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Ranaivoson, H. C.

Publications and source records attributed to Ranaivoson, H. C..

8 recordsLinked to original sources

Diversity and seasonality of ectoparasite burden on two species of Madagascar fruit bat, Eidolon dupreanum and Rousettus madagascariensis

BackgroundBats are important reservoir hosts for a variety of microparasites, some of which are transmitted by ectoparasite vectors that include mites, fleas, lice, ticks, and bat flies (families Nycteribiidae and Streblidae). All of these ectoparasite taxa are known to parasitize two endemic fruit bats of Madagascar, Eidolon dupreanum and Rousettus madagascariensis. We aimed to describe the diversity of ectoparasite infestation for both bat species through morphological observation and DNA barcoding and elucidate ecological and climatic correlates of seasonal nycteribiid parasitism of these hosts. MethodsLive E. dupreanum and R. madagascariensis fruit bats were captured monthly in northern and central-eastern Madagascar from 2013-2020. Ectoparasites on all captured bats were counted and identified in the field, then collected into ethanol. Field identification of a subset of samples were confirmed via microscopy and DNA barcoding of the cytochrome C oxidase subunit 1 (COI) and 18S genes. The seasonal abundance of nycteribiid bat flies on both host bats was analyzed using generalized additive models, and the role of climate in driving this seasonality was assessed via cross-correlation analysis combined with generalized linear models. Phylogenetic trees were generated to compare COIand 18S sequences of Madagascar nycteribiid and streblid bat flies with available reference sequences from GenBank. ResultsEctoparasites corresponding to four broad taxa (mites, ticks, fleas, and bat flies) were recovered from 628 of 873 E. dupreanum and 831 of 862 R. madagascariensis. E. dupreanum were most commonly parasitized by Cyclopodia dubia nycteribiids and R. madagascariensis by Eucampsipoda madagascariensis nycteribiids or Megastrebla wenzeli streblids. We observed significant seasonality in nycteribiid abundance on both bat hosts, which varied by bat sex and was positively correlated with lagged temperature, precipitation, and humidity variables. Barcoding sequences recovered for all three bat fly species grouped with previously reported sequences, confirming morphological species identification. Our study contributes the first DNA barcodes of any kind reported for M. wenzeli and the first 18S barcodes for C. dubia. ConclusionThis study explores the diversity and abundance of ectoparasite burdens in two Malagasy fruit bat species, highlighting the importance of seasonal ecology and the influence of climate variables on parasitism, which correlates with resource availability.

ecology↗

Picornaviridae and Caliciviridae diversity in Madagascar fruit bats is driven by cross-continental genetic exchange

Bats are reservoir hosts for numerous well-known zoonotic viruses, but their broader virus-hosting capacities remain understudied. Picornavirales are an order of enteric viruses known to cause disease across a wide range of mammalian hosts, including Hepatitis A in humans and foot-and-mouth disease in ungulates. Host-switching and recombination drive the diversification of Picornavirales worldwide. Divergent Caliciviridae and Picornaviridae (families within the Picornavirales) have been described in bats across mainland Africa, but surveillance for these viruses has been rare in the Southwest Indian Ocean Islands. Bats live in close proximity to and are consumed widely as a food source by humans in Madagascar, providing opportunities for zoonotic transmission. Prior work in Madagascar has described numerous evolutionarily divergent bat viruses, some with zoonotic potential. Using metagenomic Next Generation Sequencing of urine and fecal samples obtained from three species of endemic Malagasy fruit bats (Eidolon dupreanum, Pteropus rufus, and Rousettus madagascariensis), we recovered 13 full-length and 37 partial-length genomic sequences within the order Picornavirales (36 Picornaviridae and 14 Caliciviridae sequences), which we identify and describe here. We find evidence that genetic exchange between mainland African bat and Madagascar bat Picornavirales likely shaped the diversification patterns of these novel sequences through recombination events between closely related Picornavirales; thus far, high host fidelity appears to have limited these viruses from spilling over into other species.

evolutionary biology↗

Genomic characterization of novel bat kobuviruses in Madagascar: implications for viral evolution and zoonotic risk

Kobuviruses (family Picornaviridae, genus Kobuvirus) are enteric viruses that infect a wide range of both human and animal hosts. Much of the evolutionary history of kobuviruses remains elusive, largely due to limited screening in wildlife. Bats have been implicated as major sources of virulent zoonoses, including coronaviruses, henipaviruses, and filoviruses, though much of the bat virome still remains uncharacterized. While most bat virus research has historically focused on immediately recognizable zoonotic clades (e.g. SARS-related coronaviruses), a handful of prior reports catalog kobuvirus infection in bats and posit the role of bats as potential progenitors of downstream kobuvirus evolution. As part of a multi-year study, we carried out metagenomic Next Generation Sequencing (mNGS) on fecal samples obtained from endemic, wild-caught Madagascar fruit bats to characterize potentially zoonotic viruses circulating within these populations. The wild bats of Madagascar represent diverse Asian and African phylogeographic histories, presenting a unique opportunity for viruses from disparate origins to mix, posing significant public health threats. Here, we report detection of kobuvirus RNA in Malagasy fruit bat (Eidolon dupreanum) feces and undertake phylogenetic characterization of one full genome kobuvirus sequence, which nests within the Aichivirus A clade - a kobuvirus clade known to infect a wide range of hosts including humans, rodents, canids, felids, birds, and bats. Given the propensity of kobuviruses for recombination and cross-species infection, further characterization of this clade is critical to accurate evaluation of future zoonotic threats.

