisms are cryptic and difficult to investigate with observational data, yet they have profound effects on a species’ ecology, evolution, and genome organization. Genomic approaches offer a novel, indirect way to investigate breeding systems, specifically by studying the transmission of genetic information from parents to offspring. Here we exemplify this method through an assessment of self-fertilization vs. automictic parthenogenesis in Daphnia magna. Self-fertilization reduces heterozygosity by 50% compared to the parents, but under automixis, whereby two haploid products from a single meiosis fuse, the expected heterozygosity reduction depends on whether the two meiotic products are separated during meiosis I or II (i.e., central vs. terminal fusion). Reviewing the existing literature and incorporating recombination interference, we derive an interchromosomal and an intrachromosomal prediction of how to distinguish various forms of automixis from self-fertilization using offspring heterozygosity data. We then test these predictions using RAD-sequencing data on presumed automictic diapause offspring of so-called nonmale producing strains and compare them with “self-fertilized” offspring produced by within-clone mating. The results unequivocally show that these offspring were produced by automixis, mostly, but not exclusively, through terminal fusion. However, the results also show that this conclusion was only possible owing to genome-wide heterozygosity data, with phenotypic data as well as data from microsatellite markers yielding inconclusive or even misleading results. Our study thus demonstrates how to use the power of genomic approaches for elucidating breeding systems, and it provides the first demonstration of automictic parthenogenesis in Daphnia.

African trypanosomosis (AT), caused by protozoan parasites of the genus Trypanosoma , has plagued the African continent for centuries, affecting both humans and animals. Its principal vector, tsetse flies, can be found across sub-Saharan Africa. Vector control represents an efficient way to reduce the burden of AT. In Mozambique, control campaigns reshaped tsetse fly distribution to what it is today, with four species presently found: Glossina brevipalpis, G. pallidipes, G. morsitans and, G. austeni . Additionally, G. brevipalpis can be observed in two National parks, Gorongosa National Park in the Centre and Maputo National Park in the South, with an 840 km wide tsetse-free zone between them. In order to improve our knowledge on the genetic diversity in these populations, and their probable isolation, we undertook a population genetics study with 11 microsatellite loci. We found that these two zones behave as strongly isolated subpopulations, only exchanging a few individuals per year. To explain this finding, we suggest the existence of undocumented pocket populations between the two parks, or, in the absence of these, the accidental translocation of tsetse flies during human-driven animal transportation. We suggest that translocation through human-driven animal movement should be explored in future studies investigating Glossina populations. If eradication were to be attempted, re-invasion of the tsetse via motorized human transport should be considered in conjunction with the exploration of other sites within a 30 km radius to validate that no sources of re-invasion exist around these parks.

