Chagas disease, caused by the kinetoplastid Trypanosoma cruzi (Chagas, 1909), and transmitted by triatomine bugs, poses a significant public health challenge. Variability in the susceptibility of different triatomine species to T. cruzi infection can profoundly influence disease transmission dynamics and control measures. In this study, we assessed the susceptibility to T. cruzi infection in the first and third nymphal stages across eight triatomine species to T. cruzi infection using experimental inoculation with the NINOA strain and optical microscopy. The evaluated species were Dipetalogaster maximus (Uhler), Triatoma bassolsae (Alejandre-Aguilar, Nogueda-Torres, Cortéz-Jiménez, Jurberg, Galvão, Carcaballo), T. infestans (Klug), T. lecticularia (Stål), T. mexicana (Herrich-Schaeffer), T. pallidipennis (Stål), T. phyllosoma (Burmeister) and T. picturata (Usinger). The results indicated that T. bassolsae exhibited the highest susceptibility to infection, followed by T. pallidipennis and D. maximus. Our analysis also revealed that T. cruzi (NINOA) infection was significantly associated with triatomine species rather than nymphal stage (p < 0.0001), with substantial variability observed in susceptibility among species (p < 0.001). We ranked triatomine species susceptibility to T. cruzi infection as follows: T. bassolsae > D. maximus = T. pallidipennis = T. picturata = T. mexicana > T. phyllosoma = T. lecticularia = T. infestans. These findings enhance our understanding of T. cruzi transmission dynamics and offer valuable insights for the development of effective control strategies against this neglected tropical disease.
- Keywords
- Chagas disease, nymphal stages, triatomine infections, vector competence,
- MeSH
- Chagas Disease transmission parasitology MeSH
- Species Specificity MeSH
- Insect Vectors * parasitology MeSH
- Nymph parasitology growth & development MeSH
- Triatoma * parasitology MeSH
- Triatominae * parasitology MeSH
- Trypanosoma cruzi * physiology MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Mexico MeSH
The blood-sucking hemipteran Rhodnius prolixus is one of the main vectors of Chagas disease, a neglected tropical disease that affects several million people worldwide. Consuming a blood meal and mating are events with a high epidemiological impact since after each meal, mated females can lay fertile eggs that result in hundreds of offspring. Thus, a better knowledge of the control of R. prolixus reproductive capacity may provide targets for developing novel strategies to control vector populations, thereby reducing vector-host contacts and disease transmission. Here, we have used a combination of gene transcript expression analysis, biochemical assays, hormone measurements and studies of locomotory activity to investigate how mating influences egg development and egg laying rates in R. prolixus females. The results demonstrate that a blood meal increases egg production capacity and leads to earlier egg laying in mated females compared to virgins. Virgin females, however, have increased survival rate over mated females. Circulating juvenile hormone (JH) and ecdysteroid titers are increased in mated females, a process mainly driven through an upregulation of the transcripts for their biosynthetic enzymes in the corpus allatum and ovaries, respectively. Mated females display weaker locomotory activity compared to virgin females, mainly during the photophase. In essence, this study shows how reproductive output and behaviour are profoundly influenced by mating, highlighting molecular, biochemical, endocrine and behavioral features differentially expressed in mated and virgin R. prolixus females.
