Abstract Scientific specimens of rabbits (Lagomorpha, Leporidae) have been reported for Venezuela and Suriname, but not for neighboring Guyana. Over the past few decades, people traversing Guyana’s Deep South Rupununi have anecdotally reported sightings of rabbits, particularly along the road to the Marudi mining site; however physical documentation by camera trap images were not obtained until 2019. The goal of this study was to confirm species identification of rabbits found in Guyana and provide information on distribution, ecology, and conservation. An international team of scientists, community conservation organizations (South Rupununi Conservation Society and Rupununi Wildlife Research Unit), and community members identified the species as the Suriname tapeti ( Sylvilagus parentum ). Described in 2017, S. parentum was known only from the forests of western Suriname. Four adult rabbits were captured on small stakeholder farms located within primary forest in the Rupununi and prepared as museum vouchers with an additional 18 occurrences by camera traps. Camera traps and indigenous knowledge were used to describe the species’ distribution, ecology, and conservation status. Confirmation of S. parentum in Guyana’s South Rupununi adds another taxonomic order (Lagomorpha) to the country’s mammal list and highlights the value of combined scientific and indigenous approaches for understanding biodiversity.
Natural history museum collections are valuable but underutilized resources for viral discovery, offering opportunities to test hypotheses about viral occurrence across space, time, and taxonomic groups. We developed machine learning models of bat host suitability to guide coronavirus and paramyxovirus screening of 1330 and 491 tissues, respectively, in a museum collection. For the first time, we recovered coronavirus ( n = 16) and paramyxovirus ( n = 3) sequences from archived museum tissues, confirming three novel coronavirus host species and three novel paramyxovirus host species (3% and 33% prediction success rate, respectively). These sequences included a SARS-like coronavirus and an orthoparamyxovirus from Angolan Rhinolophus fumigatus specimens collected in June 2019, suggesting that viruses with epidemic potential may be more widespread in sub-Saharan Africa than previously believed. Our study demonstrates the value of combining predictive modeling and collections-based viral discovery, particularly for filling outstanding sampling gaps and investigating changes in host–virus associations over time. ### Competing Interest Statement The authors have declared no competing interest. NSF, DBI 2515340, CAREER Grant 2238801, NSF DBI 2515340 Gates Foundation, https://ror.org/0456r8d26, OPP1144 American Society of Mammalogists, https://ror.org/058rchw45, James L. Patton Award Field Museum of Natural History, https://ror.org/00mh9zx15, Field Museum Science Innovation Award Negaunee Seed Fund Grant Cambridge Centre for Data-Driven Discovery and Accelerate Programme for Scientific Discovery National Geographic Society, Explorer Grant (NGS-73084R-20) IIE Rodman Rockefeller Centennial Fellowship Edward Mallinckrodt, Jr. Foundation
Wildlife tagging provides critical insights into animal movement ecology, physiology, and behavior amid global ecosystem changes. However, the stress induced by capture, handling, and tagging can impact post-release locomotion and activity and, consequently, the interpretation of study results. Here, we analyze post-tagging effects on 1585 individuals of 42 terrestrial mammal species using collar-collected GPS and accelerometer data. Species-specific displacements and overall dynamic body acceleration, as a proxy for activity, were assessed over 20days post-release to quantify disturbance intensity, recovery duration, and speed. Differences were evaluated, considering species-specific traits and the human footprint of the study region. Over 70% of the analyzed species exhibited significant behavioral changes following collaring events. Herbivores traveled farther with variable activity reactions, while omnivores and carnivores were initially less active and mobile. Recovery duration proved brief, with alterations diminishing within 4-7 tracking days for most species. Herbivores, particularly males, showed quicker displacement recovery (4 days) but slower activity recovery (7 days). Individuals in high human footprint areas displayed faster recovery, indicating adaptation to human disturbance. Our findings emphasize the necessity of extending tracking periods beyond 1 week and particular caution in remote study areas or herbivore-focused research, specifically in smaller mammals.
