Necromys lasiurus (Cricetidae: Sigmodontinae) from open areas of the Atlantic Forest of Rio de Janeiro: Population structure and implications for the monitoring of hantaviruses

ABSTRACT

The hairy-tailed bolo mouse, Necromys lasiurus (Lund, 1841), which is typical of the Cerrado (CE), has been recorded in some open areas within the Atlantic Forest (AF) domain of the Brazilian state of Rio de Janeiro (RJ). In the CE, N. lasiurus is a known reservoir of zoonotic agents, and is the reservoir of an orthohantavirus genotype, Araraquara virus (ARAV), the etiological agent of Hantavirus Pulmonary Syndrome (HPS). Given this, the presence of N. lasiurus has potentially negative implications for public health in the state, and therefore it is important to elucidate the origin of its populations in RJ and their connections with populations outside the AF known to carry the ARAV. In the present study we combined phylogenetic and phylogeographic approaches to elucidate the evolutionary history of N. lasiurus populations in RJ, and to test if their dispersal into the AF domain is recent or ancient. These analyses were based on sequences of the mitochondrial Cytochrome b gene, obtained from N. lasiurus specimens from the Atlantic Forest of Rio de Janeiro (AF-RJ), together with all the sequences of this gene available for N. lasiurus in GenBank. In addition to the phylogenetic and phylogeographic analyses, the sequences were used to test among five hypothetical demographic scenarios, proposed to explain the evolutionary history of the hairy-tailed bolo mouse in the state of RJ. The results of all the analyses indicated that populations from AF and the Arid Diagonal (AD) of South America, which includes the CE, diverged in the Late Pleistocene but reconnected in the Holocene. The RJ population (AF-RJ) resulted from this recent genetic admixture among diverging populations from AF and AD. Despite the recent reconnection, no evidence has been found that the AF-RJ N. lasiurus population acts as a reservoir of ARAV, although the continued genetic connectivity with those from AD highlight the need to reinforce the public health monitoring of orthohantavirus in this rodent, especially given the potential spillover of other genotypes. Overall, then, the results of the present study provide important new insights into the evolutionary history of N. lasiurus, which should contribute to the surveillance of orthohantaviruses, and the development of more effective measures for the prevention and control of this zoonosis.

KEY WORDS:
Cytochrome b; Hantavirus; Range Expansion; Rodent; Small Mammal; Zoonoses

INTRODUCTION

The Atlantic Forest and the Cerrado biomes, are Brazilian morphoclimatic domains that have distinct biotas, although they do share some species of small mammals (Carmignotto et al. 2012). Two hypotheses have been proposed to account for the occurrence of typical Cerrado biome taxa in the Atlantic Forest biome. The first hypothesis refers to historical connections between the Cerrado biome and enclaves of open habitats in the Atlantic Forest biome, such as montane grasslands and coastal shrublands (Gonçalves et al. 2007, Tavares et al. 2011, Lemos et al. 2015). These connections would have arisen through the constant shifts in climate and associated fluctuations in the distribution of forested and open habitats that occurred during the Pleistocene and the Holocene (Behling 1995, Parizzi et al. 1998, Behling 2002). These processes would have had significant impacts on the landscape (Behling 2003, Hadler et al. 2009, Lavor et al. 2018), as well as in the composition of the present-day communities of small mammals (Hadler et al. 2009, Tavares et al. 2011, Peçanha et al. 2017).

The second hypothesis does not exclude these histori cal processes, but considers that the recent anthropogenic deforestation and habitat fragmentation have replaced fo rested areas by open habitats, such as pastures and shrubby savanna, locally known as ‘campo sujo’ (Bastos et al. 2005, Olifiers et al. 2005, Rocha et al. 2007). These man-made formations have favored the geographic expansion of species typical to the Cerrado biome into the core area of the coastal Atlantic Forest biome. These species include the maned wolf, Chrysocyon brachyurus (Illiger, 1815) (Carnivora: Canidae; Chiarello et al. 2000, Paula et al. 2013, Bereta et al. 2017), and the rattlesnake, Crotalus durissus Linnaeus, 1758 (Squamata: Viperidae; Bastos et al. 2005, Duarte & Menezes 2013). This geographic expansion of allochthonous species promoted by anthropogenic impacts may have highly deleterious ecological consequences for the native communities, similar to those caused by the invasion of exotic species and their parasites, which eventually lead to the spread of zoonotic pathogenics to new habitats and hosts (Bruno and Bard 2012, Herrera et al. 2008).

The hairy-tailed bolo mouse, Necromys lasiurus (Lund, 1841), which is typical of the Cerrado biome (sensu lato), has been recorded in areas of open habitat within the Atlantic Forest of Rio de Janeiro (Santos et al. 2018). This rodent tends to be extremely abundant in many small mammal communities of the Cerrado and the Caatinga biomes, where it has a high intraspecific genetic diversity (Becker et al. 2007, Moreira 2015, Santos et al. 2018, Santos-Filho et al. 2006). In the Cerrado biome, N. lasiurus is the reservoir of an orthohantavirus genotype, known as Araraquara virus (ARAV), the etiological agent of hantavirus pulmonary syndrome (HPS) in the Brazilian Distrito Federal and the states of São Paulo, Minas Gerais, and Goiás (Suzuki et al. 2004, Figueiredo et al. 2009, de Araujo et al. 2015, Dusi et al. 2016, Guterres et al. 2018). Necromys lasiurus is also known to part of the reservoir network of other zoonoses, such as Rocky Mountain spotted fever, arenavirus, leishmaniasis, and bubonic plague (Andrade et al. 2015, Fernandes et al. 2015, Coelho et al. 2016, de Oliveira et al. 2023).