- MeSH
- Chagas Disease * MeSH
- Oviposition physiology MeSH
- Humans MeSH
- Parasites * MeSH
- Rhodnius * physiology MeSH
- Reproduction MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Research Support, N.I.H., Extramural MeSH
The importance of gut microbiomes has become generally recognized in vector biology. This study addresses microbiome signatures in North American Triatoma species of public health significance (vectors of Trypanosoma cruzi) linked to their blood-feeding strategy and the natural habitat. To place the Triatoma-associated microbiomes within a complex evolutionary and ecological context, we sampled sympatric Triatoma populations, related predatory reduviids, unrelated ticks, and environmental material from vertebrate nests where these arthropods reside. Along with five Triatoma species, we have characterized microbiomes of five reduviids (Stenolemoides arizonensis, Ploiaria hirticornis, Zelus longipes, and two Reduvius species), a single soft tick species, Ornithodoros turicata, and environmental microbiomes from selected sites in Arizona, Texas, Florida, and Georgia. The microbiomes of predatory reduviids lack a shared core microbiota. As in triatomines, microbiome dissimilarities among species correlate with dominance of a single bacterial taxon. These include Rickettsia, Lactobacillus, "Candidatus Midichloria," and Zymobacter, which are often accompanied by known symbiotic genera, i.e., Wolbachia, "Candidatus Lariskella," Asaia, Gilliamella, and Burkholderia. We have further identified a compositional convergence of the analyzed microbiomes in regard to the host phylogenetic distance in both blood-feeding and predatory reduviids. While the microbiomes of the two reduviid species from the Emesinae family reflect their close relationship, the microbiomes of all Triatoma species repeatedly form a distinct monophyletic cluster highlighting their phylosymbiosis. Furthermore, based on environmental microbiome profiles and blood meal analysis, we propose three epidemiologically relevant and mutually interrelated bacterial sources for Triatoma microbiomes, i.e., host abiotic environment, host skin microbiome, and pathogens circulating in host blood. IMPORTANCE This study places microbiomes of blood-feeding North American Triatoma vectors (Reduviidae) into a broader evolutionary and ecological context provided by related predatory assassin bugs (Reduviidae), another unrelated vector species (soft tick Ornithodoros turicata), and the environment these arthropods coinhabit. For both vectors, microbiome analyses suggest three interrelated sources of bacteria, i.e., the microbiome of vertebrate nests as their natural habitat, the vertebrate skin microbiome, and the pathobiome circulating in vertebrate blood. Despite an apparent influx of environment-associated bacteria into the arthropod microbiomes, Triatoma microbiomes retain their specificity, forming a distinct cluster that significantly differs from both predatory relatives and ecologically comparable ticks. Similarly, within the related predatory Reduviidae, we found the host phylogenetic distance to underlie microbiome similarities.
- Keywords
- Ornithodoros, Reduviidae, Triatoma, environment, microbiome,
- MeSH
- Bacteria genetics MeSH
- Phylogeny MeSH
- Microbiota * MeSH
- Triatoma * MeSH
- Trypanosoma cruzi * MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
BACKGROUND: Triatominae are vectors of the protozoan Trypanosoma cruzi, the causative agent of Chagas disease. This study aims to report an infestation on Triatominae colonies by a beetle, previously identified as a pest. METHODS: The management of these colonies should be improved to maximize their usefulness, and factors that may cause harm to them should be avoided as much as possible. RESULTS: This is the first report on a coleopteran infestation on living Triatominae colonies worldwide. CONCLUSIONS: The present record provides an important warning to researchers who maintain insectaries in general, especially those who rear triatomines, to carry protective measures against such invasions.
- MeSH
- Coleoptera * MeSH
- Chagas Disease * MeSH
- Insect Vectors MeSH
- Reduviidae * MeSH
- Triatominae * MeSH
- Trypanosoma cruzi * MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
The rigorous balance of endocrine signals that control insect reproductive physiology is crucial for the success of egg production. Rhodnius prolixus, a blood-feeding insect and main vector of Chagas disease, has been used over the last century as a model to unravel aspects of insect metabolism and physiology. Our recent work has shown that nutrition, insulin signaling, and two main types of insect lipophilic hormones, juvenile hormone (JH) and ecdysteroids, are essential for successful reproduction in R. prolixus; however, the interplay behind these endocrine signals has not been established. We used a combination of hormone treatments, gene expression analyses, hormone measurements, and ex vivo experiments using the corpus allatum or the ovary, to investigate how the interaction of these endocrine signals might define the hormone environment for egg production. The results show that after a blood meal, circulating JH levels increase, a process mainly driven through insulin and allatoregulatory neuropeptides. In turn, JH feeds back to provide some control over its own biosynthesis by regulating the expression of critical biosynthetic enzymes in the corpus allatum. Interestingly, insulin also stimulates the synthesis and release of ecdysteroids from the ovary. This study highlights the complex network of endocrine signals that, together, coordinate a successful reproductive cycle.
- Keywords
- corpus allatum, endocrine signaling, hormone titers, insect, ovary,
- MeSH
- Ecdysteroids metabolism MeSH
- Insect Hormones * metabolism MeSH
- Insulin, Regular, Human MeSH
- Insulin metabolism MeSH
- Juvenile Hormones metabolism MeSH
- Rhodnius * metabolism MeSH
- Animals MeSH
- Check Tag
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Ecdysteroids MeSH
- Insect Hormones * MeSH
- Insulin, Regular, Human MeSH
- Insulin MeSH
- Juvenile Hormones MeSH
Juvenile hormone (JH) signalling, via its receptor Methoprene-tolerant (Met), controls metamorphosis and reproduction in insects. Met belongs to a superfamily of transcription factors containing the basic Helix Loop Helix (bHLH) and Per Arnt Sim (PAS) domains. Since its discovery in 1986, Met has been characterized in several insect species. However, in spite of the importance as vectors of Chagas disease, our knowledge on the role of Met in JH signalling in Triatominae is limited. In this study, we cloned and sequenced the Dipetalogaster maxima Met transcript (DmaxMet). Molecular modelling was used to build the structure of Met and identify the JH binding site. To further understand the role of the JH receptor during oogenesis, transcript levels were evaluated in two main target organs of JH, fat body and ovary. Functional studies using Met RNAi revealed significant decreases of transcripts for vitellogenin (Vg) and lipophorin (Lp), as well as their receptors. Lp and Vg protein amounts in fat body, as well as Vg in hemolymph were also decreased, and ovarian development was impaired. Overall, these studies provide additional molecular insights on the roles of JH signalling in oogenesis in Triatominae; and therefore are relevant for the epidemiology of Chagas´ disease.
