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Article

Evolutionary Diversity of Bat Rabies Virus in São Paulo State, Brazil

by
Luzia H. Queiroz
1,*,†,
Angélica C. A. Campos
2,3,*,†,
Marissol C. Lopes
4,
Elenice M. S. Cunha
5,
Avelino Albas
6,
Cristiano de Carvalho
1,
Wagner A. Pedro
1,
Eduardo C. Silva
4,
Monique S. Lot
7,
Sandra V. Inácio
4,
Danielle B. Araújo
3,8,
Marielton P. Cunha
9,
Edison L. Durigon
8,
Luiz Gustavo B. Góes
2 and
Silvana R. Favoretto
3,8,10
1
Departamento de Produção e Saúde Animal, Faculdade de Medicina Veterinária de Araçatuba, UNESP—Universidade Estadual Paulista, Araçatuba 16050-680, Brazil
2
Institut Pasteur de São Paulo—IPSP, São Paulo 05508-020, Brazil
3
Programa de Pós-Graduação Interunidades em Biotecnologia, Laboratório de Virologia Clínica e Molecular, Departamento de Microbiologia, Instituto de Ciências Biomédicas, USP—Universidade de São Paulo, São Paulo 05508-000, Brazil
4
FAPESP Scholarship, Faculdade de Medicina Veterinária de Araçatuba, UNESP—Universidade Estadual Paulista, Araçatuba 16050-680, Brazil
5
Secretaria de Agricultura e Abastecimento, Instituto Biológico de São Paulo, São Paulo 04016-035, Brazil
6
Agência Paulista de Tecnologia dos Agronegócios, Unidade de Pesquisa e Desenvolvimento de Presidente Prudente, Presidente Prudente 19015-970, Brazil
7
CNPq Technical Assistance Fellowship, Faculdade de Farmácia, UNIP—Universidade Paulista, Campus Araçatuba, Araçatuba 16018-555, Brazil
8
Núcleo de Pesquisas em Raiva—NPR, Departamento de Microbiologia, Instituto de Ciências Biomédicas, USP—Universidade de São Paulo, São Paulo 05508-000, Brazil
9
Laboratório de Bioinformática e Virologia, Departamento de Genética, Evolução, Microbiologia e Imunologia, Instituto de Biologia, UNICAMP—Universidade de Campinas, Campinas 13083-862, Brazil
10
Instituto Pasteur—Secretaria da Saúde do Estado de São Paulo, São Paulo 01311-000, Brazil
*
Authors to whom correspondence should be addressed.
These authors contributed equally for this work.
Viruses 2025, 17(8), 1063; https://doi.org/10.3390/v17081063
Submission received: 11 April 2025 / Revised: 5 July 2025 / Accepted: 9 July 2025 / Published: 30 July 2025
(This article belongs to the Special Issue Advances in Rabies Research 2024)

Abstract

The history of the rabies virus dates back four millennia, with the virus being considered by many to be the first known transmitted between animals and humans. In Brazil, rabies virus variants associated with terrestrial wild animals, marmosets, and different bat species have been identified. In this study, bat samples from different regions of São Paulo State, in Southeast Brazil, were analyzed to identify their genetic variability and patterns. A total of 51 samples were collected over ten years (1999–2009) and submitted to the immunofluorescent technique using monoclonal antibodies for antigenic profile detection (the diagnostic routine used in Latin American countries) and genetic evolution analysis through maximum likelihood approaches. Three antigenic profiles were detected: one related to the rabies virus maintained by hematophagous bat populations (AgV3), part of the monoclonal antibody panel used, and two other profiles not included in the panel (called NC1 and NC2). These antigenic profiles were genetically distributed in five groups. Group I was related to hematophagous bats (AgV3), Groups II and III were related to insectivorous bats (NC1) and Groups IV and V were also related to insectivorous bats (NC2). The results presented herein show that genetic lineages previously restricted to the northwest region of São Paulo State are now found in other state regions, highlighting the need for a comprehensive genetic study of bat rabies covering geographic and temporal space, through expanded genomic analysis using a standard genomic fragment.

1. Introduction

Rabies is one of the most important viral infectious diseases and, with a history dating back four millennia, is considered by many to be the first known disease transmitted between animals and humans [1]. Rabies was initially described in humans and carnivores, but studies of bats and rabies in Brazil and Trinidad in the 1920s and 1930s showed the existence of a rabies virus aerial cycle. The existence of the aerial cycle explained epidemics that occur without the presence of carnivorous animals and how the virus continues to circulate in places where rabies in domestic animals has been controlled, showing the interrelationship of this aerial cycle with the terrestrial cycle [1,2,3].
The rabies virus (RABV) belongs to the Rhabdoviridae family and Lyssavirus genus, which contains 18 viral species [4], most of them associated with bats from the Old World. The Lyssavirus rabies species is the only one that circulates among numerous mammals, including bats, carnivores, and nonhuman primates, such as marmosets in Brazil [5,6,7]. Cross-species transmission has been observed among non-canid carnivores, bats, and other mammal species, leading to the emergence of new lineages also related to American bats [5].
Antigenic characterization studies have been conducted in several Latin American countries using a panel of monoclonal antibodies (MAbs) produced by the Centers for Disease Control and Prevention (CDC), Atlanta, USA. The use of these MAbs, from the 1980s onwards, established a new era in the knowledge of RABV reservoirs and transmissibility, resulting in immediate advances in epidemiological surveillance in those countries before laboratories implemented sequencing capability. Over the years, this tool has identified several other antigenic profiles not included in the original panel [6] established by Diaz et al. [8]. These additional profiles were detected in many countries, including Brazil [9,10,11,12,13,14,15]. In a certain way, this was already expected, considering that among the samples analyzed for establishing the panel profiles, there were no varieties of isolates from different South American bat species. This identification technique continues to be used routinely in most Latin American countries.
The genetic analysis of the N gene, with a chosen genome fragment (between position 1157 and 1476 of PV-NC_001542), not only allowed the correlation of host species with their geographic distributions but also confirmed the differences observed in the reactivity pattern in the antigenic tests among samples associated with different species of bats in different countries [9,16,17,18].
In Brazil, the first antigenic [11] and genetic [19] studies showed that, as in other Latin American countries, the two predominant antigenic variants/viral lineages were associated with viruses maintained by dogs (called AgV1 and AgV2) and the Desmodus rotundus variant (AgV3). Later, antigenic variants/viral lineages associated with terrestrial wild animals, such as foxes and wild dogs [20,21], marmosets [6], and different species of insectivorous and frugivorous bats, were identified [13,22,23,24,25,26].
Both the genetic and antigenic characterizations of bat RABV isolated in the State of São Paulo in southeastern Brazil have shown the existence of variants/lineages related to D. rotundus (AgV-3), Tadarida brasiliensis (AgV4), and Lasiurus sp. (AgV6), also circulating in other species of insectivorous and frugivorous bats, along with other antigenic profiles that were not included in the CDC monoclonal panel [6,8,10,21,22].
In this study, bat samples from different regions of São Paulo State were analyzed using evolutionary approaches to identify genetic variability of the RABV in São Paulo. These isolates are compared with isolates described in previous publications, characterized antigenically and genetically, for which sequences have been deposited in Genbank (Table A1, Appendix A).