Trypanosoma brucei gambiense ( Tbg ) group 2 is a subgroup of trypanosomes able to infect humans and is found in West and Central Africa. Unlike other agents causing sleeping sickness, such as Tbg group 1 and Trypanosoma brucei rhodesiense , Tbg 2 lacks the typical molecular markers associated with resistance to human serum. Only 36 strains of Tbg 2 have been documented, and therefore, very limited research has been conducted despite their zoonotic nature. Some of these strains are only available in their procyclic form, which hinders human serum resistance assays and mechanistic studies. Furthermore, the understanding of Tbg 2’s potential to infect tsetse flies and mammalian hosts is limited. In this study, 165 Glossina palpalis gambiensis flies were experimentally infected with procyclic Tbg 2 parasites. It was found that 35 days post-infection, 43 flies out of the 80 still alive were found to be Tbg 2 PCR-positive in the saliva. These flies were able to infect 3 out of the 4 mice used for blood-feeding. Dissection revealed that only six flies in fact carried mature infections in their midguts and salivary glands. Importantly, a single fly with a mature infection was sufficient to infect a mammalian host. This Tbg 2 transmission success confirms that Tbg 2 strains can establish in tsetse flies and infect mammalian hosts. This study describes an effective in vivo protocol for transforming Tbg 2 from procyclic to bloodstream form, reproducing the complete Tbg 2 cycle from G. p. gambiensis to mice. These findings provide valuable insights into Tbg 2’s host infectivity, and will facilitate further research on mechanisms of human serum resistance. Trypanosoma brucei gambiense ( Tbg ) groupe 2 est un sous-groupe de trypanosomes capables d’infecter l’Homme, présent en Afrique de l’Ouest et en Afrique centrale. Contrairement aux autres agents responsables de la maladie du sommeil, tels que Tbg groupe 1 et Trypanosoma brucei rhodesiense , Tbg 2 ne présente pas les marqueurs moléculaires habituellement associés à la résistance au sérum humain. Seules trente-six souches de Tbg 2 ont été répertoriées, limitant considérablement les recherches sur ce sous-groupe malgré sa nature zoonotique. Certaines de ces souches ne sont disponibles que sous leur forme procyclique, ce qui freine la réalisation des tests de résistance au sérum humain et les études mécanistiques. De plus, la compréhension du potentiel de Tbg 2 à infecter les glossines et les hôtes mammifères est limitée. Dans cette étude, 165 glossines Glossina palpalis gambiensis ont été infectées expérimentalement par des parasites Tbg 2 sous leur forme procyclique. Trente-cinq jours après l’infection, 43 des 80 glossines encore en vie se sont révélées positives à Tbg 2 en PCR sur leur salive. Ces glossines ont réussi à infecter trois des quatre souris utilisées pour leur repas de sang. La dissection des glossines a révélé que seules six d’entre elles étaient réellement porteuses d’infections matures dans leur intestin et leurs glandes salivaires. Il est important de noter qu’une seule glossine porteuse d’une infection mature a suffi pour infecter un hôte mammifère. Ce succès de transmission de Tbg 2 confirme que les souches de Tbg 2 peuvent s’établir dans les glossines et infecter des hôtes mammifères. Cette étude décrit un protocole in vivo pour transformer la forme procyclique de Tbg 2 en forme sanguicole, en reproduisant le cycle complet de Tbg 2 de G. p. gambiensis à la souris. Ces résultats fournissent des informations précieuses sur le potentiel infectieux de Tbg 2 et faciliteront la recherche sur les mécanismes de résistance au sérum humain des souches.

In the population at risk of gambiense human African trypanosomiasis (gHAT), the prevalence of extravascular parasite carriage remains unclear. Here, we conducted an observational clinical study in the hypo-endemic gHAT foci of Sinfra and Bonon in Côte d’Ivoire from 2019 to 2022. A total of 74 individuals were enrolled, including 45 suspects previously found positive at least once in a serological test for gHAT and followed by the national elimination programme of Côte d’Ivoire, as well as 29 seronegative controls. No significant differences between groups were observed for any epidemiological parameters and any clinical parameters at enrolment. Whereas trypanosome DNA was detected in the blood of 0/29 controls and 2/45 suspects, the presence of extravascular dermal trypanosomes was confirmed by immuno-histochemistry (fixed trypanosome cells) and/or PCR (trypanosome DNA) in about 1/3 of the suspects (14/45, 31%). However, no gambiense -specific test was found positive in the present study. Hence, the skin could represent an anatomical reservoir for African trypanosomes sustaining a low level of transmission in hypo-endemic foci.