evolutionary biology↗

Quantifying the seasonal reproductive cycle in three species of Malagasy fruit bats with implications for pathogen and population dynamics

Bats (order Chiroptera) are hosts for highly virulent zoonotic pathogens. Many bats demonstrate seasonally varying antiviral responses, including antibody responses which have been observed to peak during the nutritionally depleted dry-season and female gestation periods, suggesting some impact of resource deficits on bat virus immunity. Given the frequent overlap in these energetically demanding periods, it is likely that endocrinological changes associated with pregnancy might partially explain the aforementioned pattern in antibody dynamics. Regardless, we know little about the seasonality of reproduction in many fruit bat species, despite the importance of reproductive biology to informing conservation management (e.g. population viability) and disease dynamics. Here, we aimed to elucidate the reproductive biology of three species of endemic fruit bat native to the island of Madagascar: Pteropus rufus, Eidolon dupreanum, and Rousettus madagascarensis. To do so, we leveraged plasma samples collected in part with a longitudinal field study, from 2018 to 2020. We adapted three standard reproductive assays previously validated in humans to quantify seasonal changes in reproductive hormones for bats and applied a mixture model approach to determine hormone cutoffs for pregnancy. As expected, we found that pregnant females showed the highest levels of estradiol and progesterone and adult males the highest levels of testosterone. Additionally, female P. rufus and R. madagascariensis showed clear seasonality in reproduction with peaks in estradiol and progesterone in August and October, respectively. Seasonality was less clearly discernible in the female E. dupreanum and male data. In general, we found that the commercially available assays were successful in quantifying endocrinological hormones for bats; when paired with histological embryo sections or field data, these offer a powerful tool to elucidate bat reproductive calendars.

ecology↗

Detection, characterization, and phylogenetic analysis of a near-whole genome sequence of a novel astrovirus in an endemic Malagasy fruit bat, Rousettus madagascariensis

Bats (order: Chiroptera) are known to host a diverse range of viruses, some of which present a public health risk. Thorough viral surveillance is therefore essential to predict and potentially mitigate zoonotic spillover. Astroviruses (family: Astroviridae) are an understudied group of viruses with a growing amount of indirect evidence for zoonotic transfer. Astroviruses have been detected in bats with significant prevalence and diversity, suggesting that bats may act as important astrovirus hosts. Most astrovirus surveillance in wild bat hosts has, to date, been restricted to single-gene PCR detection and concomitant Sanger sequencing; additionally, many bat species and many geographic regions have not yet been surveyed for astroviruses at all. Here, we use metagenomic Next Generation Sequencing (mNGS) to detect astroviruses in three species of Madagascar fruit bats, Eidolon dupreanum, Pteropus rufus, and Rousettus madagascariensis. We detect numerous partial sequences from all three species and one near-full length astrovirus sequence from Rousettus madagascariensis, which we use to characterize the evolutionary history of astroviruses both within bats and the broader mammalian clade, Mamastrovirus. Taken together, applications of mNGS implicate bats as important astrovirus hosts and demonstrate novel patterns of bat astrovirus evolutionary history, particularly in the Southwest Indian Ocean region.

evolutionary biology↗

Discovery and Genomic Characterization of a Novel Henipavirus, Angavokely virus, from fruit bats in Madagascar

The genus Henipavirus (family Paramyxoviridae) is currently comprised of seven viruses, four of which have demonstrated prior evidence of zoonotic capacity. These include the biosafety level 4 agents Hendra (HeV) and Nipah (NiV) viruses, which circulate naturally in pteropodid fruit bats. Here, we describe and characterize Angavokely virus (AngV), a divergent henipavirus identified in urine samples from wild, Madagascar fruit bats. We report the near-complete 16,740 nt genome of AngV, which encodes the six major henipavirus structural proteins (nucleocapsid, phosphoprotein, matrix, fusion, glycoprotein, and L polymerase). Within the phosphoprotein (P) gene, we identify an alternative start codon encoding the AngV C protein and a putative mRNA editing site where the insertion of one or two guanine residues encodes, respectively, additional V and W proteins. In other paramyxovirus systems, C, V, and W are accessory proteins involved in antagonism of host immune responses during infection. Phylogenetic analysis suggests that AngV is ancestral to all four previously described bat henipaviruses--HeV, NiV, Cedar virus (CedV), and Ghanaian bat virus (GhV)--but evolved more recently than rodent- and shrew-derived henipaviruses, Mojiang (MojV), Gamak (GAKV), and Daeryong (DARV) viruses. Predictive structure-based alignments suggest that AngV is unlikely to bind ephrin receptors, which mediate cell entry for all other known bat henipaviruses. Identification of the AngV receptor is needed to clarify the viruss potential host range. The presence of V and W proteins in the AngV genome suggest that the virus could be pathogenic following zoonotic spillover. ImportanceHenipaviruses include highly pathogenic emerging zoonotic viruses, derived from bat, rodent, and shrew reservoirs. Bat-borne Hendra (HeV) and Nipah (NiV) are the most well-known henipaviruses, for which no effective antivirals or vaccines for humans have been described. Here we report the discovery and characterization of a novel henipavirus, Angavokely virus (AngV), isolated from wild fruit bats in Madagascar. Genomic characterization of AngV reveals all major features associated with pathogenicity in other henipaviruses, suggesting that AngV could be pathogenic following spillover to human hosts. Our work suggests that AngV is an ancestral bat henipavirus which likely uses viral entry pathways distinct from those previously described for HeV and NiV. In Madagascar, bats are consumed as a source of human food, presenting opportunities for cross-species transmission. Characterization of novel henipaviruses and documentation of their pathogenic and zoonotic potential are essential to predicting and preventing the emergence of future zoonoses that cause pandemics.