Roughly a third of all horseshoe bat species (Rhinolophidae: Rhinolophus) are found in Africa, where a recent continent-wide genetic survey suggested the presence of both undescribed and apparently invalid species. Here, we focus on the R. landeri species complex and the recent elevation of R. lobatus Peters, 1852, to species rank. That action created ambiguity in the taxonomy of East African members of the group—are both R. landeri Martin, 1838, and R. lobatus sympatric in East Africa or is another, unnamed species present there? Here, we refine genetic, morphological, and behavioral characterizations of R. landeri and its erstwhile synonyms with samples from the vicinity of their type localities. The distribution of R. landeri appears to be limited to Central and West Africa; existing genetic records attributed to this species from Mali clearly represent another taxon. We marshal genetic evidence for the species-level distinction of R. dobsoni Thomas, 1904, from Sudan, which was previously considered a synonym of R. landeri. We reject R. axillaris J. A. Allen, 1917, as a synonym of the R. landeri complex, provisionally regarding it as a valid member of the landeri species group. Finally, we demonstrate that East Africa is home to a fourth species of the landeri complex that is named herein. Final resolution of the systematics of this species complex awaits expanded characterizations (especially of genetics, vocalizations, and noseleaves) and studies of variation in regions of contact.
More than 60 zoonoses are linked to small mammals, including some of the most devastating pathogens in human history. Millions of museum-archived tissues are available to understand natural history of those pathogens. Our goal was to maximize the value of museum collections for pathogen-based research by using targeted sequence capture. We generated a probe panel that includes 39,916 80-bp RNA probes targeting 32 pathogen groups, including bacteria, helminths, fungi, and protozoans. Laboratory-generated, mock-control samples showed that we are capable of enriching targeted loci from pathogen DNA 2,882‒6,746-fold. We identified bacterial species in museum-archived samples, including Bartonella, a known human zoonosis. These results showed that probe-based enrichment of pathogens is a highly customizable and efficient method for identifying pathogens from museum-archived tissues.
Four species of spotted skunks (Carnivora, Mephitidae, Spilogale) are currently recognized: Spilogale angustifrons, S. gracilis, S. putorius, and S. pygmaea. Understanding species boundaries within this group is critical for effective conservation given that regional populations or subspecies (e.g., S. p. interrupta) have experienced significant population declines. Further, there may be currently unrecognized diversity within this genus as some taxa (e.g., S. angustifrons) and geographic regions (e.g., Central America) never have been assessed using DNA sequence data. We analyzed species limits and diversification patterns in spotted skunks using multilocus nuclear (ultraconserved elements) and mitochondrial (whole mitogenomes and single gene analysis) data sets from broad geographic sampling representing all currently recognized species and subspecies. We found a high degree of genetic divergence among Spilogale that reflects seven distinct species and eight unique mitochondrial lineages. Initial divergence between S. pygmaea and all other Spilogale occurred in the Early Pliocene (~ 5.0 million years ago). Subsequent diversification of the remaining Spilogale into an "eastern" and a "western" lineage occurred during the Early Pleistocene (~1.5 million years ago). These two lineages experienced temporally coincident patterns of diversification at ~0.66 and ~0.35 million years ago into two and ultimately three distinct evolutionary units, respectively. Diversification was confined almost entirely within the Pleistocene during a timeframe characterized by alternating glacial-interglacial cycles, with the origin of this diversity occurring in northeastern Mexico and the southwestern United States of America. Mitochondrial-nuclear discordance was recovered across three lineages in geographic regions consistent with secondary contact, including a distinct mitochondrial lineage confined to the Sonoran Desert. Our results have direct consequences for conservation of threatened populations, or species, as well as for our understanding of the evolution of delayed implantation in this enigmatic group of small carnivores.
Patterns of rarity, endemism, and vulnerability are known for four species of yellow-eared bats of the genus Vampyressa: V. melissa, V. voragine, V. elisabethae, and V. sinchi, the last two described based on skull and external morphology. We extracted DNA from the holotypes of V. elisabethae and V. sinchi using strict ancient DNA protocols and sequenced the complete cytochrome-b gene of the mtDNA to investigate the phylogenetic relationships within the genus and employed species-delimitation tests to evaluate the validity of all the currently named species of Vampyressa. The resulting tree topology and our species-delimitation analyses corroborate the validity of V. elisabethae and V. voragine, but places V. sinchi in V. melissa. Based on these results and phenotypic variation, we recognize five valid species in Vampyressa and treat sinchi as a subspecies of a polytypic V. melissa; for which we provide a rediagnosis. Our results show that V. elisabethae is as highly divergent genetically as it is morphologically, and suggest that V. thyone, one of the two species of Vampyressa known to have wide distributions, is a species complex requiring further investigation.