Vector control (VC) is one of the strategies employed to manage African trypanosomoses. This study aimed at assessing the effectiveness of a VC campaign against Glossina palpalis palpalis using tiny targets (TTs) impregnated with insecticide in an isolated, protected forest in Abidjan, Côte d’Ivoire, while considering ecological, genetic, and operational factors. Between January 2020 and September 2022, 2,712 TTs were deployed at 684 sites, covering a total area of 1.7 km 2 . VC monitoring was conducted using Vavoua traps during 12 evaluation surveys, between June 2020 and March 2023. Five months after the initial TT deployment, tsetse fly density had decreased by 98.53%. Although tsetse density remained low due to TT redeployment and reinforcement, there was a significant increase a few months after the last redeployment. VC appeared to have minimal impact on the genetic structuring of G. p. palpalis . This suggested recruitment of local surviving tsetse flies all along the VC campaign due to a low probability of tsetse coming into contact with TTs, or to the evolution of behavioral or physiological resistance to control efforts. The genetic study revealed that one of the microsatellite markers used, the GPCAG locus, exhibited a selection signature possibly in response to VC. This could partly explain the challenges encountered in eliminating a seemingly isolated tsetse population thriving in a particularly favorable habitat. La lutte antivectorielle (LAV) fait partie des stratégies de contrôle des trypanosomoses africaines. La présente étude visait à évaluer l’efficacité d’une campagne de LAV contre Glossina palpalis palpalis avec des écrans de type « tiny targets » (TT) imprégnés d’insecticide dans une forêt isolée et protégée à Abidjan, Côte d’Ivoire, en tenant compte des facteurs écologiques, génétiques et opérationnels. Entre janvier 2020 et septembre 2022, 2 712 TT ont été déployés sur 684 sites totalisant une superficie de 1,7 km 2 . Le suivi de la LAV a été effectué en utilisant des pièges Vavoua lors de 12 enquêtes d’évaluation menées entre juin 2020 et mars 2023. Cinq mois après le premier déploiement des TT, la densité de glossines avait chuté de 98,53 %. Elle est restée faible grâce aux redéploiements et renforcements en TT, mais a ré-augmenté significativement quelques mois après le dernier redéploiement. Elle semble avoir peu impacté la structuration génétique de G. p. palpalis . Cela suggère un recrutement local de mouches survivantes tout au long de la campagne de LAV, dû à une faible probabilité pour les glossines de rencontrer un TT ou à une possible stratégie d’évitement ou de résistance aux efforts de lutte. L’étude génétique a d’ailleurs révélé que l’un des marqueurs microsatellite utilisé, le locus GPCAG, présentait une signature de sélection possiblement en réponse à la LAV. Ceci permettrait en partie d’expliquer les difficultés rencontrées pour éliminer une population de glossines apparemment isolée mais occupant un biotope particulièrement favorable.

African trypanosomoses, whose pathogens are transmitted by tsetse flies, are a threat to animal and human health. Tsetse flies observed at the military base of the French Forces in Côte d’Ivoire (FFCI base) were probably involved in the infection and death of military working dogs. Entomological and parasitological surveys were carried out during the rainy and dry seasons using “Vavoua” traps to identify tsetse fly species, their distribution, favorable biotopes and food sources, as well as the trypanosomes they harbor. A total of 1185 Glossina palpalis palpalis tsetse flies were caught, corresponding to a high average apparent density of 2.26 tsetse/trap/day. The results showed a heterogeneous distribution of tsetse at the FFCI base, linked to more or less favorable biotopes. No significant variation in tsetse densities was observed according to the season. The overall trypanosomes infection rate according to microscopic observation was 13.5%. Polymerase chain reaction (PCR) analyses confirmed the presence of Trypanosoma vivax and T. congolense forest type, responsible for African animal trypanosomosis. Our findings suggest that there is a risk of introduction and transmission of T. brucei gambiense , responsible for human African trypanosomiasis, on the study site. This risk of transmission of African trypanosomes concerns not only the FFCI base, but also inhabited peripheral areas. Our study confirmed the need for vector control adapted to the eco-epidemiological context of the FFCI base. Les trypanosomoses africaines, dont les agents pathogènes sont transmis par les mouches tsé-tsé, constituent une contrainte pour la santé animale et humaine. Des mouches tsé-tsé observées dans la base militaire des Forces françaises en Côte d’Ivoire (base FFCI) ont probablement été impliquées dans l’infection et la mort de chiens militaires. Des enquêtes entomologiques et parasitologiques ont été menées pendant la saison pluvieuse et la saison sèche à l’aide de pièges “Vavoua” afin d’identifier les espèces de mouches tsé-tsé, leur distribution, les biotopes favorables et leur source de nourriture ainsi que les trypanosomes qu’elles hébergent. Au total 1185 mouches tsé-tsé de l’espèce Glossina palpalis palpalis ont été capturées, ce qui correspond à une densité apparente moyenne élevée de 2,26 tsé-tsé/piège/jour. Les résultats ont montré une distribution hétérogène des tsé-tsé dans la base FFCI en lien avec des biotopes plus ou moins favorables. Aucune variation significative des densités de tsé-tsé n’a été observée en fonction de la saison. Le taux d’infection global par les trypanosomes était de 13,5 % selon l’observation microscopique. Les analyses PCR ont confirmé la présence de Trypanosoma vivax et T. congolense type forêt, responsable de la trypanosomose animale africaine. Nos résultats suggèrent qu’il existe un risque potentiel d’introduction et de transmission de T. brucei gambiense responsable de la trypanosomiase humaine africaine dans la zone d’étude. Ce risque de transmission des trypanosomes africains concerne non seulement l’intérieur de la base FFCI, mais aussi les espaces périphériques habités. Notre étude a confirmé la nécessité de mener une lutte antivectorielle adaptée au contexte éco-épidémiologique de la base FFCI.