2. Materials and Methods

2.1. Samples

This study included RABV isolates from 32 municipalities in different administrative regions of São Paulo State in Southeast Brazil (Figure 1), between 1999 and 2010.
All the samples had been previously diagnosed as positive for rabies by means of the fluorescent antibody test (FAT) [27] and mouse inoculation test (MIT) [28], considered the gold standard at the time of receiving samples for diagnosis between 1995 and 2010. In all, 48 bat samples were studied: 13 frugivorous (11 Artibeus lituratus, 01 Artibeus planirostris, 01 Artibeus fimbriatus) and 35 insectivorous (04 Myotis nigricans, 10 Neoeptesicus furinalis, 03 Neoeptesicus diminutus, 01 Neoeptesicus sp., 05 Molossus fluminensis, 03 Molossus molossus, 01 Cynomops abrasus, 02 Nyctinomops laticaudatus, 01 Nyctinomops macrotis, 01 Lasiurus blossevillii, 01 Lasiurus ega, 01 Eumops glaucinus and 02 non-hematophagous (NH) bats not identified). Samples from one cat, one bovine, and one horse were also included, giving 51 samples in total (Table 1).

2.2. Antigenic Characterization

Antigenic characterization was performed using the CDC (Atlanta, GA, USA) monoclonal antibodies (MAbs) panel according to the protocol determined by Favoretto et al. [11]. These eight MAbs against the RABV nucleoprotein, developed by CDC, can identify different RABV variants through different reactivity patterns.

2.3. Sequencing and Genetic Characterization

For genetic characterization, the initial steps (i.e., extracting RNA and obtaining cDNA) were performed using methods described in previous studies [13]. Molecular reactions were performed using primers described previously by Smith et al. [32] and Campos et al. [33] to amplify 320 base pairs from the coding and non-coding region of the nucleoprotein (between positions 1157 and 1476 of PV-NC_001542). Double-strand PCR-amplified products were purified using the ExoSAP-IT system (GE Healthcare Bio-Sciences Ltd.—USB Corporation, Cleveland, OH, USA) according to the manufacturer’s instructions, and Sanger sequencing was performed as previously described by Campos et al. [33]. The excess dideoxynucleotide terminators were removed with the Applied Biosystems Big Dye XTerminatorTM Purification Kit (Applied Biosystems, Foster City, CA, USA), following the manufacturer’s recommendations. Purified samples were subjected to electrophoresis in POP6 polymer using an ABI-PRISM model 3100 automatic sequencer (Applied Biosystems, Foster City, CA, USA). The samples were tracked automatically using the Automatic DNA Analyzer software package of the ABI-PRISM model 3100.

2.4. Phylogenetic Analysis

The obtained nucleotide sequences were pre-analyzed using the BLASTn program (https://blast.ncbi.nlm.nih.gov/Blast.cgi, accessed on 19 February 2025) to confirm amplification of the specific product and then aligned with available GenBank sequences (Appendix A) using Geneious Prime software version 2019.2.3. The chosen GenBank sequences were selected based on full information like the host, place, and year of collection. Pairwise distances were calculated by MEGA 11 version 11.0.13 (available at https://www.megasoftware.net/ accessed on 19 February 2025) and phylogenetic trees were reconstructed using IQTREE software version 2.4.0 (available at http://www.iqtree.org/ accessed on 18 February 2025). The best model fit determined by IQTree was TIM + F + I + G4. To analyze the temporal virus variability, we used TempEst v1.5.3 (available at http://tree.bio.ed.ac.uk/software/tempest/ accessed on 19 February 2025) in the phylogenetic tree and root-to-tip method with best-fitting root in correlation function. The time-scaled phylogenetic tree was analyzed via Augur version 21.1.0 and auspice version 2.62.0 implemented on Nextstrain [34,35].

2.5. Phylogenetic and Antigenic Site Amino Acid Visualization

Phylogenetic visualization of RABV sequences was conducted using R version 4.4.1 (14 June 2024, ucrt). A phylogenetic tree in nexus format was imported using the ape package and further processed and visualized with the ggtree, treeio, and igraph packages. The final annotated phylogenetic tree was visualized with tip points colored with regard to geographic location and a scale bar indicating time (years) and genetic distance (substitutions/site). The final figure editing and layout adjustments were performed using the Inkscape program version 1.3.2. The alignment used for phylogenetic tree reconstruction was translated to amino acid and used to prepare one Figure with the region of antigenic site I present in the nucleoprotein.

3. Results

Among the fifty-one samples submitted to antigenic characterization, twenty-five (49%) were characterized as AgV-3 (RABV maintained by D. rotundus hematophagous bat populations) and twenty-six were characterized as RABV maintained by non-hematophagous bat populations (NC1 and NC2); out of these, twenty-one (41.2%) presented the antigenic profile NC1 and five (9.8%) presented the antigenic profile NC2.
The samples from this study were segregated into five different phylogenetic groups, highlighted in colors according to their genetic and antigenic patterns (Figure 2). The group called Group I showed samples with a genetic lineage associated with the virus maintained by D. rotundus hematophagous bats and antigenic variant AgV3. The virus groups isolated from insectivorous bats presented four independent phylogenetic clades, called Group II, Group III, Group IV, and Group V, with the antigenic profile NC1 in Groups II and III, and antigenic profile NC2 in Groups IV and V. Group II presented the greatest diversity of its host species, consisting of Eptesicus spp. (currently called Neoeptesicus), Eumops spp., Myotis spp., Nyctinomops spp., and Lasiurus spp. Groups VI and VII, with isolates external to the present study, presented isolates from marmosets (Group VI) and bat isolates related to Tadarida brasiliensis (Group VII).
The lowest percentage of identity was observed in comparison with the clade related to marmosets (Group VI in the phylogenetic tree). Estimates of evolutionary divergence over sequence pairs between groups, obtained using the maximum likelihood method in MEGA 11, were used to calculate the distances between groups (Table A2, Appendix A), showing a range from 8.7% between Groups I and VII to 17.9% between Groups II and VI. Among the groups detected in this study, the highest within-group distances (Table A3, Appendix A) were observed in Groups II (6.7%), III (4.7%), and V (5.7%) while minor within-group distances were detected in Groups IV (1.8%) and I (2.5%).
In Figure 1, we can also observe the geographic distribution of the samples from this study and from Genbank, used for the reconstruction of the phylogenetic tree, according to the resulting groups (genetic characterization) and antigenic variants/profiles (AgV-3, NC1, and NC2).
During the analysis of the antigenic site present in the nucleoprotein, we identified genetic signatures for some groups in the phylogenetic tree. Groups I, IV, V, VI, and VII and the root group showed recognized patterns (AET, AEV, TEV, TEA, TEM, and TDV, respectively), indicating the stability of these genetic groups. On the other hand, we could not identify any pattern for Groups II (TEA, TDE, IDT, TEV, and TDV) and III (TEA, TEL, and TEV). In these groups, we found higher variability that was confirmed by tree topology and can be seen in Figure 3. The full map of the antigenic site was produced and can be accessed in the Supplementary Materials.
The Pearson correlation coefficient calculated in the analysis of temporal virus variability in this dataset was 0.18 (p = 0.015), as shown in Figure 4. Although the correlation coefficient is slightly positive, the TempEst analysis showed the stable evolution rate to the dataset during the sampling period considered in the analysis.