Most of the Earth’s biodiversity is concentrated in the tropics. While the ultimate causes of this geographic pattern remain to be established, ongoing anthropogenic impacts in the tropical belt lead to rapid losses of species diversity. Ancient DNA approaches may help in deciphering temporal patterns in the diversification of tropical biota and could potentially provide historical baseline data on the diversity and distribution of species in anthropogenically modified landscapes. However, studies of sedimentary ancient DNA (sedaDNA) are thus far extremely rare in tropical settings and consequently its value as a conservation tool for tropical ecosystems remains to be tested systematically. To address this issue we present meta-genomic records of shot-gun sequenced sedimentary ancient DNA (sedaDNA) from several sediment cores from the equatorial Bwindi-Impenetrable Forest in Uganda. Because Bwindi is one the most diverse rainforests in Africa and its biota is well documented (including endangered species such Mountain Gorilla and Chimpanzee) it is well suited for a baseline study. We describe the taxonomic composition of sedaDNA from Bwindi for the past 2200 years at an average resolution of 50 years – one of the first comprehensive sedaDNA records of plant and animal taxa from a tropical rainforest. We specifically address the following questions: 1) How precisely can the taxonomic level of shotgun-sequenced tropical sediments be resolved at present? 2) What is the effect of temperature, acidity, nutrient availability, elemental and lithological sediment composition, and burial age on the degradation of DNA? Taxonomic assignments are based on three metagenomic classifiers and four reference databases and their reliability tested against local pollen and modern animal occurrence data. We find that 92.3% of our metagenomic data is taxonomically not identifiable due to the substantial underrepresentation of tropical taxa in genomic reference databases. Yet at ordinal level we reconstruct typical afrotropical assemblages, which do not decline in diversity over time. Our comprehensive set of ecological and sedimentological parameters including sediment age, surface water chemistry, pH, soil temperature, sediment density, sediment water and organic matter content, XRF elemental chemistry, nutrient concentrations, and magnetic susceptibility reveals that DNA degradation cannot be explained by any sedimentary parameter alone, is at Bwindi independent of sediment type, and most likely primarily driven by burial age, suggesting that DNA taphonomic models need to be site-specific in tropical environments. The viability of sedaDNA as a conservation-biology tool requires comprehensive genomic surveys of tropical biota to drastically improve the taxonomic representativeness of DNA reference databases.
Sedimentary ancient DNA has been proposed as a key methodology for reconstructing biodiversity over time. Yet, despite the concentration of Earth's biodiversity in the tropics, this method has rarely been applied in this region. Moreover, the taphonomy of sedimentary DNA, especially in tropical environments, is poorly understood. This study elucidates challenges and opportunities of sedimentary ancient DNA approaches for reconstructing tropical biodiversity. We present shotgun-sequenced metagenomic profiles and DNA degradation patterns from multiple sediment cores from Mubwindi Swamp, located in Bwindi Impenetrable Forest (Uganda), one of the most diverse forests in Africa. We describe the taxonomic composition of the sediments covering the past 2200 years and compare the sedimentary DNA data with a comprehensive set of environmental and sedimentological parameters to unravel the conditions of DNA degradation. Consistent with the preservation of authentic ancient DNA in tropical swamp sediments, DNA concentration and mean fragment length declined exponentially with age and depth, while terminal deamination increased with age. DNA preservation patterns cannot be explained by any environmental parameter alone, but age seems to be the primary driver of DNA degradation in the swamp. Besides degradation, the presence of living microbial communities in the sediment also affects DNA quantity. Critically, 92.3% of our metagenomic data of a total 81.8 million unique, merged reads cannot be taxonomically identified due to the absence of genomic references in public databases. Of the remaining 7.7%, most of the data (93.0%) derive from Bacteria and Archaea, whereas only 0-5.8% are from Metazoa and 0-6.9% from Viridiplantae, in part due to unbalanced taxa representation in the reference data. The plant DNA record at ordinal level agrees well with local pollen data but resolves less diversity. Our animal DNA record reveals the presence of 41 native taxa (16 orders) including Afrotheria, Carnivora, and Ruminantia at Bwindi during the past 2200 years. Overall, we observe no decline in taxonomic richness with increasing age suggesting that several-thousand-year-old information on past biodiversity can be retrieved from tropical sediments. However, comprehensive genomic surveys of tropical biota need prioritization for sedimentary DNA to be a viable methodology for future tropical biodiversity studies.