The Brazilian state of Rio de Janeiro, which is predomi nantly covered by the Atlantic Forest biome, is considered a silent zone for the occurrence of hantavirus disease, given that only a single human case has been notified up to now (Vargas et al. 2016, Oliveira et al. 2017). Nevertheless, this state is still an important area for the investigation of this zoonosis, due to the circulation of the Juquitiba virus (JUQV), an orthohantavirus genotype, also known to cause HPS, identified in humans and sigmondotine rodents in Rio de Janeiro state (Oliveira et al. 2004, Sobreira et al. 2008, Oliveira et al. 2009, Lamas et al. 2013, Strecht 2014, Oliveira et al. 2017). Thus, there is a high incidence of HPS cases reported in the neighboring states (Ministério da Saúde 2024). In this case, the presence and expansion of N. lasiurus in Rio de Janeiro state may have implications in the enzootic cycles of the zoonotic agents known to be hosted by this reservoir. In this context, Santos et al. (2018) estimated the potential distribution of N. lasiurus in Rio de Janeiro state and hypothesized that the presence of the species in open areas of the Atlantic Forest domain may be the result of a recent expansion from the Cerrado biome. However, this hypothesis of geographic expansion has not been tested so far.

Moreira (2015) recorded considerable genetic diversity in the mitochondrial cytochrome b gene among N. lasiurus specimens collected in different regions of the Cerrado biome and Caatinga biome, and the Pantanal wetland biome. This pattern indicates that at least five distinct populations are found within its distribution in central Brazil. However, this study did not verify the relationship between these populations and those present within the Atlantic Forest domain of Rio de Janeiro state.

The present study used a phylogeographic approach to elucidate the evolutionary history of N. lasiurus in the Brazilian state of Rio de Janeiro, and to test the alternative hypotheses of the recent or historical dispersal of N. lasiurus populations from neighboring biomes. This analysis was used to define the phylogeographic structure of the Rio de Janeiro populations, and their phylogenetic relationships with the populations found in other biomes, and the potential connectivity between these populations. The findings of this study provide an important database for the epidemiological monitoring of the zoonoses carried by this rodent and the control of potential outbreaks in the Atlantic Forest domain of Rio de Janeiro state.

MATERIAL AND METHODS

Samples and molecular data collection

The present study was based on the analysis of N. lasiurus specimens collected from the Atlantic Forest domain of Rio de Janeiro state (License number 13373 MMA/ICMBIO/SISBIO, license CEUA L-036/2018), together with all the Cytochrome b sequences of the species available in GenBank (^{Appendix 1}). The sample consisted of a total of 98 individuals, of which, 23 were obtained from the genetic database of the Laboratório de Biologia e Parasitologia de Pequenos Mamíferos Silvestres Reservatórios (LABPMR/IOC), and eight from the Instituto de Biodiversidade e Sustentabilidade (NUPEM/UFRJ) collection, while the other 67 sequences were obtained from GenBank (Appendix 1). All the sequences gene rated during the present study were deposited in GenBank, under accession numbers: PP068207-PP068237.

Genomic DNA was extracted from samples of liver tissue preserved in absolute ethanol using the Chelex protocol (Walsh et al. 1991). These tissue samples were obtained from N. lasiurus specimens collected from a series of different localities within the known area of occurrence of the species. The concentration and quality of the extracted DNA were verified by electrophoresis in 0.8% agarose gel. The copies of the mitocondrial Cytochrome b were amplified by Polymerase Chain Reaction (PCR), using the primers MVZ 05 and MVZ 16 (Smith and Patton 1993, 1999) to amplify a sequence of 800 base pairs, confirmed by electrophoresis in 1.5% agarose gel, the PCR products were purified using the PureLink™ PCR Purification kit (Invitrogen™, Waltham, MA, EUA), before being sequenced. The amplification reaction mixture contained 1.0 µl of DNA template, 2.5 µl of 10 × buffer (Invitrogen™), 1.0 µl of MgCl2 (50 mM; Invitrogen™), 0.5 µl of forward primer (10 mM), 0.5 µl of reverse primer (10 mM), 0.2 µl of dNTPs (10 mM), 0.2 µl of Platinum^® Taq DNA Polymerase (Invitrogen™), and Ultrapure water for a total volume of 19.1 µl. PCR amplification conditions consisted of an initial denaturation at 94 °C for 3 minutes, followed by 35 cycles of denaturation at 94 °C for 45 seconds, annealing at 48 °C for 60 seconds, extension at 72 °C for 90 seconds, and the final extension at 72 °C for 10 minutes. The sequences obtained here were aligned manually in Chromas Pro (Technelysium Inc.), using the N. lasiurus sequences available from GenBank as a reference.

Phylogeographic analyses

Sequences were aligned in Muscle and the substitution model that best fit the original data was selected using tests implemented in MEGA X (Kumar et al. 2018). The Mesquite v. 2.75 software was used to evaluate the presence of stop codons in the sequences. The HKY+G+I model was selected as the best nucleotide substitution model based on Maximum Likelihood (ML) analyses, which were run in Phyml (Guindon et al. 2010). Bayesian Inference (BI) of genealogies was implemented in MrBayes on the CIPRES V3.1. platform (Miller et al. 2010). Median-joining haplotype networks (Bandelt et al. 1999) were also compiled in PopArt 1.7. (Leigh and Bryant 2015), using GenBank sequences of the following taxa as the outgroup: Necromys obscurus (Waterhouse, 1837), Necromys lactens (Thomas, 1918), Akodon montesis Thomas, 1913, Brucepattersonius soricinus Hershkovitz, 1998, and Thalpomys lasiotis Thomas, 1916.

The most probable number of N. lasiurus genetic groups was inferred using the Bayesian Analysis of Population Structure (BAPS), run in BAPS 6.0 (Corander et al. 2008). In general, the grouping of the individuals by ecoregion or biome tended to coincide with the genetic groups inferred by this analysis. For this, the genetic mixing option was used, which includes information on the spatial relationships among the individuals in the analysis. The best K value was determined from 20 replicates with K values ranging from 1 to 10. The Arlequin 3.5 (Excoffier and Lischer 2010) program was used to compute population statistics for the groups inferred by the phylogenetic analyses and the previously-defined groups, as well as nucleotide diversity, the fixation index (F_ST), the components of the Analysis of Molecular Variance (AMOVA; Excoffier et al. 1992), Fu’s Fs test, Tajima’s D, and the tau, theta, and raggedness parameters of the mismatch distribution of the population groups. The Fu and Tajima statistics, and the mismatch distribution, were computed to test the hypothesis of recent demographic expansion. All maps were produced in Quantum Gis® program (QGIS 2023).