4. Discussion

All 13 fruit bats of the genus Artibeus presented antigenic variant 3 (AgV-3), as did bats from the genera Molossus (04), Eumops (1), and Neoeptesicus (2) and non-identified bats (2). Similar results were observed in rabies-positive bat samples from other regions of São Paulo State [11,15,19,24,36]. Previous studies had demonstrated that the frequency of RABV in Artibeus was higher than that in Desmodus bats in the study area [36,37,38,39], which could explain how AgV-3 is present in species that do not co-inhabit with D. rotundus species. This is corroborated by the finding that the genetic lineage of D. rotundus is not exclusive to the species since this lineage has been detected in non-hematophagous bats such as the fruit bat Artibeus lituratus [40] and insectivorous bats in this study, in addition to other previous studies [13].
The samples antigenically described as NC1 in phylogenetic group II were segregated with samples from the same geographic region and with one sample (EU981922) from Uruguay, with a geographical distance of more than 1,200 miles. The samples in the phylogenetic group III were segregated with samples from the same geographical region and with one sample (AB297647) from Rio de Janeiro State, more than 300 m away, and another sample (AB618034) from Paraiba State, more than 1600 m away. This antigenic profile was previously described in São Paulo State [11,12,13,14,15,41]. These groups were previously related particularly with host species described by Oliveira et al. [42]; nonetheless, in the present study, we observed different species in the same clade/phylogenetic group. Bats play an important role in virus transmission and spread in the Americas [42,43,44], and it was clearly demonstrated in this study that insectivorous bats present a heterogeneous genetic distribution independent of host species.
The NC2 antigenic profile detected in five samples from the Molossus and Lasiurus genera was previously described in the same geographical region [7] and was observed in three monophyletic clades with high bootstrap value support (81 to 98%). In a previous study [13], two samples (GU646777 and HM854031) were segregated independently as subgroups; in the present study, these samples were segregated as part of phylogenetic groups IV and V, confirming the importance of including more sequences and information from other regions of the state and the country, as well as from other bat host species. This was also visualized on the map (Figure 1), where the geographical distribution of the variants was described. With the inclusion of new samples, a more homogeneous distribution of antigenic profiles and genetic lineages across Sao Paulo State can be observed since, previously, these profiles and lineages were restricted to the northwest region of the state [13]. Nonetheless, important data from previous publications regarding the central region of this state and from other states of Brazil could not be compared with the isolates from this study, considering that the authors sequenced a different genome region or only a coding region [15,40,42,45,46,47]. This reinforces the idea that the same region of the genome should be analyzed and standardized by researchers in future studies.
Currently, the term “antigenic variants” and the CDC MAbs panel still are used mainly in Latin America and only in a few accredited laboratories. The results obtained in the present sample’s dataset corroborated previous results [13,15] that showed that this panel, despite its valuable importance in the past, does not have sufficient resolution as high as that obtained using genetic tools to characterize RABV variants from non-hematophagous bats, leading to divergences. An approach of comparing samples from different geographical regions using antigenic and genetic characterization is no longer ideal, as previously highlighted in other studies [15]. In any case, the term ‘antigenic variant’ will not become extinct immediately since it is still the language used in Ministry of Health reports in Brazil, for example. As found in this study, the antigenic characterization was realized during sample processing almost twenty years ago, providing useful information that could be used for future studies and to better understand rabies epidemiology. Therefore, future RABV studies must be focused on genetic analyses to provide a deeper and more comprehensive understanding of the virus, explaining its epidemiology, its dynamics, and possible interventions. This could lead to significant advances in rabies surveillance, prevention, and control at both population and individual levels.
Antigenic site I was presented here using nucleoprotein amino acid alignments, and the authors observed a genetic signature that had previously been described [6]. However, for genetic groups II and III, these signatures could not be observed; in fact, they are genetically and antigenically diverse, independent of the comparison between these two approaches.
In the first RABV genetic studies in Latin America, it was established that the 320 nucleotides in the nucleoprotein carboxi-terminus region, including the nucleo- and phosphoprotein intergenic regions (non-coding) between genome positions 1157 and 1476 (based in PV genome NC_001542), could be the standard for phylogenetic studies because this region presents the large nucleotide variability, 1.9 times greater than in the coding region [17]. For phylogenetic analyses, according to Smith et al. [46], groups that present a distance higher than 5% from other groups can be considered a distinct genetic lineage. Thus, for this study, the groups in the phylogenetic tree were determined by following this consideration.
In the phylogenetic tree (Figure 3 and Figure S1), the high bootstrap values (100% for aerial cycle of transmission; 78% for genetic lineages segregated into Groups I, II, III and VII; and 81% for Groups I, II and VII) support the presence of basal genotypes of the virus. For example, sample HQ666860 from an insectivorous bat, Neoeptesicus furinalis, collected in 2009 presented a long branch in Group II (bootstrap 81%), indicating a high number of nucleotide substitutions. Group I, Group III, Group IV, and Group V showed bootstrap values of 100%, 98%, 78% and 92%, respectively; this tree topology could also explain how and why samples in the antigenic analysis from genetic groups II to V presented a different antigenic profile.
The positive but low correlation coefficient (0.18) associated with the phylogenetic analysis suggests that during the short period of sequence sampling, between the years of 1986 and 2022, there was an accumulation of diversity, but the occurrence of the common ancestor to all sequences was distant in the past. This had been previously shown by other researchers [42], and this result means a stable RABV evolution rate in the analyzed period. This result reflects the profile of zoonotic viruses such as rabies, considering only the aerial cycle, and agrees with the TMRCA (time to the most recent common ancestor) of approximately 170 years determined by de Souza et al. [40] when analyzing the D. rotundus/A. lituratus genetic lineage (both antigenically AgV3).

5. Conclusions

Despite some limitations, such as analyzing only a 320-nucleotide fragment; the limited number of sequences available in GenBank for this same fragment; the absence of relevant information such as on the date, species, and collection location of these available sequences in the GenBank; and the retrospective nature of this study performed over a decade ago, these data provide valuable insights into RABV among bats. The key findings of this study are as follows: (i) antigenic profiles and genetic lineages previously restricted to the northwest region of the state of São Paulo are now found in other state regions, (ii) future rabies studies must be focused only on genetic analysis, and (iii) there is a need for a comprehensive genetic study of bat rabies in São Paulo State and greater Brazil with diverse sample locations and expanded genomic analyses using a standard genomic fragment or full genome when possible. Moreover, focusing only on host species could lead to misleading conclusions about RABV evolution and dispersal concerning time and geography.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/v17081063/s1, Figure S1: Conventional phylogenetic tree, Figure S2: Partial amino acid antigenic site I for all sequences used in phylogenetic tree reconstruction.

Author Contributions

Conceptualization: L.H.Q., S.R.F. and A.C.A.C.; methodology, L.H.Q., A.C.A.C., M.C.L., E.M.S.C., A.A., C.d.C., W.A.P., E.C.S., M.S.L., S.V.I., D.B.A. and S.R.F.; software, A.C.A.C., M.P.C. and L.G.B.G.; validation, A.C.A.C., M.C.L., E.C.S., M.S.L., S.V.I. and D.B.A.; formal analysis, A.C.A.C., L.H.Q., M.P.C. and L.G.B.G.; investigation, A.C.A.C. and L.H.Q.; resources, S.R.F., E.L.D. and L.G.B.G.; data curation, A.C.A.C. and L.H.Q.; writing—original draft preparation, A.C.A.C. and L.H.Q.; writing—review and editing, A.C.A.C., L.H.Q., S.R.F., D.B.A., M.P.C. and L.G.B.G.; visualization, A.C.A.C., L.H.Q. and S.R.F.; supervision, L.H.Q., S.R.F. and E.L.D.; project administration, L.H.Q.; funding acquisition, L.H.Q., S.R.F. and E.L.D. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)—grant number 2008/00976-0 and 2007/01843-0 and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)—grant number 578281/2008-2. Data analysis and publication were supported by LGBG FAPESP 2022-13054-0. Scholarships: A.C.A.C.—CNPq 102474/2022-2 and FAPESP 2024-08821-8; M.C.L.—FAPESP (04/12793-6); E.C.S.—FAPESP (2008/08423-0); M.S.L.—CNPq technical assistance (grant number 578281/2008-2), S.V.I.—FAPESP (2008/00976-0). M.P.C. was supported by the Fund to Support Teaching, Research and Extension (FAEPEX/UNICAMP) (grant #2502/24). L.G.B.G. is supported by Young Research Project FAPESP 2022/13054-0. A.C.A.C. is currently supported by Young Research Project FAPESP 2024/10801-5.