The molecular phylogeny of extant genets (Carnivora, Viverridae, Genetta) was generated using all species with the exception of the Ethiopian genet Genetta abyssinica. Herein, we provide the first molecular phylogenetic assessment of G. abyssinica using molecular sequence data from multiple mitochondrial genes generated from a recent record of this species from the Foret du Day (the Day Forest) in Djibouti. This record represents the first verified museum specimen of G. abyssinica collected in over 60 years and the first specimen with a specific locality for the country of Djibouti. Multiple phylogenetic analyses revealed conflicting results as to the exact relationship of G. abyssinica to other Genetta species, providing statistical support for a sister relationship to all other extant genets for only a subset of mitochondrial analyses. Despite the inclusion of this species for the first time, phylogenetic relationships among Genetta species remain unclear, with limited nodal support for many species. In addition to providing an alternative hypothesis of the phylogenetic relationships among extant genets, this recent record provides the first complete skeleton of this species to our knowledge and helps to shed light on the distribution and habitat use of this understudied African small carnivore.
We assessed the genetic variability of the eastern spotted skunk (Spilogale putorius) throughout the range of the species, with an emphasis on the potentially endangered plains spotted skunk subspecies (S. p. interrupta). Tissue samples from a variety of sources including field surveys, state agencies, and museum tissue collections allowed a detailed assessment of the genetic variability in S. putorius using both microsatellite markers and cytochrome b (Cytb) gene sequences. Our analysis of 118 specimens established that genetic patterns were consistent with the currently accepted taxonomy of the 3 recognized subspecies: S. p. putorius, S. p. ambarvalis, and S. p. interrupta. The differentiation between S. p. putorius and S. p. ambarvalis was less pronounced (F-ST = 0.178; Cytb sequence divergence = 1.2%) than between these subspecies and the plains spotted skunk (average F-ST = 0.278; Cytb sequence divergence = 2.9%). Overall, genetic variability in the plains spotted skunk was lower than that seen in common carnivores (e.g., striped skunks, Mephitis mephitis, and raccoons, Procyon lotor), but slightly higher than in the endangered black-footed ferret (Mustela nigripes). The heterozygosity levels more closely resemble those found within the island spotted skunk (S. gracilis amphiala) from the Channel Islands of California and other vertebrates that have a "threatened" conservation status.
Taxonomy is a scientific discipline that has provided the universal naming and classification system of biodiversity for centuries and continues effectively to accommodate new knowledge. A recent publication by Garnett and Christidis [1] expressed concerns regarding the difficulty that taxonomic changes represent for conservation efforts and proposed the establishment of a system to govern taxonomic changes. Their proposal to “restrict the freedom of taxonomic action” through governing subcommittees that would “review taxonomic papers for compliance” and their assertion that “the scientific community’s failure to govern taxonomy threatens the effectiveness of global efforts to halt biodiversity loss, damages the credibility of science, and is expensive to society” are flawed in many respects. They also assert that the lack of governance of taxonomy damages conservation efforts, harms the credibility of science, and is costly to society. Despite its fairly recent release, Garnett and Christidis' proposition has already been rejected by a number of colleagues [2,3,4,5,6,7,8]. Herein, we contribute to the conversation between taxonomists and conservation biologists aiming to clarify some misunderstandings and issues in the proposition by Garnett and Christidis.
High-throughput sequencing methods have facilitated obtaining large amounts of data from degraded DNA, thus resulting in a dramatic increase in destructive sampling requests to museums. Because the tissues taken from museum specimens as sources of DNA are destroyed during analysis, consideration of the costs and benefits of loss of valuable specimen material relative to knowledge gained is required for any project utilizing destructive sampling. Variation exists in the preservation of DNA in historical specimens due to specimen age and type of museum preparation, among other factors. Thus, it is important to assess DNA yield and quality from different sources of museum specimens when considering the needs of a particular molecular project. We compared DNA derived from several common sources of museum specimens including bone, claw, skin, and soft tissue adherent to skeletal preparations. To account for differences in preparation type and therefore specimen preservation, we tested the performance of samples representing 3 taxonomic groups: mephitids, rodents, and marsupials. We also compared yields from 2 commonly used DNA extraction techniques. DNA quality was assessed by comparing average fragment size, concentration, and copy number of template DNA (for mitochondrial and nuclear markers) in genomic DNA extracts, as well as mitochondrial genome sequence coverage resulting from shotgun sequencing. We show that DNA quality derived from historic museum samples differs depending on specimen and sample type; however, all samples yielded high mitochondrial copy number except the skin and nail from the tanned specimen. Overall, claw samples produced the greatest number of high-quality sequencing reads with the least amount of bacterial contamination. We also found that high DNA concentrations did not necessarily result in high percentages of on-target reads; in fact, the samples that yielded the highest DNA quantities also had the highest amount of exogenous bacterial DNA. Our results indicate that most historical tissue types can be suitable for next-generation sequencing approaches, therefore providing multiple options for natural history collection staff and researchers when considering destructive sampling requests.
