An official website of the United States government
Few studies have addressed viral diversity in lemurs despite their unique evolutionary history on the island of Madagascar and high risk of extinction. Further, while a large number of studies on animal viromes focus on fecal samples, understanding viral diversity across multiple sample types and seasons can reveal complex viral community structures within and across species. Groups of captive lemurs at the Duke Lemur Center (Durham, NC, USA), a conservation and research center, provide an opportunity to build foundational knowledge on lemur-associated viromes. We sampled individuals from seven lemur species, i.e., collared lemur (Eulemur collaris), crowned lemur (Eulemur coronatus), blue-eyed black lemur (Eulemur flavifrons), ring-tailed lemur (Lemur catta), Coquerel’s sifaka (Propithecus coquereli), black-and-white ruffed lemur (Varecia variegata variegata), and red ruffed lemur (Varecia rubra), across two lemur families (Lemuridae, Indriidae). Fecal, blood, and saliva samples were collected from Coquerel’s sifaka and black-and-white ruffed lemur individuals across two sampling seasons to diversify virome biogeography and temporal sampling. Using viral metagenomic workflows, the complete genomes of anelloviruses (n = 4), cressdnaviruses (n = 47), caudoviruses (n = 15), inoviruses (n = 34), and microviruses (n = 537) were determined from lemur blood, feces, and saliva. Many virus genomes, especially bacteriophages, identified in this study were present across multiple lemur species. Overall, the work presented here uses a viral metagenomics approach to investigate viral communities inhabiting the blood, oral cavity, and feces of healthy captive lemurs.
more »
« less
Interspecies Papillomavirus Type Infection and a Novel Papillomavirus Type in Red Ruffed Lemurs (Varecia rubra)
The Papillomaviridae are a family of vertebrate-infecting viruses of oncogenic potential generally thought to be host species- and tissue-specific. Despite their phylogenetic relatedness to humans, there is a scarcity of data on papillomaviruses (PVs) in speciose non-human primate lineages, particularly the lemuriform primates. Varecia variegata (black-and-white ruffed lemurs) and Varecia rubra (red ruffed lemurs), two closely related species comprising the Varecia genus, are critically endangered with large global captive populations. Varecia variegata papillomavirus (VavPV) types −1 and −2, the first PVs in lemurs with a fully identified genome, were previously characterized from captive V. variegata saliva. To build upon this discovery, saliva samples were collected from captive V. rubra with the following aims: (1) to identify PVs shared between V. variegata and V. rubra and (2) to characterize novel PVs in V. rubra to better understand PV diversity in the lemuriform primates. Three complete PV genomes were determined from V. rubra samples. Two of these PV genomes share 98% L1 nucleotide identity with VavPV2, denoting interspecies infection of V. rubra by VavPV2. This work represents the first reported case of interspecies PV infection amongst the strepsirrhine primates. The third PV genome shares <68% L1 nucleotide identity with that of all PVs. Thus, it represents a new PV species and has been named Varecia rubra papillomavirus 1 (VarPV1). VavPV1, VavPV2, and VarPV1 form a new clade within the Papillomaviridae family, likely representing a novel genus. Future work diversifying sample collection (i.e., lemur host species from multiple genera, sample type, geographic location, and wild populations) is likely to uncover a world of diverse lemur PVs.