Evaluation of demographic scenarios

Approximate Bayesian Analysis was used to test among five hypothetical demographic scenarios involving the Atlan tic Forest domain of Rio de Janeiro state population and the other N. lasiurus populations. These analyses were run in DIYABC Random Forest 2.1 (Colin et al. 2021). This program simulates the population genetic statistics associated with each hypothetical demographic scenario, and then validates the scenarios by estimating their posterior probabilities given the empirical genetic data. The validation and posterior proba bilities were calculated using the “Random Forest” machine learning algorithm, with the scenarios being selected through the addition of the Linear Discriminant Analysis (LDA) to the axis of the vector. A total of 200,000 simulations were run assuming the HKY+ G + I substitution model, and the following priors of divergence time (t) and population size (N_e): for the three populations (N1, N2, N3), N_e was assumed to be between a minimum of 10 and maximum of 10,000, with t1= 2,000,000 generations and t2 = 100,000 generations, t1>t2, and mutation rate per generation 3 x 10^-8 (lower bound) and 7.3 x 10^-9 (Upper bound; Steppan and Schenck 2017). All the other priors were set to the default values provided by the program. Following the simulation, the scenarios were validated using Random Forest over 1,000 regression trees. After the selection of the best-fit scenario, a new tree was generated to estimate the t1 and t2 parameters of the best scenario, with the objective of obtaining a mean value of each parameter per generation. The value in years of parameters t1 and t2 were estimated from their number of generations, assuming a mean of five generations per year (da Rosa et al. 2021, Francisco et al. 1995). Given this, each year is the result of five generations reported in parameters t1 and t2.

The samples were arranged in four groups for these analyses, with one group representing the Rio de Janeiro state population, and the other three representing populations from the four ecoregions (Olson et al. 2001, Pavan et al. 2016) in which the study species occurs: the Arid Diagonal ecoregion of dry ecosystems that cross eastern South Ameri ca from southwest to northeast, and in Brazil, it includes the Cerrado biome and Pantanal biomes and part of the Caatinga biome; the Amazonia ecoregion, which coincides with the Amazon biome in Brazil; and the Atlantic Forest ecoregion which, for the purposes of this analysis, includes the Pampa biome, due to the paucity of records from this ecoregion and Atlantic Forest biome (Fig. 1; see also Pavan et al. 2016 for a more detailed description of the Brazilian ecoregions). Five hypothetical evolutionary scenarios were formulated here (Fig. 2), of which, two (1 and 4) were assu med genetic isolation among the different population groups after their divergence, while the other three (2, 3, and 5) assumed secondary introgression among the groups after their divergence. In scenario 1, Arid Diagonal ecoregion is the ancestral population of Atlantic Forest ecoregion, which originates Atlantic Forest of Rio de Janeiro state population. In scenario 2, Arid Diagonal ecoregion is also the ancestral population, but in this case, it admixed with the Atlantic Forest ecoregion population, resulting in Atlantic Forest of Rio de Janeiro state population. In scenario 3, by contrast, the ancestral population is Atlantic Forest of Rio de Janeiro state population, which admixture with Atlantic Forest ecoregion before originating Arid Diagonal ecoregion. In scenario 4 and 5, Arid Diagonal ecoregion is once again the ancestral population, in the former case, originating both Atlantic Forest ecoregion and Atlantic Forest of Rio de Janeiro state population, and in the latter, admixture with Atlantic Forest of Rio de Janeiro state population before originating the Atlantic Forest ecoregion population. This analysis permitted the identification of the potential ancestral population, as well as whether the diversification of the modern populations involved gene flow or not.

Figure 1
Distribution of Necromys lasiurus sample groups by ecoregion. The points are color-coded by ecoregion and sample group. Insert map shows the Brazilian biomes.

Figure 2
The demographic scenarios formulated for testing in the DIYABC Random Forest analysis. Pop1 = Arid Diagonal ecoregion (AD), Pop2 = Atlantic Forest ecoregion (AF), Pop3 = Atlantic Forest of Rio de Janeiro state (AF-RJ). The scenarios tested here were: (1) AD as the ancestral population of AF, which originates AF-RJ, (2) AD as the ancestral population, which mixes with AF before originating AF-RJ, (3) AF-RJ as the ancestral population, which mixes with AF before originating AD, (4) AD as the ancestral population of AF and AF-RJ, and (5) AD as the ancestral population, mixing with AF-RJ before originating AF.

The sample group from the Amazonia ecoregion was not included in the population analyses, given that the main objective of these analyses was to understand the relationships between the Atlantic Forest of Rio de Janeiro state populations and the groups from the neighboring biomes, i.e., the other Atlantic Forest localities, and the Pampa, Cerrado, and Caatinga domains.

RESULTS

Phylogeography

The consensus tree generated in both ML and the BI analyses recovered four well-supported clades within N. lasiurus (Fig. 3), an arrangement also observed in the haplotype network (Fig. 4). The clades were denominated according to the classification of Moreira (2015), namely, central-northern clade (clade CN), which includes samples from Brazilian Amazonia biome, the Cerrado biome and the Caatinga biome, central-eastern clade (clade CE), with samples from the Cerrado biome, Caatinga biome, and Atlantic Forest biome, western-cerrado clade (clade CW), which covers the Cerrado Biome and the Chaco dry forest of Paraguay, and the large, widespread south-southeastern clade (clade SS), which includes samples from the Atlantic Forest biome, the Cerrado biome, and the Chaco of both Argentina and Paraguay. The mean p distance between groups was 0.01, except in the case of clade CW, where it was 0.02. The same four-clade structure was found in the haplotype network, in which 55 haplotypes were recognized (Fig. 4). The sequences from the Atlantic Forest domain of Rio de Janeiro state were constituted as a monophyletic group, including two samples from Minas Gerais (Fig. 3). The Atlantic Forest domain of Rio de Janeiro state group is nested within the widespread clade SS, and is genetically closer to samples from São Paulo, Rio Grande do Sul, and Santa Catarina states (Fig. 5). The structure observed in both the phylogenies and the haplotype network was also confirmed in the BAPS analysis (Fig. 6), which revealed K = 4 groups (logML = -2207.9374).

