Biology subjects

Moreira, S. B.

Publications and source records attributed to Moreira, S. B..

7 recordsLinked to original sources

bioRxiv2025

Genomic Insights into Derived Dwarfism and Exudivory in a Genus (Callithrix) of the World's Smallest Anthropoid Monkeys

The primate Callitrichidae family represents the smallest anthropoid primates, which are known to possess dietary specializations for eating viscous plant exudates (exudivory), and as callitrichids Callithrix marmosets push these biological traits to extremes. Using low-coverage whole genome sequencing of Callithrix species, we investigated Callithrix evolutionary history, species genetic diversity, and the genomic basis of derived small body size and exudivory. Our phylogenetic species tree shows that Callithrix likely originated in southeastern Brazil and migrated northward to the semi-arid regions of central and northeastern Brazil. We show that there is greater genetic similarity between smaller and more exudivorous Callithrix species relative to larger and less exudivorous species, and that the genus likely experienced extensive past reticulation. Based on these results, we argue that the Callithrix migration from the Atlantic Forest biome to the relatively more extreme environments of Cerrado/Caatinga biomes progressively reduced body size and increased exudivory specialization in Callithrix marmosets. We also identified species-specific candidate genes under putative positive selection for traits that include body growth, bone development, reproduction, fat metabolism, insulin signaling, and liporegulation. In conclusion, we increased genomic resources for understudied Callithrix species, while providing the most comprehensive overview of marmoset genomic diversity to-date, and identify several candidate genes under positive selection for traits related to small body size and exudivory. Future studies should sample wild marmosets more widely and perform higher-coverage genomic sequencing to better understand how specific genomic variants may impact the evolution of key Callithrix biological traits.

evolutionary biology↗

bioRxiv2023

Lessons from a multilaboratorial task force for diagnosis of a fatal toxoplasmosis outbreak in captive primates in Brazil

As exemplified by the Coronavirus Disease 2019 (COVID-19) pandemic, infectious diseases may emerge and spread rapidly, often causing serious economic losses and public health concerns. In fact, disease outbreaks have become increasingly common, especially those of zoonotic origin. The Brazilian Ministry of Health is responsible for national epizootic surveillance. However, the systems focus primarily on diseases affecting humans has led to the neglect of other zoonotic diseases. In this report, we present an integrated investigation of an outbreak that occurred during the first year of the COVID-19 pandemic among captive neotropical primates housed at a primatology center in Brazil. After presenting a range of non-specific clinical signs, including fever, prostration, inappetence, and abdominal pain, ten primates from five different species died within approximately four days. Despite the state of health emergency due to the pandemic, a network of volunteer researchers was established to investigate the outbreak. A wide range of high-resolution techniques was used for different pathogens, including SARS-CoV-2 (RTq-PCR, ELISA and IHC), Toxoplasma gondii (IHC and IFA) and Escherichia coli (IFA), as well as a portable Metagenomic Sequencing utilizing Nanopore Technology. Within a span of four days after necropsies, we successfully identified T. gondii as the causative agent of this outbreak. This case highlights some of the obstacles faced with the current Brazilian surveillance system, which is still limited. A cross-platform interdisciplinary investigation could be a possible model for future epizootic investigations in non-human animals. Author summaryThe Brazilian epizootic surveillance system, under the regulation of the Ministry of Health, has been established to address a national list of compulsory notifiable diseases. However, focusing mainly on the risks to humans causes other zoonoses to be neglected. Here we present an outbreak that occurred during the first year of the COVID-19 pandemic that affected eleven neotropical primates (NP) belonging to six different species. Within four days of exhibiting a range of non-specific clinical signs, including fever, prostration, inappetence, and abdominal pain, ten NPs died. Despite testing negative for pathogens included in the national surveillance policy, a collaborative group of researchers investigated the outbreak in detail. Using integrated diagnostic techniques, we identified Toxoplasma gondii as the causative agent four days after necropsy. Toxoplasmosis causes devastating acute death outbreaks in neotropical primates and is currently absent in the national guidelines. This unified effort proved the effectiveness of a multidisciplinary collaborative surveillance network in facilitating precise diagnoses.

microbiology↗

bioRxiv2023

Validating Dynamic Body Acceleration metrics as a measure of energy expenditure in a Neotropical primate