Institutional Review Board Statement

The study was conducted in accordance with the ethics principles of the Brazilian College of Animal Experimentation (COBEA) and approved by the Animal Experimentation Ethics Committee of the School of Dentistry and Veterinary Medicine of Araçatuba, UNESP (Process No. 00858-2012 and 00902-2016).

Informed Consent Statement

Not applicable.

Data Availability Statement

The original contributions presented in this study are included in the article. Further inquiries can be directed to the corresponding author(s).

Acknowledgments

The authors thank Adriana Ruckert da Rosa for bat species revision.

Conflicts of Interest

The authors declare no conflicts of interest.

Appendix A

Table A1. Bat sample sequences used in this work [47,48,49,50,51,52,53,54].
Table A1. Bat sample sequences used in this work [47,48,49,50,51,52,53,54].
Sequence IDGroupYearHostSite OriginCountryGenbank AccessReference
AB201802_BR_AL4I2002Artibeus lituratusDracena, SPBrazilAB201802[24]
AB201803_BR_DR1I2000Desmodus rotundusLindóia, SPBrazilAB201803[24]
AB201805_BR_DR3I2001Desmodus rotundusSão José do Barreiro, SPBrazilAB201805[24]
AB201806_BR_NL1III1998Nyctinomops laticaudatusSão José do Rio Preto, SPBrazilAB201806[24]
AB201807_BR_NL2II1999Nyctinomops laticaudatusSão José do Rio Preto, SPBrazilAB201807[24]
AB201808_BR_NL3III2001Nyctinomops laticaudatusNova Granada, SPBrazilAB201808[24]
AB201812_BR_EF2II2001Eptesicus furinalisOlimpia, SPBrazilAB201812[24]
AB201813_BR_EF3II2001Eptesicus furinalisSão José do Rio Preto, SPBrazilAB201813[24]
AB201814_BR_EF4II2002Eptesicus furinalisCatanduva, SPBrazilAB201814[24]
AB201815_BR_MM1IV1999Molossus molossusJales, SPBrazilAB201815[24]
AB201816_BR_MM2IV2002Molossus molossusIlha Solteira, SPBrazilAB201816[24]
AB201817_BR_MR1I2002Molossus rufusPresidente Venceslau, SPBrazilAB201817[24]
AB201818_BR_MA1IV2000Molossus abrasusItapira, SPBrazilAB201818[24]
AB297630_BR_AL6I2001Artibeus lituratusRio de Janeiro, RJBrazilAB297630[48]
AB297631_BR_AL7I2004Artibeus lituratusVargem Grande Paulista, SPBrazilAB297631[48]
AB297647_BR_NL4III2004Nyctinomops laticaudatusRio de Janeiro, RJBrazilAB297647[48]
AB618034_strain_MPVIIII2007Molossus molossusSanto Antonio, ParaíbaBrazilAB618034Unpublished
AF394886_2085V1986Lasiurus borealisWalker County, TexasUSAAF394886[49]
AF396064_cym3941_1995II1995Myotis chiloensis-ChileAF396064[50]
AY233427_Batbbt123VII2001Tadarida brasiliensisBuenos AiresArgentineAY233427[44]
AY233448_Stchmbt80III2000Histiotus montanusRio Turbio, Santa CruzArgentineAY233448[44]
AY233451_Batbbt125V2001Tadarida brasiliensisBuenos AiresArgentineAY233451[44]
AY654585_Brhm4097VI1998HumanCearáBrazilAY654585[6]
AY654586_Brsg4108VI1998Callithrix jacchus jacchusCearáBrazilAY654586[6]
AY654587_Brhm4138VI1998HumanCearáBrazilAY654587[6]
AY877435_V920I1993BovineChiapasMexicoAY877435[51]
DQ631835_bref8150_05III2005Eptesicus furinalisJundiaí, SPBrazilDQ631835[41]
EF363743_IP306_Portel_PA_2004I2004HumanPortel, PABrazilEF363743[52]
EF363751_IP5214Viseu_PA_2004I2004HumanViseu, PABrazilEF363751[52]
EF363757_IP7541Viseu_PA_2005I2005HumanViseu, PABrazilEF363757[52]
EU293113_9001FRAI1990Fox-French GuyanaEU293113[53]
EU293116_9704ARGVII1997bat-ArgentineEU293116[53]
EU873001_brctSP4551_96III1996catSão Paulo StateBrazilEU873001Unpublished, Favoretto
EU981922_IP6773U_2008II2008Myotis sp.-UruguayEU981922[43]
GU552788_IP2989_2007VII2007Nyctnomops laticaudatusJoanópolis, SPBrazilGU552788[25]
GU552789_IP1779_2006IV2006Molossus rufusRibeirão Preto, SPBrazilGU552789[25]
GU552790_IP1992_2005III2005Histiotus velatusVargem Grande Paulista, SPBrazilGU552790[25]
GU552791_IP6883_2006III2006Histiotus velatusCampo Limpo Paulista, SPBrazilGU552791[25]
GU552792_IP3321_2005III2005Histiotus sp.Belo Horizonte, MGBrazilGU552792[25]
GU552795_IP10529_2005III2005Nyctnomops laticaudatusRibeirão Preto, SPBrazilGU552795[25]
GU552796_IP4359_2007III2007Molossus molossusCampinas, SPBrazilGU552796[25]
GU552798_IP8089_2005III2005Nyctnomops laticaudatusSão Sebastião, SPBrazilGU552798[25]
GU552807_IP8061_2006II2006Eptesicus furinalisCampinas, SPBrazilGU552807[25]
GU552810_IP3056_2007II2007Eptesicus furinalisBarretos, SPBrazilGU552810[25]
GU552815_IP8665_2005II2005Myotis nigricansRibeirão Preto, SPBrazilGU552815[25]
GU552820_IP4157_2005II2005Myotis nigricansÁguas de Lindóia, SPBrazilGU552820[25]
GU552821_IP4896_2005II2005Myotis nigricansCaçapava, SPBrazilGU552821[25]
GU552824_IP2654_2006V2006Lasiurus cinereusGarça, SPBrazilGU552824[25]
GU592648_brdrusp100_07I2007Desmodus rotundusSão José do Barreiro, SPBrazilGU592648[33]
GU646775_brmn131_03II2003Myotis nigricansAraçatuba, SPBrazilGU646775[13]
GU646776_brmn45_03II2003Myotis nigricansAraçatuba, SPBrazilGU646776[13]
GU646777_brmm95_03V2003Molossus molossusNova Independência, SPBrazilGU646777[13]
GU646778_brmn38_03II2003Myotis nigricansPenápolis, SPBrazilGU646778[13]
GU646779_bral268_98I1998Artibeus lituratusMirandópolis, SPBrazilGU646779[13]
GU646780_bral452_99I1999Artibeus lituratusIlha Solteira, SPBrazilGU646780[13]
GU646781_bref431_04II2004Eptesicus furinalisBilac, SPBrazilGU646781[13]
GU646782_brlb46_04II2004Lasiurus blossevilliiValparaíso, SPBrazilGU646782[13]
GU646783_bral311_03I2003Artibeus lituratusPenápolis, SPBrazilGU646783[13]
GU646784_bral304_03I2003Artibeus lituratusPenápolis, SPBrazilGU646784[13]
GU646785_brmn150_03II2003Myotis nigricansAraçatuba, SPBrazilGU646785[13]
GU646786_brmn234_02II2002Myotis nigricansBilac, SPBrazilGU646786[13]
GU646787_bral625_01I2001Artibeus lituratusBirigui, SPBrazilGU646787[13]