The taxonomy of American deer has been established almost entirely on the basis of morphological data and without the use of explicit phylogenetic methods; hence, phylogenetic analyses including data for all of the currently recognized species, even if based on a single gene, might improve current understanding of their taxonomy. We tested the monophyly of the morphology-defined genera and species of New World deer (Odocoileini) with phylogenetic analyses of mitochondrial DNA sequences. This is the first such test conducted using extensive geographic and taxonomic sampling. Our results do not support the monophyly of Mazama, Odocoileus, Pudu, M. americana, M. nemorivaga, Od. hemionus, and Od. virginianus. Mazama contains species that belong to other genera. We found a novel sister-taxon relationship between "Mazama" pandora and a clade formed by Od. hemionus columbianus and Od. h. sitkensis, and transfer pandora to Odocoileus. The clade formed by Od. h. columbianus and Od. h. sitkensis may represent a valid species, whereas the remaining subspecies of Od. hemionus appear closer to Od. virginianus. Pudu (Pudu) puda was not found sister to Pudu (Pudella) mephistophiles. If confirmed, this result will prompt the recognition of the monotypic Pudella as a distinct genus. We provide evidence for the existence of an undescribed species now confused with Mazama americana, and identify other instances of cryptic, taxonomically unrecognized species-level diversity among populations here regarded as Mazama temama, "Mazama" nemorivaga, and Hippocamelus antisensis. Noteworthy records that substantially extend the known distributions of M. temama and "M." gouazoubira are provided, and we unveil a surprising ambiguity regarding the distribution of "M." nemorivaga, as it is described in the literature. The study of deer of the tribe Odocoileini has been hampered by the paucity of information regarding voucher specimens and the provenance of sequences deposited in GenBank. We pinpoint priorities for future systematic research on the tribe Odocoileini.
Robert C. Dowler, Department of Biology at Angelo State University is the corresponding author, robert dot dowler at angelo dot edu
AbstractWe analyzed phylogeographic patterns in the western spotted skunk, Spilogale gracilis Merriam, 1890 (Carnivora: Mephitidae) in relation to historical events associated with Pre‐Pleistocene Divergence (PPD) and Quaternary climate change (QCC) using mitochondrial DNA from 97 individuals distributed across Western North America. Divergence times were generated using BEAST to estimate when isolation in putative refugia occurred. Patterns and timing of demographic expansion was performed using Bayesian skyline plot. Putative climatic refugia resulting from Quaternary climate change were identified using paleoecological niche modeling and divergence dates compared to major vicariant events associated with Pre‐Pleistocene conditions. We recovered three major mitochondrial clades corresponding to western North America (California, Baja, and across the Great Basin), east‐central North America (Texas, central Mexico, New Mexico), and southwestern Arizona/northwestern Mexico. Time to most recent common ancestor for S. gracilis occurred ~1.36 Ma. Divergence times for each major clade occurred between 0.25 and 0.12 Ma, with signature of population expansion occurring 0.15 and 0.10 Ma. Ecological niche models identified three potential climatic refugia during the Last Interglacial, (1) west coast of California and Oregon, (2) northwestern Mexico, and (3) southern Texas/northeastern Mexico as well as two refugia during the Last Glacial Maximum, (1) western USA and (2) southern Texas/northeastern Mexico. This study supports PPD in shaping species‐level diversity compared to QCC‐driven changes at the intraspecific level for Spilogale, similar to the patterns reported for other small mammals (e.g., rodents and bats). Phylogeographic patterns also appear to have been shaped by both habitat and river vicariance, especially across the desert southwest. Further, continuing climate change during the Holocene coupled with anthropogenic modifications during the Anthropocene appears to be removing both of these barriers to current dispersal of western spotted skunks.