more »
« less
- Award ID(s):
- 2314898
- PAR ID:
- 10529585
- Publisher / Repository:
- Viruses
- Date Published:
- Journal Name:
- Viruses
- Volume:
- 16
- Issue:
- 1
- ISSN:
- 1999-4915
- Page Range / eLocation ID:
- 37
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Measuring energy balance and energy metabolism can provide crucial information for understanding the ecological and behavioral drivers of an animal's energetic and physiological condition. Both urinary C‐peptide (uCP) of insulin and urinary total triiodothyronine (uTT3) have been validated as noninvasive biomarkers of energy balance and metabolic activity in haplorrhine primates. This study attempts to validate uCP and uTT3 measures in strepsirrhines, a phylogenetically distinct primate clade, using the ruffed lemur (genusVarecia) as a model. We experimentally manipulated the diet of captive black‐and‐white (Varecia variegata) and red (Varecia rubra) ruffed lemurs at Duke Lemur Center across a 4‐week period. We collected urine samples from subjects (n = 5) each day during 1 week of control diet, 2 weeks of calorie‐restricted diet and 1 week of refeeding, designed to temporarily reduce energy balance and metabolism. We also tested the outcome of filter paper as a storage method by comparing to controls (frozen at −20°C) to assess its suitability for studies of wild populations. We successfully measured uCP and uTT3 levels in frozen urine samples using commercial enzyme immunoassay kits and found that both biomarkers were excreted at lower concentrations (C‐peptide: 1.35 ng/mL, 54% reduction; TT3: 1.5 ng/mL, 37.5% reduction) during calorie‐restricted periods compared to normal diet periods. Filter paper recovery for uCP was 19%, though values were significantly positively correlated with frozen control samples. uTT3 could not be recovered at measurable concentrations using filter paper. These methods enable noninvasive measurement of energetic conditions in wild strepsirrhines and subsequent assessment of relationships between energy balance and numerous socioecological drivers in primate populations.more » « less
-
Dispersal is a fundamental aspect of primates’ lives and influences both population and community structuring, as well as species evolution. Primates disperse within an environmental context, where both local and intervening environmental factors affect all phases of dispersal. To date, research has primarily focused on how the intervening landscape influences primate dispersal, with few assessing the effects of local habitat characteristics. Here, we use a landscape genetics approach to examine between- and within-site environmental drivers of short-range black-and-white ruffed lemur (Varecia variegata) dispersal in the Ranomafana region of southeastern Madagascar. We identified the most influential drivers of short-range ruffed lemur dispersal as being between-site terrain ruggedness and canopy height, more so than any within-site habitat characteristic evaluated. Our results suggest that ruffed lemurs disperse through the least rugged terrain that enables them to remain within their preferred tall-canopied forest habitat. Furthermore, we noted a scale-dependent environmental effect when comparing our results to earlier landscape characteristics identified as driving long-range ruffed lemur dispersal. We found that forest structure drives short-range dispersal events, whereas forest presence facilitates long-range dispersal and multigenerational gene flow. Together, our findings highlight the importance of retaining high-quality forests and forest continuity to facilitate dispersal and maintain functional connectivity in ruffed lemurs.more » « less
-
Abstract In 1974, Sue Herring described the relationship between two important performance variables in the feeding system, bite force and gape. These variables are inversely related, such that, without specific muscular adaptations, most animals cannot produce high bite forces at large gapes for a given sized muscle. Despite the importance of these variables for feeding biomechanics and functional ecology, the paucity of in vivo bite force data in primates has led to bite forces largely being estimated through ex vivo methods. Here, we quantify and compare in vivo bite forces and gapes with output from simulated musculoskeletal models in two craniofacially distinct strepsirrhines:Eulemur, which has a shorter jaw and slower chewing cycle durations relative to jaw length and body mass compared toVarecia. Bite forces were collected across a range of linear gapes from 16 adult lemurs (suborder Strepsirrhini) at the Duke Lemur Center in Durham, North Carolina representing three species:Eulemur flavifrons(n = 6; 3F, 3M),Varecia variegata(n = 5; 3F, 2M), andVarecia rubra(n = 5; 5F). Maximum linear and angular gapes were significantly higher forVareciacompared toEulemur(p = .01) but there were no significant differences in recorded maximum in vivo bite forces (p = .88). Simulated muscle models using architectural data for these taxa suggest this approach is an accurate method of estimating bite force‐gape tradeoffs in addition to variables such as fiber length, fiber operating range, and gapes associated with maximum force. Our in vivo and modeling data suggestVareciahas reduced bite force capacities in favor of absolutely wider gapes compared toEulemurin relation to their longer jaws. Importantly, our comparisons validate the simulated muscle approach for estimating bite force as a function of gape in extant and fossil primates.more » « less
-
Schwitzer, Christoph; Clark, Fay; Fichtel, Claudia; Ganzhorn, Jörg U; King, Tony; Mass, Vanessa; Rasoloarison, Rodin M; Ratsimbazafy, Jonah H; Volampeno, Sylviane N; Yoder, Anne D (Ed.)Black-and-white ruffed lemurs (Varecia variegata) are often described as highly sensitive to habitat disturbance (White et al., 1995; Balko, 1998; Ratsimbazafy, 2002; Ratsimbazafy, 2006; Herrera et al., 2011). In fact, local habitat quality has been shown to be a major predictor of Varecia occupancy across the species’ range (Morelli et al., 2020). In Ranomafana National Park, Varecia occupy several structurally and compositionally distinct sites. Disturbed sites—those previously subject to logging—have lower densities of shorter trees with smaller canopies and lower cover, as well as lower floristic diversity than undisturbed sites (Balko, 1998; Mancini, 2023). Resultantly, sites of lower quality habitat, particularly those with fewer large fruiting trees available, have lower population numbers of Varecia, with highly disturbed sites completely absent of this taxon (e.g., Herrera et al., 2011). However, our recent observations of Varecia in a disturbed forest site in Ranomafana National Park suggests the latter is not always the case.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/v16010037
