No Evidence of Rabies Exposure in Wild Marmosets (Callithrix jacchus) of Northeast Brazil.

Rabies transmitted by wildlife is the main source of human rabies mortality in Latin America and considered an emerging disease. The common marmoset Callithrix jacchus of Brazil is the only known primate reservoir of rabies worldwide. We tested whether alive free-ranging C. jacchus were exposed to rabies in four northeast states that have previously reported rabies-positive dead C. jacchus (Pernambuco and Bahia) or not (Paraíba and Rio Grande do Norte). Our results show no evidence of rabies antibodies or infection in the sampled C. jacchus, suggesting that apparently healthy marmosets are not widely exposed to rabies over their natural range.

Spatio-temporal dynamics of rabies and habitat suitability of the common marmoset Callithrix jacchus in Brazil.

Rabies transmitted by wildlife is now the main source of human rabies in the Americas. The common marmoset, Callithrix jacchus, is considered a reservoir of rabies causing sporadic and unpredictable human deaths in Brazil, but the extent of the spillover risk to humans remains unknown. In this study, we described the spatiotemporal dynamics of rabies affecting C. jacchus reported to Brazil's Ministry of Health passive surveillance system between 2008 and 2020, and combined ecological niche modelling with C. jacchus occurrence data to predict its suitable habitat. Our results show that 67 outbreaks (91 cases) of rabies affecting C. jacchus were reported by 41 municipalities between January 2008 and October 2020, with a mean of 5 outbreaks/year [range: 1-14]. The maximum number of outbreaks and municipalities reporting cases occurred in 2018, coinciding with higher surveillance of primate deaths due to Yellow Fever. A mean of 3 [1-9] new municipalities reported outbreaks yearly, suggesting potential spatial expansions of the C. jacchus variant in northeastern Brazil and emerging rabies spillover from vampire bat Desmodus rotundus to C. jacchus in the north and south. Outbreaks were concentrated in the states of Ceará (72%) and Pernambuco (16%) up to 2012, but are now reported in Piauí since 2013, in Bahia since 2017 (D. rotundus' antigenic variant, AgV3) and in Rio de Janeiro since 2019 (AgV3). Besides confirming suitable habitat for this primate in the northeast and the east coast of Brazil, our Maximum Entropy model also predicted suitable habitat on the north and the west states of the country but predicted low habitat suitability among inland municipalities of the Caatinga biome reporting rabies. Our findings revealed new areas reporting rabies infecting C. jacchus, highlighting the need to implement strategies limiting spillover to humans and to better understand the drivers of C. jacchus rabies dynamics.

An Introduction to the Callithrix Genus and Overview of Recent Advances in Marmoset Research.

We provide here a current overview of marmoset (Callithrix) evolution, hybridization, species biology, basic/biomedical research, and conservation initiatives. Composed of 2 subgroups, the aurita group (C aurita and C flaviceps) and the jacchus group (C geoffroyi, C jacchus, C kuhlii, and C penicillata), this relatively young primate radiation is endemic to the Brazilian Cerrado, Caatinga, and Atlantic Forest biomes. Significant impacts on Callithrix within these biomes resulting from anthropogenic activity include (1) population declines, particularly for the aurita group; (2) widespread geographic displacement, biological invasions, and range expansions of C jacchus and C penicillata; (3) anthropogenic hybridization; and (4) epizootic Yellow Fever and Zika viral outbreaks. A number of Brazilian legal and conservation initiatives are now in place to protect the threatened aurita group and increase research about them. Due to their small size and rapid life history, marmosets are prized biomedical models. As a result, there are increasingly sophisticated genomic Callithrix resources available and burgeoning marmoset functional, immuno-, and epigenomic research. In both the laboratory and the wild, marmosets have given us insight into cognition, social group dynamics, human disease, and pregnancy. Callithrix jacchus and C penicillata are emerging neotropical primate models for arbovirus disease, including Dengue and Zika. Wild marmoset populations are helping us understand sylvatic transmission and human spillover of Zika and Yellow Fever viruses. All of these factors are positioning marmosets as preeminent models to facilitate understanding of facets of evolution, hybridization, conservation, human disease, and emerging infectious diseases.

Natural and Anthropogenic Hybridization in Two Species of Eastern Brazilian Marmosets (Callithrix jacchus and C. penicillata).

Animal hybridization is well documented, but evolutionary outcomes and conservation priorities often differ for natural and anthropogenic hybrids. Among primates, an order with many endangered species, the two contexts can be hard to disentangle from one another, which carries important conservation implications. Callithrix marmosets give us a unique glimpse of genetic hybridization effects under distinct natural and human-induced contexts. Here, we use a 44 autosomal microsatellite marker panel to examine genome-wide admixture levels and introgression at a natural C. jacchus and C. penicillata species border along the São Francisco River in NE Brazil and in an area of Rio de Janeiro state where humans introduced these species exotically. Additionally, we describe for the first time autosomal genetic diversity in wild C. penicillata and expand previous C. jacchus genetic data. We characterize admixture within the natural zone as bimodal where hybrid ancestry is biased toward one parental species or the other. We also show evidence that São Francisco River islands are gateways for bidirectional gene flow across the species border. In the anthropogenic zone, marmosets essentially form a hybrid swarm with intermediate levels of admixture, likely from the absence of strong physical barriers to interspecific breeding. Our data show that while hybridization can occur naturally, the presence of physical, even if leaky, barriers to hybridization is important for maintaining species genetic integrity. Thus, we suggest further study of hybridization under different contexts to set well informed conservation guidelines for hybrid populations that often fit somewhere between "natural" and "man-made."

Hybridization effects and genetic diversity of the common and black-tufted marmoset (Callithrix jacchus and Callithrix penicillata) mitochondrial control region.

Hybridization is continually documented in primates, but effects of natural and anthropogenic hybridization on biodiversity are still unclear and differentiating between these contexts remains challenging in regards to primate evolution and conservation. Here, we examine hybridization effects on the mitochondrial DNA (mtDNA) control region of Callithrix marmosets, which provide a unique glimpse into interspecific mating under distinct anthropogenic and natural conditions. DNA was sampled from 40 marmosets along a 50-km transect from a previously uncharacterized hybrid zone in NE Brazil between the ranges of Callithrix jacchus and Callithrix penicillata. DNA was also collected from 46 marmosets along a 30-km transect in a hybrid zone in Rio de Janeiro state, Brazil, where exotic marmosets appeared in the 1980s. Combining Callithrix DNA sampled inside and outside of these hybrid zones, phylogenetic and network analyses show C. jacchus and C. penicillata being parental species to sampled hybrids. We expand limited Callithrix population genetics work by describing mtDNA diversity and demographic history of these parental species. We show ancient population expansion in C. jacchus and historically constant population size in C. penicillata, with the latter being more genetically diverse than the former. The natural hybrid zone contained higher genetic diversity relative to the anthropogenic zone. While our data suggest hybrid swarm formation within the anthropogenic zone due to removed physical reproductive barriers, this pattern is not seen in the natural hybrid zone. These results suggest different genetic dynamics within natural and anthropogenic hybridization contexts that carry important implications for primate evolution and conservation.