Figure 3
Consensus phylogenetic tree produced by the Maximum Likelihood (ML) and Bayesian Inference (BI) analyses of the Cytochrome b sequences of Necromys lasiurus included in the present study. The clades are color-coded according to the results of the Bayesian Analysis of Population Structure (BAPS; see Fig. 6). The samples shaded green are from Atlantic Forest domain of Rio de Janeiro state. The circles at each branch represent the bootstrap values of the ML (left semi-circles) and the posterior probabilities of the BI (right semi-circles). In the left semi-circles, white indicates bootstrap values of 0.40-0.66, while gray represents values of 0.66-0.90, and black, values of over 0.90. In the right semi-circles, white indicates a posterior probability of less than 0.64, with gray representing posterior probabilities of 0.64-0.90, and black, values of over 0.90.

Figure 4
Haplotype network of the Necromys lasiurus Cytochrome b sequences analyzed in the present study, color-coded according to the results of the Bayesian Analysis of Population Structure (BAPS; see Fig. 6). (AF-RJ) Atlantic Forest domain of Rio de Janeiro state. Mutational steps are indicated with stripes.

Figure 5
Haplotype network of the Necromys lasiurus Cytochrome b sequences obtained in the present study from localities in the Atlantic Forest and Pampa biomes (AF), color-coded by locality. (ARG) Argentina, (MS) Mato Grosso do Sul, (MG) Minas Gerais, (PY) Paraguay, (PR) Paraná, (RJ) Rio de Janeiro, (RS) Rio Grande do Sul, (SC) Santa Catarina, (SP) São Paulo. Mutational steps are indicated with stripes.

Figure 6
Results of the Bayesian Analysis of Population Structure (BAPS) of the Necromys lasiurus Cytochrome b sequences compiled in the present study, showing the four genetic clades, which are color-coded. The vertical black lines separate the sample groups. Insert map shows the Brazilian biomes.

Genetic diversity

The Atlantic Forest domain of Rio de Janeiro state group presented moderate haplotype diversity (0.4299 ± 0.1079) and low nucleotide diversity (0.003238 ± 0.002062) in comparison to the other sample groups, which presented relatively higher levels of haplotype diversity (Table 1). The lowest level of genetic divergence, in terms of the F_ST index, was found between the Atlantic Forest ecoregion and Arid Diagonal ecoregion sample groups, while the highest divergence was recorded between Atlantic Forest domain of Rio de Janeiro state and Arid Diagonal ecoregion (Table 2).

Table 1
Genetic diversity of the Necromys lasiurus Cytochrome b sequences analyzed in the present study. (AF-RJ) Atlantic Forest domain of Rio de Janeiro state, (AF) Atlantic Forest ecoregion, (AM) Amazonia ecoregion, (AD) Arid Diagonal ecoregion.

Group	Number of haplotypes	Haplotype diversity (h)	Nucleotide diversity - π (%)
AF-RJ	8	0.4299 ± 0.1079	0.003238 ± 0.002062
AF (except RJ)	17	1.0000 ± 0.0202	0.019008 ± 0.010112
AM	6	0.7778 ± 0.7778	0.007511 ± 0.004526
AD	25	0.9636 ± 0.0166	0.055556 ± 0.056322
All samples	56	0.9301 ± 0.0207	0.021487 ± 0.010771

Table 2
Genetic distances between the Necromys lasiurus sample groups, based on the F_ST values. (AF-RJ) Atlantic Forest domain of Rio de Janeiro state, (AF) Atlantic Forest ecoregion, (AD) Arid Diagonal ecoregion.

	AF-RJ	AF (except RJ)	AD
AF-RJ	0.00000
AF (except RJ)	0.22929*	0.00000
AD	0.30228*	0.07996*	0.00000

• *Significant distances (p < 0.05).

The AMOVA showed that the genetic differences between the Atlantic Forest domain of Rio de Janeiro state group and the other groups (Atlantic Forest ecoregion + Arid Diagonal ecoregion) are lower than those found between individuals of the same sample group (Table 3), with F_ST va lues of 0.41571-0.91816 (p < 0.05). The analyses of neutrality (Tajima’s D and Fu’s Fs) of the Atlantic Forest domain of Rio de Janeiro state specimens returned negative values, although they were very close to zero, and only the D values were significant (Table 4), which indicates only a slight tendency for population expansion. This tendency was corroborated by the mismatch distribution, which did not refute the null hypothesis of demographic expansion (p = 0.34; Table 4, Fig. 7).

Figure 7
Mismatch distribution of the Necromys lasiurus samples from the Rio de Janeiro state, Brazil. The observed frequencies are shown in red, and the expected frequencies, in green.

Table 3
Results of the Analysis of Molecular Variance (AMOVA) of the N. lasiurus sample groups analyzed in the present study, arranged by set (within parentheses). (AF-RJ) Atlantic Forest domain of Rio de Janeiro state, (AF) Atlantic Forest ecoregion, (AD) Arid Diagonal ecoregion.

(AF-RJ) vs. (AF, AD)
Source of the variation	d.f.	Sum of the squares	Components of the variance	Percentageof the variation
Between sets	1	67.163	0.90960 Va	13.59
Between the groups within the sets	1	22.646	0.74350 Vb	11.11
Within sample groups	86	433.484	5.04051 Vc	75.30
Total	88	523.292	6.69361
FST (Vc)	0.24697	p = 0.00000 ± 0.00000
FSC (Vb)	0.12854	p = 0.00386 ± 0.00064
FCT (Va)	0.13589	p = 0.33228 ± 0.00403

Table 4
Results of the analyses of population expansion in the Necromys lasiurus samples from the Atlantic Forest domain of Rio de Janeiro state (AF-RJ).

Mismatch distribution AF-RJ				Tajima’s D		Fu’s Fs
Tau	θ0	θ1	Raggedness index	D	p	Fs	p
1.311	2.125	13.34473	0.05397 (p = 0.3427)	-2.45366	0.00*	-1.33958	0.172

• *Significant values (p < 0.05).