- MeSH
- Juvenile Hormones metabolism MeSH
- Methoprene * metabolism MeSH
- Oogenesis genetics MeSH
- Triatominae * MeSH
- Vitellogenins MeSH
- Animals MeSH
- Check Tag
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Research Support, N.I.H., Extramural MeSH
- Names of Substances
- Juvenile Hormones MeSH
- Methoprene * MeSH
- Vitellogenins MeSH
The Canary Archipelago is home to two species of obligately cavernicolous assassin bugs of the genus Collartida Villiers, 1949 (Hemiptera: Heteroptera: Reduviidae: Emesinae: Collartidini). These species are highly adapted for cave life, being blind and wingless. In the present study, we describe a new species of the genus, C. phantasma sp. nov. from the Federica mine in Gran Canaria. C. phantasma sp. nov. differs from the other two Collartida species found in the Canary Archipelago in that the male is fully winged, the female is wingless, and both sexes have well-developed eyes. We provide information regarding the new species habitat, its taxonomic affinities, and its ability to fly.
- MeSH
- Hemiptera * MeSH
- Heteroptera * MeSH
- Caves MeSH
- Reduviidae * MeSH
- Animal Distribution MeSH
- Triatoma * MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Spain MeSH
Triatomine bugs are the blood feeding insect vectors transmitting Chagas disease to humans, a neglected tropical disease that affects over 8 million people, mainly in Latin America. The behavioral responses to host cues and bug signals in Rhodnius prolixus are state dependent, i.e., they vary as a function of post-ecdysis age. At the molecular level, these changes in behavior are probably due to a modulation of peripheral and central processes. In the present study, we report a significant modulation of the expression of a large set of sensory-related genes. Results were generated by means of antennal transcriptomes of 5th instar larvae along the first week (days 0, 2, 4, 6 and 8) after ecdysis sequenced using the Illumina HiSeq platform. Significant age-induced changes in transcript abundance were established for more than 6120 genes (54,7% of 11,186 genes expressed) in the antenna of R. prolixus. This was especially true between the first two days after ecdysis when more than 2500 genes had their expression significantly altered. In contrast, expression profiles were almost identical between day 6 and 8, with only a few genes showing significant modulation of their expression. A total of 86 sensory receptors, odorant carriers and odorant degrading enzymes were significantly modulated across age points and clustered into three distinct expression profiles. The set of sensory genes whose expression increased with age (profile 3) may include candidates underlying the increased responsiveness to host cues shown by R. prolixus during the first days after molting. For the first time, we describe the maturation process undergone at the molecular level by the peripheral sensory system of a hemimetabolous insect.
- Keywords
- Age, Antennae, Rhodnius prolixus, Sensory genes, Transcriptome,
- MeSH
- Chagas Disease transmission MeSH
- Smell genetics MeSH
- Insect Vectors genetics metabolism MeSH
- Genes, Insect * MeSH
- Larva genetics metabolism MeSH
- Odorants MeSH
- Receptors, Odorant genetics metabolism MeSH
- Rhodnius * genetics metabolism MeSH
- Sense Organs * embryology physiology MeSH
- Gene Expression Profiling MeSH
- Transcriptome MeSH
- Arthropod Antennae * MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Receptors, Odorant MeSH
Triatomines are vectors of Chagas disease and important model organisms in insect physiology. "Kissing bugs" are obligatory hematophagous insects. A blood meal is required to successfully complete oogenesis, a process primarily controlled by juvenile hormone (JH). We used Dipetalogaster maxima as an experimental model to further understand the roles of JH in the regulation of vitellogenesis and oogenesis. A particular focus was set on the role of JH controlling lipid and protein recruitment by the oocytes. The hemolymph titer of JH III skipped bisepoxide increased after a blood meal. Following a blood meal there were increased levels of mRNAs in the fat body for the yolk protein precursors, vitellogenin (Vg) and lipophorin (Lp), as well as of their protein products in the hemolymph; mRNAs of the Vg and Lp receptors (VgR and LpR) were concomitantly up-regulated in the ovaries. Topical administration of JH induced the expression of Lp/LpR and Vg/VgR genes, and prompted the uptake of Lp and Vg in pre-vitellogenic females. Knockdown of the expression of LpR by RNA interference in fed females did not impair the Lp-mediated lipid transfer to oocytes, suggesting that the bulk of lipid acquisition by oocytes occurred by other pathways rather than by the endocytic Lp/LpR pathway. In conclusion, our results strongly suggest that JH signaling is critical for lipid storage in oocytes, by regulating Vg and Lp gene expression in the fat body as well as by modulating the expression of LpR and VgR genes in ovaries.