Daphnia reproduce by cyclic-parthenogenesis, where phases of asexual reproduction are intermitted by sexual production of diapause stages. This life cycle, together with environmental sex determination, allow the comparison of gene expression between genetically identical males and females. We investigated gene expression differences between males and females in four genotypes of Daphnia magna and compared the results with published data on sex-biased gene expression in two other Daphnia species, each representing one of the major phylogenetic clades within the genus. We found that 42% of all annotated genes showed sex-biased expression in D. magna. This proportion is similar both to estimates from other Daphnia species as well as from species with genetic sex determination, suggesting that sex-biased expression is not reduced under environmental sex determination. Among 7453 single copy, one-to-one orthologs in the three Daphnia species, 707 consistently showed sex-biased expression and 675 were biased in the same direction in all three species. Hence these genes represent a core-set of genes with consistent sex-differential expression in the genus. A functional analysis identified that several of them are involved in known sex determination pathways. Moreover, 75% were overexpressed in females rather than males, a pattern that appears to be a general feature of sex-biased gene expression in Daphnia.

Tsetse flies (genus Glossina) transmit deadly trypanosomes to human populations and domestic animals in sub-Saharan Africa. Some foci of Human African Trypanosomiasis due to Trypanosoma brucei gambiense (g-HAT) persist in southern Chad, where a program of tsetse control was implemented against the local vector Glossina fuscipes fuscipes in 2018 in Maro. We analyzed the population genetics of G. f. fuscipes from the Maro focus before control (T0), one year (T1), and 18 months (T2) after the beginning of control efforts. Most flies captured displayed a local genetic profile (local survivors), but a few flies displayed outlier genotypes. Moreover, disturbance of isolation by distance signature (increase of genetic distance with geographic distance) and effective population size estimates, absence of any genetic signature of a bottleneck, and an increase of genetic diversity between T0 and T2 strongly suggest gene flows from various origins, and a limited impact of the vector control efforts on this tsetse population. Continuous control and surveillance of g-HAT transmission is thus recommended in Maro. Particular attention will need to be paid to the border with the Central African Republic, a country where the entomological and epidemiological status of g-HAT is unknown.

The existence of an animal reservoir of Trypanosoma brucei gambiense (T. b. gambiense), the agent of human African trypanosomiasis (HAT), may compromise the interruption of transmission targeted by World Health Organization. The aim of this study was to investigate the presence of trypanosomes in pigs and people in the Vavoua HAT historical focus where cases were still diagnosed in the early 2010's. For the human survey, we used the CATT, mini-anion exchange centrifugation technique and immune trypanolysis tests. For the animal survey, the buffy coat technique was also used as well as the PCR using Trypanosoma species specific, including the T. b. gambiense TgsGP detection using single round and nested PCRs, performed from animal blood samples and from strains isolated from subjects positive for parasitological investigations. No HAT cases were detected among 345 people tested. A total of 167 pigs were investigated. Free-ranging pigs appeared significantly more infected than pigs in pen. Over 70% of free-ranging pigs were positive for CATT and parasitological investigations and 27-43% were positive to trypanolysis depending on the antigen used. T. brucei was the most prevalent species (57%) followed by T. congolense (24%). Blood sample extracted DNA of T. brucei positive subjects were negative to single round TgsGP PCR. However, 1/22 and 6/22 isolated strains were positive with single round and nested TgsGP PCRs, respectively. Free-ranging pigs were identified as a multi-reservoir of T. brucei and/or T. congolense with mixed infections of different strains. This trypanosome diversity hinders the easy and direct detection of T. b. gambiense. We highlight the lack of tools to prove or exclude with certainty the presence of T. b. gambiense. This study once more highlights the need of technical improvements to explore the role of animals in the epidemiology of HAT.