Selection of the demographic scenario

The best scenario selected by the DIYABC Random Forest analysis based on the Posterior Probability was scenario 2, with 398 “votes” and a posterior probability of 0.721 (Fig. 8). This scenario proposes secondary genetic connectivity among the Atlantic Forest domain of Rio de Janeiro state, Atlan tic Forest ecoregion, and Arid Diagonal ecoregion groups, after the divergence between Atlantic Forest ecoregion and Arid Diagonal ecoregion groups. The scenarios that proposed the complete isolation among the groups (scenarios 1 and 4) had lower posterior probabilities, with only 99 “votes” for scenario 1, and 76 “votes” for scenario 4. The other two scenarios postulating introgression presented moderate ade quacy, with scenario 3 receiving 229 “votes”, and scenario 5, 198 “votes”. These findings indicate that the scenarios with no gene flow were the least supported, in statistical terms. The mean time in years estimated for the t1 in scenario 2, which represents the time of primary divergence between Atlantic Forest ecoregion and Arid Diagonal ecoregion, was ~94,120 years (90% HPD: ~18,707 - ~266,584 years), whereas the mean value for t2, which represents the time of introgression among Atlantic Forest ecoregion, Atlantic Forest domain of Rio de Janeiro state and Arid Diagonal ecoregion, was ~7,455 years (HPD 90%: ~561 -18.459).

Figure 8
Plot of the DIYABC Random Forest simulations for the five hypothetical demographic scenarios proposed for the Necromys lasiurus groups (Atlantic Forest ecoregion, Atlantic Forest domain of Rio de Janeiro state, and Arid Diagonal ecoregion), and the location of the observed data, used to validate the best scenario. In this analysis, scenario 1 received 99 “votes”, scenario 2, 398 “votes”, scenario 3, 229 “votes”, and scenario 4, 76 “votes”, with 198 “votes” for scenario 5.

DISCUSSION

Our phylogenetic, haplotype network, BAPS, and DYABC Random Forest analyses reveal that the population of the hairy-tailed bolo mouse, N. lasiurus from Rio de Janeiro state is the result of genetic admixture between other popu lations from the Atlantic Forest ecoregion and the Arid Diagonal ecoregion of South America (Fig. 2), corroborating the model represented by the hypothetical demographic scenario 2. This scenario proposes that, following an initial event of primary divergence, the Atlantic Forest ecoregion and Arid Diagonal ecoregion were reconnected secondarily through the Atlantic Forest domain of Rio de Janeiro state population.

The timing of the secondary connection (t2) was estimated by the DIYABC Random Forest analysis at a mean value ofapproximately 7,455 years (90% HPD: ~561-18,459), which indicates that the admixture of the Atlantic Forest ecoregion and Arid Diagonal ecoregion populations that originated the Atlantic Forest domain of Rio de Janeiro state population occurred relatively recent, during the Holocene. The climatic events of the Holocene influenced the landscape of the study region (Behling 2003, Hadler et al. 2009) and, in turn, the composition of the small mammal communities of the Arid Diagonal ecoregion and the Atlan tic Forest ecoregion of southern and southeastern Brazil (Hadler et al. 2009, Tavares et al. 2011, Peçanha et al. 2017). Open habitats persisted in the Atlantic Forest ecoregion during the early and mid-Holocene, as remnants of the Late Pleistocene last glacial maximum (Behling 1995, 2002, Parizzi et al. 1998). This landscape may have favored the dispersal of N. lasiurus from the Arid Diagonal ecoregion to the coastal Atlantic Forest ecoregion, and eventually, the area today delimited by the Atlantic Forest domain of Rio de Janeiro state.

Other South American rodents typical of open habitats appear to have diverged earlier, during the Pleistocene, as in the case of the species of Cerradomys, which had its diversification occurring around 1.32 million years ago (Di-Nizo et al. 2022). Tavares et al. (2011) suggested that the similarities and past connections of the coastal restinga of Rio de Janeiro state with open areas of the Cerrado biome during this period may account for the presence of Cerradomys goytaca (Tavares, Pessôa & Gonçalves, 2011) in the lowlands of the state. Another example is the rodent Oxymycterus nasutus (Waterhouse, 1837), which also appears to have diverged and dispersed during the Pleistocene (Peçanha et al. 2017). Overall, then, the Late Quaternary climatic conditions contributed significantly to the recent divergence of many rodent species.

Even though the dispersal of N. lasiurus occurred before the extensive deforestation of Atlantic Forest ecoregion during the last two centuries, it is likely that recent anthropogenic modifications of the landscape, substituting forest environments by open habitats, have favored the connectivity and gene flow between the Atlantic Forest domain of Rio de Janeiro state populations and those of the Arid Diagonal ecoregion. Similar processes appear to have occurred in the case of the rattlesnake C. durissus, that expanded its range favored by shifts in land use (Guerra et al. 2023), and the recent dispersal of the maned wolf, C. brachyurus, which also appears to have been influenced by human actions (Chiarello et al. 2000, Paula et al. 2013, Bereta et al. 2017).

The Atlantic Forest domain of Rio de Janeiro state popu lations are genetically close to the Atlantic Forest ecoregion and Arid Diagonal ecoregion populations. The small number of haplotypes observed here, which are separated by relatively few mutational steps in the haplotype network, the reduced genetic distances indicated by the F_ST, and the greater differentiation between the sets of samples observed in the AMOVA are all consistent with recent gene flow among these three populations (Dutech et al. 2004, Cuterra et al. 2005, Gonçalves et al. 2009, Kajdacsi et al. 2013). The persistent connectivity between the Atlantic Forest domain of Rio de Janeiro state and Arid Diagonal ecoregion populations of N. lasiurus is also supported by the recent confirmation of the presence of helminth endoparasites, recorded previously only in the Cerrado biome, in specimens collected in the municipalities of Casimiro de Abreu and Silva Jardim, in the coastal lowlands of Rio de Janeiro state (Lucio et al. 2021).