evolutionary biology↗

Reproduction, seasonal morphology, and juvenile growth in three Malagasy fruit bats

The island nation of Madagascar is home to three endemic species of Old World Fruit Bat in the family Pteropodidae: Pteropus rufus, Eidolon dupreanum, and Rousettus madagascariensis, all three of which are IUCN Red Listed under some category of threat. To inform conservation efforts to model population viability for these threatened species, as well understand the mechanisms underpinning persistence of several potentially zoonotic pathogens hosted by these bats, we here define the seasonal limits of a staggered annual birth pulse across the three species. Our field studies in central-eastern Madagascar indicate that this annual birth pulse takes place in September/October for P. rufus, November for E. dupreanum, and December for R. madagascariensis. Juvenile development periods vary across the three Malagasy pteropodids, resulting in near-synchronous weaning of pups for all species in late January-February at the height of the fruiting season for Madagascar, a pattern characteristic of most mammalian frugivores on the island. We here document the size range in morphological traits for the three Malagasy fruit bat species; these traits span the range of those known for pteropodids more broadly, with P. rufus and E. dupreanum among the larger of recorded species and R. madagascariensis among the smaller. All three species demonstrate subtle sexual dimorphism in observed traits with larger-bodied males vs. females. We explore seasonal variation in adult body condition by comparing observed body mass with body mass predicted by forearm length, demonstrating that pregnant females add weight during staggered gestation periods and males lose weight during the nutritionally-deficit Malagasy winter. Finally, we quantify forearm, tibia, and ear length growth rates in juvenile bats, demonstrating both faster growth and more protracted development times for the largest P. rufus species. The longer development period for the already-threatened P. rufus further jeopardizes this species conservation status as human hunting of bats for subsistence is particularly detrimental to population viability during reproductive periods. The more extreme seasonal variation in the mass to forearm relationship for P. rufus may also modulate immune function, an important consideration given these bats roles as reservoir hosts for several high profile viral families known to cause severe disease in humans. Our work highlights the importance of longitudinal field studies in collecting critical data for mammalian conservation efforts and human public health alike.

ecology↗

Full genome Nobecovirus sequences from Malagasy fruit bats define a unique evolutionary history for this coronavirus clade

Bats are natural reservoirs for both Alpha- and Betacoronaviruses and the hypothesized original hosts of five of seven known zoonotic coronaviruses. To date, the vast majority of bat coronavirus research has been concentrated in Asia, though coronaviruses are globally distributed; indeed, SARS-CoV and SARS-CoV-2-related Betacoronaviruses in the subgenus Sarbecovirus have been identified circulating in Rhinolophid bats in both Africa and Europe, despite the relative dearth of surveillance in these regions. As part of a long-term study examining the dynamics of potentially zoonotic viruses in three species of endemic Madagascar fruit bat (Pteropus rufus, Eidolon dupreanum, Rousettus madagascariensis), we carried out metagenomic Next Generation Sequencing (mNGS) on urine, throat, and fecal samples obtained from wild-caught individuals. We report detection of RNA derived from Betacoronavirus subgenus Nobecovirus in fecal samples from all three species and describe full genome sequences of novel Nobecoviruses in P. rufus and R. madagascariensis. Phylogenetic analysis indicates the existence of five distinct Nobecovirus clades, one of which is defined by the highly divergent sequence reported here from P. rufus bats. Madagascar Nobecoviruses derived from P. rufus and R. madagascariensis demonstrate, respectively, Asian and African phylogeographic origins, mirroring those of their fruit bat hosts. Bootscan recombination analysis indicates significant selection has taken place in the spike, nucleocapsid, and NS7 accessory protein regions of the genome for viruses derived from both bat hosts. Madagascar offers a unique phylogeographic nexus of bats and viruses with both Asian and African phylogeographic origins, providing opportunities for unprecedented mixing of viral groups and, potentially, recombination. As fruit bats are handled and consumed widely across Madagascar for subsistence, understanding the landscape of potentially zoonotic coronavirus circulation is essential for mitigation of future zoonotic threats.

evolutionary biology↗