2AO_SCPLOWBSTRACTC_SCPLOWQuantifying energy expenditure in free-living primates is fundamentally important yet challenging. Acceleration-based metrics such as Dynamic Body Acceleration (DBA), obtained from accelerometers, are potential proxies for energy expenditure, yet have not been previously validated in primates. Here, we validated DBA in black lion tamarins (Leontopithecus chrysopygus) by comparison to doubly labelled water (DLW) in 10 captive tamarins housed at the Rio de Janeiro Primate Centre. Individuals were equipped over 48 hours with a backpack with a tri-axial accelerometer and received an intra-peritoneal DLW injection at the beginning of the experiment, with blood samples taken 1 and 48h later. Daily Energy Expenditure by DLW was 326 (SD=66) kJ/day, close to expected values for primates of their size. The accelerometers recorded at 40 Hz, collecting >6.9 million records per axis for each individual. Individual DBA metrics were calculated and regressed against DLW daily energy measures. From this regression, we found a consistent and significant linear relationship (R2 = 0.46) between DLW and DBA, which could be improved by the incorporation of activity and resting time information (R2 = 0.52). Our results provide the first estimates of total daily energy expenditure for black lion tamarins and a validation of the method for estimating energy expenditure through accelerometers. Given the similar levels of total energy expenditure of captive and wild primates, this method can now be used in the field to estimate the energy cost of black lion tamarin movements in its natural environment. 1 SO_SCPLOWUMMARYC_SCPLOWO_SCPCAP C_SCPCAPO_SCPLOWSTATEMENTC_SCPLOWDynamic body acceleration was validated against doubly labelled water in black lion tamarins, showing it is a useful tool for measuring free-living energy demands.

zoology↗

bioRxiv2023

Pelage Variation and Morphometrics of Closely Related Callithrix Marmoset Species and Their Hybrids

BackgroundHybrids are expected to show greater phenotypic variation than their parental species, yet how hybrid phenotype expression varies with genetic distances in closely-related parental species remains surprisingly understudied. Here we study pelage and morphometric trait variation in anthropogenic hybrids vailable at the end of the article between four species of Brazilian Callithrix marmosets, a relatively recent primate radiation. Marmoset species are distinguishable by pelage phenotype and morphological specializations for eating tree exudates. Here, we (1) describe qualitative phenotypic pelage differences between parental species and hybrids; (2) test whether significant quantitative differences exist between parental and hybrid morphometric phenotypes; and (3) determine which hybrid morphometic traits show heterosis, dysgenesis, trangression, or intermediacy relative to the parental trait. For morphometric traits, we investigated both cranial and post-cranial traits, particularly as most hybrid morphological studies focus on the former instead of the latter. Finally, we estimate mitogenomic distances between marmoset species from previously published data. ResultsMarmoset hybrid facial and overall body pelage variation reflected novel combinations of coloration and patterns present in parental species. In morphometric traits, C. jacchus and C. penicillata were the most similar to each other, while C. aurita was the most distinct, and C. geoffroyi trait measures fell between these other species. Only three traits in C. jacchus x C. penicillata hybrids showed heterosis. We observed heterosis and dysgenesis in several traits of C. penicillata x C. geoffroyi hybrids. Transgressive segregation was observed in hybrids of C. aurita and the other species. These hybrids were also C. aurita-like for a number of traits. Genetic distance was closest between C. jacchus and C. penicillata and farthest between C. aurita and the other species. ConclusionWe attributed significant morphometric differences between marmoset species to variable levels of morphological specialization for exudivory in these species. Our results suggest that intermediate or parental species-like hybrid traits relative to the parental trait values are more likely in crosses between species with relatively lesser genetic distance. More extreme phenotypic variation is more likely in parental species with greater genetic distance, with transgressive traits appearing in hybrids of the most genetically distant parental species. We further suggest that less developmental disturbances can be expected in hybrids of more recently diverged parental species, and that future studies of hybrid phenotypic variation should investigate selective pressures on Callithrix cranial and post-cranial morphological traits.