It is interesting to note that the phylogenetic analyses included the populations of N. lasiurus from Atlantic Forest domain of Rio de Janeiro state in the clade SS of Moreira (2015). This clade encompasses populations from some Atlan tic Forest ecoregion localities, as well as areas of the Arid Diagonal ecoregion, and encompasses an extremely ample geographic area, with short branches in the phylogenetic tree, a star-shaped distribution in the haplotype network, and other features characteristic of a process of demographic and spatial expansion (Posada and Crandall 2001). This scenario was indeed corroborated by the Tajima’s D and mismatch distribution results.

The potential for the exchange of parasites and pathogens between hosts and the introduction of these species into new habitats has clear implications for the epidemiology of zoonoses that are harmful to human health. Hantaviruses have been responsible for hundreds of deaths since their discovery in the Cerrado biome (Ministério da Saúde 2024). Necromys lasiurus is known to be the reservoir of the ARAV, with a prevalence approximately 4% in the Cerrado biome populations of this rodent (Figueiredo et al. 2010; Limongi et al. 2013, 2016). Up to now, however, no evidence has been found that N. lasiurus acts as a reservoir of ARAV in the open areas of Atlantic Forest ecoregion in Rio de Janeiro state (Santos et al. 2018).

The existence of gene flow between host populations is an important factor in predicting the diffusion of host-associated pathogens, where populations with gene flow will exchange pathogens more easily among themselves than populations without gene flow (Vollmer et al. 2011, Milholland et al. 2019, Saxenhofer et al. 2022).

Other authors suggested that the Atlantic Forest ecoregion provides more favorable conditions for the expansion of N. lasiurus and a possible introduction of ARAV. de Oliveira et al. (2013), in their study with ecological niche modeling, demonstrated that there is potential for the expansion of N. lasiurus mainly to the South and Southeast regions of the Atlantic Forest ecoregion. Sobral et al. (2023), reinforces the existence of these favorable conditions, indicating that humid areas with resource availability, as observed in coastal Atlantic Forest ecoregion, favor the reproduction of this species and are related to its evolutionary success and its importance as a reservoir. Prist et al. (2021) showed that the risk of HPS transmission is increased in degraded areas of Atlantic Forest ecoregion, which can influence transmission by approximately 45%. The occurrence of degraded areas also affects positively the abundance of N. lasiurus in up to 46%, depending on the level of degradation.

In this context, the findings of the present study on the evolutionary history of this rodent reinforce the importance of systematic monitoring of the hantavirus in Rio de Janeiro state, considering the apparent ongoing expansion of N. lasiurus in this state, and the potential for the introduction of ARAV by individuals dispersing from the Cerrado biome. The present study also provides important insights into the demographic history of N. lasiurus that led to its occurrence in the Atlantic Forest domain of Rio de Janeiro state. These findings can also be valuable for the surveillance of orthohantaviruses by local public health authorities and for the development of effective measures for preventing and controlling this highly lethal zoonosis.

ACKNOWLEDGMENTS

We thank the IOC/FIOCRUZ, the Programa de Pós-Graduação em Biodiversidade e Saúde and the Programa de Pós-Graduação em Biologia Parasitária, Instituto Oswaldo Cruz/FIOCRUZ for supporting this study, and Stephen Ferrari for reviewing the text and correcting the English. We appreciate the reviewers’ contributions, which increase the quality of the work. We are also grateful to the FIOCRUZ technician Jorge Pinto for technical support in the field. We also thank ICMBio for authorizing fieldwork at REBIO Poço das Antas and providing infrastructure at this site, where we were supported by Gustavo Peixoto and Rafael Puglia. The present study was financed by the Instituto Oswaldo Cruz (IOC), Fundação Oswaldo Cruz (FIOCRUZ), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Finance Code 001, through a Ph.D scholarship to Fernando de Oliveira Santos, the Conselho Nacional de Desenvolvimento Científico e Tecnológico (MCTIC/CNPq Universal 439208/2018-1), and the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ “Sediadas” E-26/210.245/2018, APQ1 E-26/210.467/2019, COLBIO E-26/210.309/2021 and CNE E-26/201.223/2022).

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ADDITIONAL NOTES

• ZooBank register

  https://zoobank.org/04D904FC-AA53-4F1F-8A1A-8D3F36B213EF

• How to cite this article

  Santos FO, Moreira JC, Gonçalves PR, Lucio CS, Teixeira BR, D’Andrea PS (2024) Necromys lasiurus (Cricetidae: Sigmodontinae) from open areas of the Atlantic Forest of Rio de Janeiro: Population structure and implications for the monitoring of hantaviruses. Zoologia 41: e23086. https://doi.org/10.1590/S1984-4689.v41.e23086

• Published by

  Sociedade Brasileira de Zoologia at Scientific Electronic Library Online (https://www.scielo.br/zool)

APPENDIX

Appendix 1
Details of the mitochondrial Cytochrome b gene sequences of the specimens used for analyses. Voucher number (field and/or collection numbers); GenBank accession number; and source.