GU646788_brmn610_01II2001Myotis nigricansSud Menucci, SPBrazilGU646788[13]
GU646789_bral499_01I2001Artibeus lituratusGuararapes, SPBrazilGU646789[13]
GU646790_bref126_01II2001Eptesicus furinalisPenápolis, SPBrazilGU646790[13]
GU646791_bral84_01I2001Artibeus lituratusGuararapes, SPBrazilGU646791[13]
GU646792_bref40_01II2001Epitesicus furinalisBilac, SPBrazilGU646792[13]
GU646793_breg01_01II2001Eumops glaucinusBilac, SPBrazilGU646793[13]
GU646794_brmn839_00II2000Myotis nigricansBilac, SPBrazilGU646794[13]
GU646795_bral566_00I2000Artibeus lituratusPenápolis, SPBrazilGU646795[13]
GU646796_bref213_00II2000Eptesicus furinalisAraçatuba, SPBrazilGU646796[13]
GU646818_brbv119_03I2003Bovine/CattleJosé Bonifácio, SPBrazilGU646818[13]
GU646828_brbv356_97I1997Bovine/CattleGuararapes, SPBrazilGU646828[13]
GU646833_brbv32_94T1994Bovine/CattleAraçatuba, SPBrazilGU646833[13]
GU646835_brdg70_93T1993DogAraçatuba, SPBrazilGU646835[13]
GU646841_brhr308_00I2000HorseBarbosa, SPBrazilGU646841[13]
GU646842_bral5341I1999Artibeus lituratusBirigui, SPBrazilGU646842[13]
GU646843_brmm4105I1998Molossus molossusMirandópolis, SPBrazilGU646843[13]
GU646844_brle4132I1988Lasiurus egaGlicério, SPBrazilGU646844[13]
GU646845_brmr4114I1998Molossus molossusPenápolis, SPBrazilGU646845[13]
GU646846_brmr4095I1998Molossus rufusAraçatuba, SPBrazilGU646846[13]
GU646849_brdg5356I2000DogIlha Solteira, SPBrazilGU646849[13]
GU646855_brct60_92T1992CatAndradina, SPBrazilGU646855[13]
GU646856_brmr298_07I2007Molossus rufusIlha Solteira, SPBrazilGU646856[13]
GU646857_brmn182_07II2007Myotis nigricansBilac, SPBrazilGU646857[13]
GU646858_brmr350_06I2006Molossus rufusAndradina, SPBrazilGU646858[13]
GU646859_bral309_06I2006Artibeus lituratusIlha Solteira, SPBrazilGU646859[13]
GU646860_bral195_06I2006Artibeus lituratusAraçatuba, SPBrazilGU646860[13]
GU646861_bref341_02II2002Epitesicus furinalisBirigui, SPBrazilGU646861[13]
HM173087_brmn100_05II2005Myotis nigricansGuararapes, SPBrazilHM173087[13]
HM173088_bral239_05I2005Artibeus lituratusBirigui, SPBrazilHM173088[13]
HM854029_brdg354_95I1995DogBirigui, SPBrazilHM854029[13]
HM854030_brct100_04I2004CatGuararapes, SPBrazilHM854030[13]
HM854031_brmr178_05IV2005Molossus rufusAndradina, SPBrazilHM854031[13]
HM854032_brmn391_05II2005Myotis nigricansIlha Solteira, SPBrazilHM854032[13]
HM854033_bral540_05I2005Artibeus lituratusAraçatuba, SPBrazilHM854033[13]
HM014315_brmm1994_08V2008Molossus molossusSão Paulo, SPBrazilHM014315[14]
HM014316_brmng2449_05III2005Molossops neglectusSão Paulo, SPBrazilHM014316[14]
HM014317_brmr6464_05II2005Myotis ripariusSão Paulo, SPBrazilHM014317[14]
HQ666824_bral346_99I1999Artibeus lituratusSão José do Rio Preto, SPBrazilHQ666824This work
HQ666825_brma777_00IV2000Cynomops abrasusIpiguá, SPBrazilHQ666825This work
HQ666826_brnl249_01III2001Nyctinomops macrotisSão José do Rio Preto, SPBrazilHQ666826This work
HQ666827_brnl250_01III2001Nyctinomops laticaudatusSão José do Rio Preto, SPBrazilHQ666827This work
HQ666828_bref636_01II2001Neoepitesicus furinalisOlímpia, SPBrazilHQ666828This work
HQ666829_bral808_01I2001Artibeus lituratusSão José do Rio Preto, SPBrazilHQ666829This work
HQ666830_bresp1019_01II2001Neoepitesicus sp.Cardoso, SPBrazilHQ666830This work
HQ666831_bref1070_01II2001Neoepitesicus furinalisSão José do Rio Preto, SPBrazilHQ666831This work
HQ666832_bref62_02II2002Neoepitesicus furinalisCatanduva, SPBrazilHQ666832This work
HQ666833_brmm109_02IV2002Molossus molossusIlha Solteira, SPBrazilHQ666833This work
HQ666834_brmn835_02II2002Myotis nigricansCajobi, SPBrazilHQ666834This work
HQ666835_bral992_02I2002Artibeus lituratusDracena, SPBrazilHQ666835This work
HQ666836_brmr1021_02I2002Molossus fluminensisPresidente Venceslau, SPBrazilHQ666836This work
HQ666837_bref1141_02II2002Neoepitesicus furinalisSanto Anastácio, SPBrazilHQ666837This work
HQ666838_brbat1256_02I2002Non- hematophagous batMartinópolis, SPBrazilHQ666838This work
HQ666839_bral1371_02I2002Artibeus lituratusPresidente Venceslau, SPBrazilHQ666839This work
HQ666840_bral1535_02I2002Artibeus lituratusTaciba, SPBrazilHQ666840This work
HQ666841_brmm1539_02I2002Molossus molossusPresidente Prudente, SPBrazilHQ666841This work
HQ666842_brle1782_02III2002Lasiurus egaPresidente Prudente, SPBrazilHQ666842This work
HQ666843_braj349_03I2003Artibeus planirostrisSanta Fé do Sul, SPBrazilHQ666843This work
HQ666844_brbat350_03I2003Non-hematophagous batCatanduva, SPBrazilHQ666844This work
HQ666845_bral791_03I2003Artibeus lituratusPresidente Prudente, SPBrazilHQ666845This work
HQ666846_brmn168_04II2004Myotis nigricansCampinas, SPBrazilHQ666846This work
HQ666847_brnl184_04III2004Nyctinomops laticaudatusSão José do Rio Preto, SPBrazilHQ666847This work
HQ666848_bral550_04I2004Artibeus lituratusCaçapava, SPBrazilHQ666848This work
HQ666849_breg329_05I2005Eumops glaucinusAraçatuba, SPBrazilHQ666849This work
HQ666850_bred43_09II2009Neoepitesicus diminutusPereira Barreto, SPBrazilHQ666850This work
HQ666851_bred84_09II2009Neoepitesicus diminutusAraçatuba, SPBrazilHQ666851This work
HQ666852_brmn149_09II2009Myotis nigricansCoroados, SPBrazilHQ666852This work
HQ666853_bral181_09I2009Artibeus lituratusPenápolis, SPBrazilHQ666853This work
HQ666854_bref199_09II2009Neoeptesicus furinalisDracena, SPBrazilHQ666854This work
HQ666855_bref224_09I2009Neoeptesicus furinalisParapuã, SPBrazilHQ666855This work
HQ666856_bral325_09I2009Artibeus lituratusBirigui, SPBrazilHQ666856This work
HQ666857_bral374_09I2009Artibeus lituratusGuararapes, SPBrazilHQ666857This work
HQ666858_brmr389_09I2009Molossus fluminensisGuararapes, SPBrazilHQ666858This work