zoology↗

bioRxiv2020

Mitogenomic Phylogeny of Callithrix with Special Focus on Human Transferred Taxa

Callithrix marmosets are a relatively young primate radiation, whose phylogeny is not yet fully resolved. These primates are naturally para- and allopatric, but three species with highly invasive potential have been introduced into the southeastern Brazilian Atlantic Forest by the pet trade. There, these species hybridize with each other and endangered, native congeners. We aimed here to reconstruct a robust Callithrix phylogeny and divergence time estimates, and identify the biogeographic origins of autochthonous and allochthonous Callithrix mitogenome lineages. We sequenced 49 mitogenomes from four species (C. aurita, C. geoffroyi, C. jacchus, C. penicillata) and anthropogenic hybrids (C. aurita x Callithrix sp., C. penicillata x C. jacchus, Callithrix sp. x Callithrix sp., C. penicillata x C. geoffroyi) via Sanger and whole genome sequencing. We combined these data with previously published Callithrix mitogenomes to analyze five Callithrix species in total. ResultsWe report the complete sequence and organization of the C. aurita mitogenome. Phylogenetic analyses showed that C. aurita was the first to diverge within Callithrix 3.54 million years ago (Ma), while C. jacchus and C. penicillata lineages diverged most recently 0.5 Ma as sister clades. MtDNA clades of C. aurita, C. geoffroyi, and C. penicillata show intraspecific geographic structure, but C. penicillata clades appear polyphyletic. Hybrids, which were identified by phenotype, possessed mainly C. penicillata or C. jacchus mtDNA haplotypes. The biogeographic origins of mtDNA haplotypes from hybrid and allochthonous Callithrix were broadly distributed across natural Callithrix ranges. Our phylogenetic results also evidence introgression of C. jacchus mtDNA into C. aurita. ConclusionOur robust Callithrix mitogenome phylogeny shows C. aurita lineages as basal and C. jacchus lineages among the most recent within Callithrix. We provide the first evidence that parental mtDNA lineages of anthropogenic hybrid and allochthonous marmosets are broadly distributed inside and outside of the Atlantic Forest. We also show evidence of cryptic hybridization between allochthonous Callithrix and autochthonous C. aurita. Our results encouragingly show that further development of genomic resources will allow to more clearly elucidate Callithrix evolutionary relationships and understand the dynamics of Callithrix anthropogenic introductions into the Brazilian Atlantic Forest.

genomics↗

bioRxiv2019

The genome of the zoonotic malaria parasite Plasmodium simium reveals adaptions to host-switching

BackgroundPlasmodium simium, a malaria parasite of non-human primates (NHP) was recently shown to cause zoonotic infections in humans in Brazil. We sequenced the P. simium genome to investigate its evolutionary history and to identify any genetic adaptions that may underlie the ability of this parasite to switch between host species. ResultsPhylogenetic analyses based on whole genome sequences of P. simium from humans and NHPs reveals that P. simium is monophyletic within the broader diversity of South American Plasmodium vivax, suggesting P. simium first infected NHPs as a result of a host-switch of P. vivax from humans. The P. simium isolates show the closest relationship to Mexican P. vivax isolates. Analysis of erythrocyte invasion genes reveals differences between P. vivax and P. simium, including large deletions in the Duffy Binding Protein 1 (DBP1) and Reticulocyte Binding Protein 2a genes of P. simium. Analysis of P. simium isolated from NHPs and humans revealed a deletion of 38 amino acids in DBP1 present in all human-derived isolates, whereas NHP isolates were multi-allelic. ConclusionsAnalysis of the P. simium genome confirmed a close phylogenetic relationship between P. simium and P. vivax, and suggests a very recent American origin for P. simium. The presence of the DBP1 deletion in all human-derived isolates tested suggests that this deletion, in combination with other genetic changes in P. simium, may facilitate the invasion of human red blood cells and may explain, at least in part, the basis of the recent zoonotic infections.

genomics↗

bioRxiv2019

The Effects of Host Taxon, Hybridization, and Environment on the Gut Microbiome of Callithrix Marmosets

Mammalian captive dietary specialists like folivores are prone to gastrointestinal distress and primate dietary specialists suffer the greatest gut microbiome diversity losses in captivity compared to the wild. Marmosets represent another group of dietary specialists, exudivores that eat plant exudates, but whose microbiome remains relatively less studied. The common occurrence of gastrointestinal distress in captive marmosets prompted us to study the Callithrix gut microbiome composition and predictive function through bacterial 16S ribosomal RNA V4 region sequencing. We sampled 59 wild and non-wild Callithrix across four species and their hybrids. Host environment had a stronger effect on the gut microbiome than host taxon. Wild Callithrix gut microbiomes were enriched for Bifidobacterium, which process host-indigestible carbohydrates. Captive marmoset guts were enriched for Enterobacteriaceae, a family containing pathogenic bacteria. While gut microbiome function was similar across marmosets, Enterobacteriaceae seem to carry out most functional activities in captive host guts. More diverse bacterial taxa seem to perform gut functions in wild marmosets, with Bifidobacterium being important for carbohydrate metabolism. Non-wild marmosets showed gut microbiome composition aspects seen in human gastrointestinal diseases. Thus, captivity may perturb the exudivore gut microbiome, which raises implications for captive exudivore welfare and calls for husbandry modifications.

microbiology↗