Species	Voucher	State/Locality	Country	GenBank	Source
Necromys lasiurus	LBCE 7752	Rio de Janeiro/Sumidouro	Brazil	PP068236	LABPMR
Necromys lasiurus	LBCE 7764	Rio de Janeiro/Sumidouro	Brazil	PP068235	LABPMR
Necromys lasiurus	LBCE 9994	Rio de Janeiro/Cordeiro	Brazil	PP068234	LABPMR
Necromys lasiurus	LBCE 10756	Rio de Janeiro/Cantagalo	Brazil	PP068233	LABPMR
Necromys lasiurus	NPM1767	Minas Gerais/Estação Ecológica Água Limpa	Brazil	PP068208	NUPEM
Necromys lasiurus	NPM1777	Minas Gerais/Estação Ecológica Água Limpa	Brazil	PP068207	NUPEM
Necromys lasiurus	LBCE 18703	Rio de Janeiro/Rio das Ostras	Brazil	PP068232	LABPMR
Necromys lasiurus	LBCE 18944	Rio de Janeiro/Casimiro de Abreu	Brazil	PP068231	LABPMR
Necromys lasiurus	LBCE 18945	Rio de Janeiro/Casimiro de Abreu	Brazil	PP068230	LABPMR
Necromys lasiurus	LBCE 18946	Rio de Janeiro/Casimiro de Abreu	Brazil	PP068229	LABPMR
Necromys lasiurus	LBCE 18948	Rio de Janeiro/Casimiro de Abreu	Brazil	PP068228	LABPMR
Necromys lasiurus	LBCE 18949	Rio de Janeiro/Casimiro de Abreu	Brazil	PP068227	LABPMR
Necromys lasiurus	LBCE 18950	Rio de Janeiro/Casimiro de Abreu	Brazil	PP068226	LABPMR
Necromys lasiurus	LBCE 19724	Rio de Janeiro/Casimiro de Abreu	Brazil	PP068225	LABPMR
Necromys lasiurus	LBCE 19725	Rio de Janeiro/Casimiro de Abreu	Brazil	PP068224	LABPMR
Necromys lasiurus	LBCE 19726	Rio de Janeiro/Casimiro de Abreu	Brazil	PP068223	LABPMR
Necromys lasiurus	LBCE 19948	Rio de Janeiro/Casimiro de Abreu	Brazil	PP068221	LABPMR
Necromys lasiurus	LBCE 19952	Rio de Janeiro/Silva Jardim	Brazil	PP068220	LABPMR
Necromys lasiurus	LBCE 20204	Rio de Janeiro/Silva Jardim	Brazil	PP068219	LABPMR
Necromys lasiurus	LBCE 20214	Rio de Janeiro/Silva Jardim	Brazil	PP068218	LABPMR
Necromys lasiurus	LBCE 20215	Rio de Janeiro/Silva Jardim	Brazil	PP068217	LABPMR
Necromys lasiurus	LBCE 20216	Rio de Janeiro/Silva Jardim	Brazil	PP068216	LABPMR
Necromys lasiurus	LBCE 20217	Rio de Janeiro/Silva Jardim	Brazil	PP068215	LABPMR
Necromys lasiurus	LBCE 19727	Rio de Janeiro/Silva Jardim	Brazil	PP068222	LABPMR
Necromys lasiurus	NPM556	Rio de Janeiro/ARIE de Itapebussus	Brazil	PP068214	NUPEM
Necromys lasiurus	NPM565	Rio de Janeiro/ARIE de Itapebussus	Brazil	PP068213	NUPEM
Necromys lasiurus	NPM1413	Rio de Janeiro/R101 KM 123 + 800 Pista Sul	Brazil	PP068212	NUPEM
Necromys lasiurus	NPM1613	Rio de Janeiro/Fazenda Santa Rita	Brazil	PP068211	NUPEM
Necromys lasiurus	NPM1620	Rio de Janeiro/Fazenda Santa Rita	Brazil	PP068210	NUPEM
Necromys lasiurus	NPM1647	Rio de Janeiro/Fazenda Santa Rita	Brazil	PP068209	NUPEM
Necromys lasiurus	FC 154	Minas Gerais/Caratinga	Brazil	EF531690	Genbank
Necromys lasiurus	LBCE 8684	Mato Grosso do Sul/Sidrôlandia	Brazil	KP122251.1	Genbank
Necromys lasiurus	CRB 1217	São Paulo/Pedreira	Brazil	MT006399	Genbank
Necromys lasiurus	CRB 1418	São Paulo/Pedreira	Brazil	MT006400.1	Genbank
Necromys lasiurus	LBCE 10544	São Paulo/Ribeirão Grande	Brazil	PP214909	Genbank
Necromys lasiurus	NK 42164	São Paulo/Tupi Paulista	Brazil	EF531663	Genbank
Necromys lasiurus	JR 346	Rio Grande do Sul/Rondinha	Brazil	EF531662.1	Genbank
Necromys lasiurus	CRB 1889	Santa Catarina/Itá	Brazil	MT006403.1	Genbank
Necromys lasiurus	LBCE 23277	Paraná/Lidanópolis	Brazil	PP068237	LABPMR
Necromys lasiurus	LS052III	Minas Gerais/Lagoa Santa	Brazil	EF531688.1	Genbank
Necromys lasiurus	CRB2704	Bahia/Correntina	Brazil	MT006406.1	Genbank
Necromys lasiurus	CRB1603	Bahia/Jaborandi	Brazil	MT006402	Genbank
Necromys lasiurus	CRB1570	Bahia/Jaborandi	Brazil	MT006401.1	Genbank
Necromys lasiurus	CRB1138	Goiás/Alto Paraíso de Goiás	Brazil	MT006398.1	Genbank
Necromys lasiurus	CRB998	Goiás/Cavalcante	Brazil	MT006421.1	Genbank
Necromys lasiurus	CRB997	Goiás/Cavalcante	Brazil	MT006420.1	Genbank
Necromys lasiurus	CRB993	Goiás/Cavalcante	Brazil	MT006419.1	Genbank
Necromys lasiurus	CRB938	Goiás/Cavalcante	Brazil	MT006417.1	Genbank
Necromys lasiurus	CRB909	Goiás/Cavalcante	Brazil	MT006416.1	Genbank
Necromys lasiurus	CRB904	Goiás/Cavalcante	Brazil	MT006415.1	Genbank
Necromys lasiurus	CRB1020	Goiás/Cavalcante	Brazil	MT006397.1	Genbank
Necromys lasiurus	CRB1014	Goiás/Cavalcante	Brazil	MT006396.1	Genbank
Necromys lasiurus	CRB504	Goiás/Corumbá de Goiás	Brazil	MT006408.1	Genbank
Necromys lasiurus	CRB1010	Goiás/Cavalcante	Brazil	MT006395.1	Genbank