HQ666859_brmn433_09II2009Myotis nigricansPenápolis, SPBrazilHQ666859This work
HQ666860_bref589_09II2009Neoeptesicus furinalisPenápolis, SPBrazilHQ666860This work
HQ666861_brbv672_09I2009BovineNarandiba, SPBrazilHQ666861This work
HQ666862_brmr17_10II2010Molossus fluminensisPenápolis, SPBrazilHQ666862This work
HQ666863_breq28_10I2010EquineTaciba, SPBrazilHQ666863This work
HQ666864_bred43_10I2010Neoeptesicus diminutusOsvaldo Cruz, SPBrazilHQ666864This work
HQ666865_bref60_10II2010Neoeptesicus furinalisBirigui, SPBrazilHQ666865This work
HQ666866_bref76_10II2010Neoeptesicus furinalisPenápolis, SPBrazilHQ666866This work
HQ666867_brmm169_10V2010Molossus molossusAraçatuba, SPBrazilHQ666867This work
HQ666868_brct171_10I2010FelineAraçatuba, SPBrazilHQ666868This work
HQ666869_brmr177_10V2010Molossus fluminensisBirigui, SPBrazilHQ666869This work
HQ666870_brlbl198_10V2010Lasiurus blossevilliiTeodoro Sampaio, SPBrazilHQ666870This work
HQ666871_bref299_10II2010Neoeptesicus furinalisPenápolis, SPBrazilHQ666871This work
HQ666872_brmr300_10I2010Molossus fluminensisPenápolis, SPBrazilHQ666872This work
JF916647_BRLB4096_1995V1995Lasiurus blossevilliiUnknownBrazilBRLB4096Unpublished, Favoretto
JF916650_brmyaSP4115_1998II1998Myotis albecensUnknownBrazilJF916650Unpublished, Favoretto
JF916652_bralusp041_05I2005Artibeus lituratusPresidente Prudente, SPBrazilJF916652[26]
JF916655_brlbusp040_07V2007Lasiurus blossevilliiPresidente Prudente, SPBrazilJF916655[26]
JF916656_bralusp042_07I2007Artibeus lituratusPresidente Prudente, SPBrazilJF916656[26]
JF916657_brmmusp043_07I2007Molossus molossusPresidente Prudente, SPBrazilJF916657[26]
JF916659_bralusp047_07I2007Artibeus lituratusPresidente Prudente, SPBrazilJF916659[26]
JF916661_bralusp049_07I2007Artibeus lituratusPresidente Prudente, SPBrazilJF916661[26]
JF916662_bralusp050_07I2007Artibeus lituratusPresidente Prudente, SPBrazilJF916662[26]
JF916663_bralusp052_07I2007Artibeus lituratusPresidente Prudente, SPBrazilJF916663[26]
JF916664_bralusp054_07VII2007Artibeus lituratusPresidente Prudente, SPBrazilJF916664[26]
JF916667_brmnusp058_07II2007Myotis nigricansPresidente Prudente, SPBrazilJF916667[26]
JF916668_brmnusp061_07II2007Myotis nigricansPresidente Prudente, SPBrazilJF916668[26]
JF916669_bralusp062_07I2007Artibeus lituratusPresidente Prudente, SPBrazilJF916669[26]
JF916671_brefusp064_07II2007Eptesicus furinalisPresidente Prudente, SPBrazilJF916671[26]
JF916672_bralusp069_07I2007Artibeus lituratusPresidente Prudente, SPBrazilJF916672[26]
JF916673_bralusp071_07I2007Artibeus lituratusPresidente Prudente, SPBrazilJF916673[26]
JF916674_bralusp001_08I2008Artibeus lituratusPresidente Prudente, SPBrazilJF916674[26]
JF916678_brefusp008_09II2009Eptesicus furinalisPresidente Prudente, SPBrazilJF916678[26]
KM594026_IP_512_09II2009Eptesicus furinalisRibeirão Preto, SPBrazilKM594026[42]
KM594027_IP_230_10II2010Eptesicus furinalisValinhos, SPBrazilKM594027[42]
KM594028_IP_346_10II2010Eptesicus furinalisTambaú, SPBrazilKM594028[42]
KM594029_IP_3208_06III2006Eptesicus furinalisVinhedo, SPBrazilKM594029[42]
KM594030_IP_1400_10II2010Myotis nigricansCampinas, SPBrazilKM594030[42]
KM594031_IP_163_10II2010Myotis nigricansCaieiras, SPBrazilKM594031[42]
KM594032_IP_497_10II2010Myotis nigricansCampinas, SPBrazilKM594032[42]
KM594034_IP_350_10III2010Nyctinomops laticaudatusConchal, SPBrazilKM594034[42]
KM594035_IP_412_10III2010Nyctinomops laticaudatusBarretos, SPBrazilKM594035[42]
KM594036_IP_542_10III2010Nyctinomops laticaudatusRibeirão Preto, SPBrazilKM594036[42]
KM594037_IP_3176_09VII2009Tadarida brasiliensisSanto André, SPBrazilKM594037[42]
KM594038_IP_1586_10VII2010Tadarida brasiliensisSão Bernardo do Campo, SPBrazilKM594038[42]
MG458314_RV1789I1997CowUnknownBritish Est IndiesMG458314[54]
PQ671596_RS61VII2022Tadarida brasiliensisRio Grande do SulBrazilPQ671596unpublished
Legend: samples in red are from this study; samples in blue are from our group’s previous study [13].
Table A2. Estimates of evolutionary divergence over sequence pairs between groups.
Table A2. Estimates of evolutionary divergence over sequence pairs between groups.
Gp_1Gp_3Gp_2Gp_4Gp_5Gp_7Gp_6
Gp_1
Gp_30.140
Gp_20.1280.126
Gp_40.1390.1030.138
Gp_50.1520.1340.1600.132
Gp_70.0870.1170.1180.1110.136
Gp_60.1810.1480.1790.1520.1580.167
outgroup0.1780.1800.1880.1620.1720.1820.213
Gp 1 means group I Related to hematophagous bats-AgV3, Gp 2 means group II Related to insectivorous bats-NC1, Gp 3 means group III Related to insectivorous bats-NC1, Gp 4 means group IV Related to insectivorous bats-NC2, Gp 5 means group V Related to insectivorous bats-NC2, Gp 6 means group VI Related to marmosets, Gp 7 means group VII Related to Tadarida brasiliensis-AgV4 and outgroup represents the Terrestrial cycle of transmission-root of phylogenetic tree.
Table A3. Estimates of average evolutionary divergence over sequence pairs within groups.
Table A3. Estimates of average evolutionary divergence over sequence pairs within groups.
Gp 10.0253
Gp 30.0467
Gp 20.0674
Gp 40.0185
Gp 50.0566
Gp 70.0029
Gp 60.0051
outgroup0.0051
Gp 1 means group I Related to hematophagous bats-AgV3, Gp 2 means group II Related to insectivorous bats-NC1, Gp 3 means group III Related to insectivorous bats-NC1, Gp 4 means group IV Related to insectivorous bats-NC2, Gp 5 means group V Related to insectivorous bats-NC2, Gp 6 means group VI Related to marmosets, Gp 7 means group VII Related to Tadarida brasiliensis-AgV4 and outgroup represents the Terrestrial cycle of transmission-root of phylogenetic tree.