- Keywords
- Endocytic receptors, Juvenile hormone, Lipid metabolism, Lipophorin, Oogenesis, Triatomine,
- MeSH
- Insecta metabolism physiology MeSH
- Insect Proteins metabolism MeSH
- Juvenile Hormones metabolism MeSH
- Lipoproteins metabolism MeSH
- Lipid Metabolism * MeSH
- Oocytes metabolism MeSH
- Oogenesis physiology MeSH
- Ovary metabolism MeSH
- Receptors, Cytoplasmic and Nuclear metabolism MeSH
- RNA Interference MeSH
- Signal Transduction MeSH
- Triatominae * metabolism physiology MeSH
- Vitellogenesis physiology MeSH
- Vitellogenins metabolism MeSH
- Animals MeSH
- Check Tag
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Research Support, N.I.H., Extramural MeSH
- Names of Substances
- Insect Proteins MeSH
- Juvenile Hormones MeSH
- lipophorin receptor MeSH Browser
- lipophorin MeSH Browser
- Lipoproteins MeSH
- Receptors, Cytoplasmic and Nuclear MeSH
- Vitellogenins MeSH
BACKGROUND: Kissing bugs (Triatominae) are blood-feeding insects best known as the vectors of Trypanosoma cruzi, the causative agent of Chagas' disease. Considering the high epidemiological relevance of these vectors, their biology and bacterial symbiosis remains surprisingly understudied. While previous investigations revealed generally low individual complexity but high among-individual variability of the triatomine microbiomes, any consistent microbiome determinants have not yet been identified across multiple Triatominae species. METHODS: To obtain a more comprehensive view of triatomine microbiomes, we investigated the host-microbiome relationship of five Triatoma species sampled from white-throated woodrat (Neotoma albigula) nests in multiple locations across the USA. We applied optimised 16S rRNA gene metabarcoding with a novel 18S rRNA gene blocking primer to a set of 170 T. cruzi-negative individuals across all six instars. RESULTS: Triatomine gut microbiome composition is strongly influenced by three principal factors: ontogeny, species identity, and the environment. The microbiomes are characterised by significant loss in bacterial diversity throughout ontogenetic development. First instars possess the highest bacterial diversity while adult microbiomes are routinely dominated by a single taxon. Primarily, the bacterial genus Dietzia dominates late-stage nymphs and adults of T. rubida, T. protracta, and T. lecticularia but is not present in the phylogenetically more distant T. gerstaeckeri and T. sanguisuga. Species-specific microbiome composition, particularly pronounced in early instars, is further modulated by locality-specific effects. In addition, pathogenic bacteria of the genus Bartonella, acquired from the vertebrate hosts, are an abundant component of Triatoma microbiomes. CONCLUSION: Our study is the first to demonstrate deterministic patterns in microbiome composition among all life stages and multiple Triatoma species. We hypothesise that triatomine microbiome assemblages are produced by species- and life stage-dependent uptake of environmental bacteria and multiple indirect transmission strategies that promote bacterial transfer between individuals. Altogether, our study highlights the complexity of Triatominae symbiosis with bacteria and warrant further investigation to understand microbiome function in these important vectors. Video abstract.
- Keywords
- Bacteria, Blood, Hematophagous, Insect, Microbiome, Ontogeny, Pathogen, Triatominae, Vector,
- MeSH
- Chagas Disease parasitology MeSH
- Animals, Wild classification microbiology MeSH
- Microbiota genetics physiology MeSH
- RNA, Ribosomal, 16S genetics MeSH
- Triatominae classification microbiology MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Video-Audio Media MeSH
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- RNA, Ribosomal, 16S MeSH