Necromys lasiurus	CRB2327	Goiás/Mimoso de Goias	Brazil	MT006405.1	Genbank
Necromys lasiurus	CRB2323	Goiás/Mimoso de Goias	Brazil	MT006404.1	Genbank
Necromys lasiurus	ARB135	Mato Gosso do Sul/Costa Rica	Brazil	MT006393	Genbank
Necromys lasiurus	ARB142	Mato Gosso do Sul/Costa Rica	Brazil	MT006394	Genbank
Necromys lasiurus	ARB133	Mato Gosso do Sul/Costa Rica	Brazil	MT006392	Genbank
Necromys lasiurus	CD21	Bahia/Chapada Diamantina	Brazil	EF531689.1	Genbank
Necromys lasiurus	roe255	Pampa del Indio	Argentina	KF207862.1	Genbank
Necromys lasiurus	roe300	Pampa del Indio	Argentina	KF207857.1	Genbank
Necromys lasiurus	roe278	Pampa del Indio	Argentina	KF207854.1	Genbank
Necromys lasiurus	roe306	Pampa del Indio	Argentina	KF207853.1	Genbank
Necromys lasiurus	roe171	Pampa del Indio	Argentina	KF207845.1	Genbank
Necromys lasiurus	roe252	Pampa del Indio	Argentina	KF207844.1	Genbank
Necromys lasiurus	TK65362	Alto Paraguay	Paraguay	EF531673.1	Genbank
Necromys lasiurus	NK27519	Bella Vista	Paraguay	EF531665.1	Genbank
Necromys lasiurus	NK27506	Bella Vista	Paraguay	EF531664.1	Genbank
Necromys lasiurus	TK63511	Canindeyu	Paraguay	EF531667.1	Genbank
Necromys lasiurus	TK 61813	Canindeyu	Paraguay	EF531666	Genbank
Necromys lasiurus	TK 63980	Canindeyu	Paraguay	EF531668	Genbank
Necromys lasiurus	TK 63982	Canindeyu	Paraguay	EF531669	Genbank
Necromys lasiurus	CNP 535	Concepcion	Paraguay	AY273914	Genbank
Necromys lasiurus	TK 64302	Concepcion	Paraguay	AY273912	Genbank
Necromys lasiurus	TK64268	Concepcion	Paraguay	EF531671.1	Genbank
Necromys lasiurus	TK64242	Concepcion	Paraguay	EF531670.1	Genbank
Necromys lasiurus	UMMZ 134431	Presidente Hayes	Paraguay	U03528	Genbank
Necromys lasiurus	JPJ530	Catamarca	Argentina	EF531661.1	Genbank
Necromys lasiurus	CNP 795	Misiones	Argentina	EF531659	Genbank
Necromys lasiurus	CNP 801	Misiones	Argentina	EF531660	Genbank
Necromys lasiurus	CNP 531	Santa Fé	Argentina	EF531656	Genbank
Necromys lasiurus	CNP532	Santa Fé	Argentina	EF531657.1	Genbank
Necromys lasiurus	CNP 519	Bahia Blanca	Argentina	EF531654	Genbank
Necromys lasiurus	CNP520	Bahia Blanca	Argentina	EF531655.1	Genbank
Necromys lasiurus	CNP 472	Cerro Ventana	Argentina	EF531652	Genbank
Necromys lasiurus	CNP 473	San Mateo	Argentina	EF531653	Genbank
Necromys lasiurus	CNP 534	Misiones	Argentina	EF531658	Genbank
Necromys lasiurus	BM 79.1665	Cerro Ventana	Argentina	EF531651	Genbank
Necromys lasiurus	CRB593	Pará/Arapiranga	Brazil	MT006414.1	Genbank
Necromys lasiurus	CRB592	Pará/Arapiranga	Brazil	MT006413.1	Genbank
Necromys lasiurus	CRB586	Pará/Arapiranga	Brazil	MT006412.1	Genbank
Necromys lasiurus	CRB580	Pará/Arapiranga	Brazil	MT006411.1	Genbank
Necromys lasiurus	CRB579	Pará/Arapiranga	Brazil	MT006410.1	Genbank
Necromys lasiurus	CRB578	Pará/Arapiranga	Brazil	MT006409.1	Genbank
Necromys lasiurus	CRB2820	Mato Grosso/São José do Xingu	Brazil	MT006407.1	Genbank
Necromys lasiurus	FLV140r	Tocantins/Lagoa da Confusão	Brazil	KR190456.1	Genbank
Necromys lasiurus	FLV11r	Tocantins Lagoa da Confusão	Brazil	KR190443.1	Genbank
Necromys obscurus	EV 1028	San José/Estancia El Relincho	Uruguay	EF531682.1	Genbank
Necromys obscurus	GD 754	Montevideo	Uruguay	EF531683.1	Genbank
Necromys obscurus	CNP 891	Aarroyo de las Brusquitas	Argentina	EF531684.1	Genbank
Necromys lactens	CNP 892	Aarroyo de las Brusquitas	Argentina	EF531685.1	Genbank
Necromys lactens	JPJ 419	Catamarca	Argentina	EF531644.1	Genbank
Necromys lactens	JPJ 447	Tucumán	Argentina	EF531645.1	Genbank
Necromys lactens	JPJ 552	Catamarca	Argentina	EF531646.1	Genbank
Necromys lactens	JPJ 630	Jujuy	Argentina	EF531647.1	Genbank
Necromys lactens	JPJ 721	Salta	Argentina	EF531648.1	Genbank
Necromys lactens	JPJ 953	Jujuy	Argentina	EF531649.1	Genbank
Necromys lactens	JPJ1315	Salta	Argentina	EF531650.1	Genbank
Akodon montesis	OMNH 34512	Catamarca	Argentina	EU260470.1	Genbank
Akodon montesis	LMT428	-	-	EF101874.1	Genbank
Akodon montesis	LMT425	Paraná/Piraquara	Brazil	EF101873.1	Genbank
Brucepattersonius soricinus	MN 78954	-	-	KF815439.1	Genbank
Thalpomys lasiotis	isolate 1647	-	-	AY310347	Genbank
Thalpomys lasiotis	isolate 1591	-	-	AY310349	Genbank

Edited by

Editorial responsibility

Guilherme S.T. Garbino

Publication Dates

• Publication in this collection
  07 June 2024
• Date of issue
  2024

History

• Received
  06 Nov 2023
• Accepted
  29 Jan 2024