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Figure 1. Geographic location of sample collection. Colors are related with antigenic variant/profile: red for Group I (AgV3) related to D. rotundus, orange for Group II and III (related to antigenic Non-compatible 1-NC1 profile), and dark blue for Groups IV and V (NC2). Cities where more than one genetic group and/or antigenic variant was detected are in pale blue with a graphic following determined pattern of colors. GenBank sequences used in phylogenetic tree reconstruction can be observed as red dots for Group I, orange stars for samples clustered in Groups II and III, and dark blue dots for Groups IV and V. The map was modified for this study using Inkscape software version 1.3.2 (available at www.inkscape.org accessed on 4 July 2025). The original map is available at https://pt.m.wikipedia.org/wiki/Ficheiro:SaoPaulo_MesoMicroMunicip.svg (accessed on 19 February 2025).
Figure 1. Geographic location of sample collection. Colors are related with antigenic variant/profile: red for Group I (AgV3) related to D. rotundus, orange for Group II and III (related to antigenic Non-compatible 1-NC1 profile), and dark blue for Groups IV and V (NC2). Cities where more than one genetic group and/or antigenic variant was detected are in pale blue with a graphic following determined pattern of colors. GenBank sequences used in phylogenetic tree reconstruction can be observed as red dots for Group I, orange stars for samples clustered in Groups II and III, and dark blue dots for Groups IV and V. The map was modified for this study using Inkscape software version 1.3.2 (available at www.inkscape.org accessed on 4 July 2025). The original map is available at https://pt.m.wikipedia.org/wiki/Ficheiro:SaoPaulo_MesoMicroMunicip.svg (accessed on 19 February 2025).
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Figure 2. Time-scaled phylogenetic tree reconstructed using 320 nucleotides from nucleoprotein terminal gene using IQ-TREE software version 2.4.0, visualized and edited using FigTree software version 1.4.4 and plotted in RStudio version 2024.12.1+563 using ggtree version 3.14.0, treeio version 1.30.0, and igraph version 2.1.4 packages. The samples from this study can be observed in the tree in red dots; other samples from Brazil, available in GenBank, are marked in a blue pallet of colors while samples from other countries are marked in a green pallet of colors. The groups determined in this study are delineated vertically by red (Group I), orange (Groups II and III), and dark blue (Groups IV and V) shading. The groups without segregated samples from this study are shown with pink (Group VI) and gray (Group VII) shadings.
Figure 2. Time-scaled phylogenetic tree reconstructed using 320 nucleotides from nucleoprotein terminal gene using IQ-TREE software version 2.4.0, visualized and edited using FigTree software version 1.4.4 and plotted in RStudio version 2024.12.1+563 using ggtree version 3.14.0, treeio version 1.30.0, and igraph version 2.1.4 packages. The samples from this study can be observed in the tree in red dots; other samples from Brazil, available in GenBank, are marked in a blue pallet of colors while samples from other countries are marked in a green pallet of colors. The groups determined in this study are delineated vertically by red (Group I), orange (Groups II and III), and dark blue (Groups IV and V) shading. The groups without segregated samples from this study are shown with pink (Group VI) and gray (Group VII) shadings.
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Figure 3. A partial amino-acid alignment showing the presence of antigenic site I in the nucleoprotein. The color match those in the phylogenetic tree presented in Figure 2. For this figure, the sequences used in the phylogenetic tree reconstruction were employed, maintaining only the variability in the antigenic site region, with a preference for sequences from this study. The genetic signature AET is shown in red (and also highlighted with red shading) for phylogenetic Group I related to hematophagous bat species D. rotundus; AEV is shown in dark blue (and also highlighted with dark blue shading) for phylogenetic Group IV related to non-hematophagous bats; TEV is shown in a gradient of dark blue (and also highlighted in a gradient dark blue shading) for phylogenetic Group V; TEA is shown in magenta/pink (and also highlighted with pink shading) for phylogenetic Group VI related to marmosets; TEM in black (and also highlighted with gray shading) for phylogenetic Group VII related to the bat species T. brasiliensis; TDV is shown in green for the root group related to the terrestrial cycle of transmission of RABV. For phylogenetic groups II and III (highlighted with gradient orange shading), it was not possible to find one genetic signature in the antigenic site I; in fact, in these groups, the variability was diverse and is noted in different colors: TEA in orange for the major antigenic site found (which was the same genetic signature found in Group VI related to marmosets), purple for variations (TEL, TDE, IDT), dark blue for the same signature present in Group V (TEV), and green for the same signature present in the terrestrial cycle of transmission (TDV) in one sequence available at GenBank (AF396064). The amino acid letters and class are outlined above.
Figure 3. A partial amino-acid alignment showing the presence of antigenic site I in the nucleoprotein. The color match those in the phylogenetic tree presented in Figure 2. For this figure, the sequences used in the phylogenetic tree reconstruction were employed, maintaining only the variability in the antigenic site region, with a preference for sequences from this study. The genetic signature AET is shown in red (and also highlighted with red shading) for phylogenetic Group I related to hematophagous bat species D. rotundus; AEV is shown in dark blue (and also highlighted with dark blue shading) for phylogenetic Group IV related to non-hematophagous bats; TEV is shown in a gradient of dark blue (and also highlighted in a gradient dark blue shading) for phylogenetic Group V; TEA is shown in magenta/pink (and also highlighted with pink shading) for phylogenetic Group VI related to marmosets; TEM in black (and also highlighted with gray shading) for phylogenetic Group VII related to the bat species T. brasiliensis; TDV is shown in green for the root group related to the terrestrial cycle of transmission of RABV. For phylogenetic groups II and III (highlighted with gradient orange shading), it was not possible to find one genetic signature in the antigenic site I; in fact, in these groups, the variability was diverse and is noted in different colors: TEA in orange for the major antigenic site found (which was the same genetic signature found in Group VI related to marmosets), purple for variations (TEL, TDE, IDT), dark blue for the same signature present in Group V (TEV), and green for the same signature present in the terrestrial cycle of transmission (TDV) in one sequence available at GenBank (AF396064). The amino acid letters and class are outlined above.
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Figure 4. Correlation between genetic divergence and sampling time was obtained by a root-to-tip analysis using the RABV sequences and plotted using R command line. The dots are related with clades from phylogenetic tree, the red dots are related with Group I, the orange with Group II, the brown with Group III, the blue with Group IV, the clear blue with Group V, the pink with Group VI, the clear gray with the Group VII and the dark gray dots are related with the terrestrial cycle of transmission. The dashed line (colored dark gray) represents the regression line, and the light gray area around the dashed line is the confidence interval.
Figure 4. Correlation between genetic divergence and sampling time was obtained by a root-to-tip analysis using the RABV sequences and plotted using R command line. The dots are related with clades from phylogenetic tree, the red dots are related with Group I, the orange with Group II, the brown with Group III, the blue with Group IV, the clear blue with Group V, the pink with Group VI, the clear gray with the Group VII and the dark gray dots are related with the terrestrial cycle of transmission. The dashed line (colored dark gray) represents the regression line, and the light gray area around the dashed line is the confidence interval.
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Table 1. Sequences obtained in the study, including environmental and geographical information.
Table 1. Sequences obtained in the study, including environmental and geographical information.
GenBank AccessID Sample/
Year
SpeciesPlace of OriginAntigenic
Variant/Profile
Genetic Lineage
HQ666824IB 346/99Artibeus lituratusSão José do Rio PretoV-3D. rotundus
HQ666825IB 777/00Cynomops abrasusIpiguáNC2Insect. Bats
HQ666826IB 249/01Nyctinomops macrotisSão José do Rio PretoNC1Insect. bats
HQ666827IB 250/01Nyctinomops laticaudatusSão José do Rio PretoNC1Insect. Bats
HQ666828IB 636/01Neoeptesicus furinalis *OlímpiaNC1Insect. Bats
HQ666829IB 808/01Artibeus lituratusSão José do Rio PretoV-3D. rotundus
HQ666830IB 1019/01Neoeptesicus sp. *CardosoNC1Insect. Bats
HQ666831IB 1070/01Neoeptesicus furinalis *São José do Rio PretoNC1Insect. Bats
HQ666832IB 62/02Neoeptesicus furinalis *CatanduvaNC1Insect. Bats
HQ666833IB 109/02Molossus molossusIlha SolteiraNC2Insect. Bats
HQ666834IB 835/02Myotis nigricansCajobiNC1Insect. Bats
HQ666835IB 992/02Artibeus lituratusDracenaV-3D. rotundus
HQ666836IB 1021/02Molossus fluminensis *Presidente VenceslauV-3D. rotundus
HQ666837IB 1141/02Neoeptesicus furinalis *Santo AnastácioNC1Insect. Bats
HQ666838IB 1256/02NH bat (not identified)MartinópolisV-3D. rotundus
HQ666839IB 1371B/02Artibeus lituratusPresidente VenceslauV-3D. rotundus
HQ666840IB 1535/02Artibeus lituratusTacibaV-3D. rotundus
HQ666841IB 1539/02Molossus molossusPresidente PrudenteV-3D. rotundus
HQ666842IB 1782/02Lasiurus egaPresidente PrudenteNC1D. rotundus
HQ666843IB 349/03Artibeus planirostrisSanta Fé do SulV-3D. rotundus
HQ666844IB 350/03NH bat (not identified)CatanduvaV-3D. rotundus
HQ666845IB 791/03Artibeus lituratusPresidente PrudenteV-3D. rotundus
-IB 826/03Artibeus fimbriatusSão José do Rio PretoV-3ND
HQ666846IB 168/04Myotis nigricansCampinasNC1Insect. Bats
HQ666847IB 184/04Nyctinomops laticaudatusSão José do Rio PretoNC1Insect. Bats
HQ666848IB 550/04Artibeus lituratusCaçapavaV-3D.rotundus
HQ666849LRU 329/05Eumops glaucinusAraçatubaV-3D.rotundus
-LRU 397/05Artibeus lituratusAraçatubaV-3ND
HQ666850LRU 43/09Neoeptesicus diminutus *Pereira BarretoNC1Insect. Bats
HQ666851LRU 84/09Neoeptesicus diminutus *AraçatubaNC1Insect. Bats
HQ666852LRU 149/09Myotis nigricansCoroadosNC1Insect. Bats
HQ666853LRU 181/09Artibeus lituratusPenápolisV-3D. rotundus
HQ666856LRU 325/09Artibeus lituratusBiriguiV-3D. rotundus
HQ666857LRU 374/09Artibeus lituratusGuararapesV-3D. rotundus
HQ666858LRU 389/09Molossus fluminensis *GuararapesV-3D. rotundus
HQ666859LRU 433/09Myotis nigricansPenápolisNC1Insect. Bats
HQ666860LRU 589/09Neoeptesicus furinalis *PenápolisNC1Insect. Bats
HQ666854LRPP 199/09Neoeptesicus furinalis *DracenaNC1Insect. Bats
HQ666855LRPP 224/09Neoeptesicus furinalis *ParapuãV-3D. rotundus
HQ666861LRPP 672/09Bovine/CattleNarandibaV-3D. rotundus
HQ666862LRU 17/10Molossus fluminensis *PenápolisNC1Insect. Bats
KU299782LRPP 28/10HorseTacibaV-3D. rotundus
HQ666864LRPP 43/10Neoeptesicus diminutus *Osvaldo CruzV-3D. rotundus
HQ666865LRU 60/10Neoeptesicus furinalis *BiriguiNC1Insect. Bats
HQ666866LRU 76/10Neoeptesicus furinalis *PenápolisNC1Insect. Bats
HQ666867LRU 169/10Molossus molossusAraçatubaNC2Insect. Bats
HQ666868LRU 171/10CatAraçatubaV-3D. rotundus
HQ666869LRU 177/10Molossus fluminensis *BiriguiNC2Insect. Bats
HQ666870LRPP 198/10Lasiurus blossevilliiTeodoro SampaioNC2Insect. Bats
HQ666871LRU 299/10Neoeptesicus furinalis *PenápolisNC1Insect. Bats
HQ666872LRU 300/10Molossus fluminensis *PenápolisV-3D. rotundus
ND = not done; NC = not compatible; NH = non-hematophagous; V-3 = variant 3. IB—Rabies Laboratory of “Instituto Biológico de São Paulo”; LRU—Rabies Laboratory of UNESP (São Paulo State University), Araçatuba; LRPP—Rabies Laboratory of APTA (São Paulo Agribusiness Technology Agency) of Presidente Prudente; * new taxonomy bat species classification according to [29,30,31].
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Queiroz, L.H.; Campos, A.C.A.; Lopes, M.C.; Cunha, E.M.S.; Albas, A.; de Carvalho, C.; Pedro, W.A.; Silva, E.C.; Lot, M.S.; Inácio, S.V.; et al. Evolutionary Diversity of Bat Rabies Virus in São Paulo State, Brazil. Viruses 2025, 17, 1063. https://doi.org/10.3390/v17081063

AMA Style

Queiroz LH, Campos ACA, Lopes MC, Cunha EMS, Albas A, de Carvalho C, Pedro WA, Silva EC, Lot MS, Inácio SV, et al. Evolutionary Diversity of Bat Rabies Virus in São Paulo State, Brazil. Viruses. 2025; 17(8):1063. https://doi.org/10.3390/v17081063

Chicago/Turabian Style

Queiroz, Luzia H., Angélica C. A. Campos, Marissol C. Lopes, Elenice M. S. Cunha, Avelino Albas, Cristiano de Carvalho, Wagner A. Pedro, Eduardo C. Silva, Monique S. Lot, Sandra V. Inácio, and et al. 2025. "Evolutionary Diversity of Bat Rabies Virus in São Paulo State, Brazil" Viruses 17, no. 8: 1063. https://doi.org/10.3390/v17081063

APA Style

Queiroz, L. H., Campos, A. C. A., Lopes, M. C., Cunha, E. M. S., Albas, A., de Carvalho, C., Pedro, W. A., Silva, E. C., Lot, M. S., Inácio, S. V., Araújo, D. B., Cunha, M. P., Durigon, E. L., Góes, L. G. B., & Favoretto, S. R. (2025). Evolutionary Diversity of Bat Rabies Virus in São Paulo State, Brazil. Viruses, 17(8), 1063. https://doi.org/10.3390/v17081063

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