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1.
Proc Biol Sci ; 291(2014): 20230921, 2024 Jan 10.
Article in English | MEDLINE | ID: mdl-38196370

ABSTRACT

Large carnivores (order Carnivora) are among the world's most threatened mammals due to a confluence of ecological and social forces that have unfolded over centuries. Combining specimens from natural history collections with documents from archival records, we reconstructed the factors surrounding the extinction of the California grizzly bear (Ursus arctos californicus), a once-abundant brown bear subspecies last seen in 1924. Historical documents portrayed California grizzlies as massive hypercarnivores that endangered public safety. Yet, morphological measurements on skulls and teeth generate smaller body size estimates in alignment with extant North American grizzly populations (approx. 200 kg). Stable isotope analysis (δ13C, δ15N) of pelts and bones (n = 57) revealed that grizzlies derived less than 10% of their nutrition from terrestrial animal sources and were therefore largely herbivorous for millennia prior to the first European arrival in this region in 1542. Later colonial land uses, beginning in 1769 with the Mission era, led grizzlies to moderately increase animal protein consumption (up to 26% of diet), but grizzlies still consumed far less livestock than otherwise claimed by contemporary accounts. We show how human activities can provoke short-term behavioural shifts, such as heightened levels of carnivory, that in turn can lead to exaggerated predation narratives and incentivize persecution, triggering rapid loss of an otherwise widespread and ecologically flexible animal.


Subject(s)
Ursidae , Animals , Humans , Body Size , California , Carnivory , Herbivory
2.
Proc Biol Sci ; 290(2012): 20230525, 2023 Dec 06.
Article in English | MEDLINE | ID: mdl-38052246

ABSTRACT

The accelerating pace of emerging zoonotic diseases in the twenty-first century has motivated cross-disciplinary collaboration on One Health approaches, combining microbiology, veterinary and environmental sciences, and epidemiology for outbreak prevention and mitigation. Such outbreaks are often caused by spillovers attributed to human activities that encroach on wildlife habitats and ecosystems, such as land use change, industrialized food production, urbanization and animal trade. While the origin of anthropogenic effects on animal ecology and biogeography can be traced to the Late Pleistocene, the archaeological record-a long-term archive of human-animal-environmental interactions-has largely been untapped in these One Health approaches, thus limiting our understanding of these dynamics over time. In this review, we examine how humans, as niche constructors, have facilitated new host species and 'disease-scapes' from the Late Pleistocene to the Anthropocene, by viewing zooarchaeological, bioarchaeological and palaeoecological data with a One Health perspective. We also highlight how new biomolecular tools and advances in the '-omics' can be holistically coupled with archaeological and palaeoecological reconstructions in the service of studying zoonotic disease emergence and re-emergence.


Subject(s)
Ecosystem , One Health , Animals , Humans , Archaeology , Zoonoses/epidemiology , Ecology
3.
Biol Lett ; 19(4): 20220566, 2023 04.
Article in English | MEDLINE | ID: mdl-37122196

ABSTRACT

Past and ongoing human activities have shaped the geographical ranges and diversity of species. New genomic techniques applied to degraded samples, such as those from natural history collections, can uncover the complex evolutionary consequences of human pressures and generate baselines for interpreting magnitudes of species loss or persistence relevant to conservation. Here we integrate mitogenomic data with historical records from a recently rediscovered Bahamian hutia (Geocapromys ingrahami; (FMP Z02816)) specimen at the Fairbanks Museum & Planetarium (Vermont, USA) to determine when and where the specimen was collected and to place it in a phylogenetic context with specimens that both predate (palaeontological) and postdate (archaeological) human arrival in The Bahamas. We determined that this specimen was part of the same population as the named holotype specimen in 1891 on East Plana Cay (EPC). Bahamian hutia populations were widely extirpated following European colonization. Today, EPC hosts the last remaining natural Bahamian hutia population. Mitogenomic data places the focal specimen within the southern Bahamian hutia population, which is now largely restricted to EPC. The results reveal previously undocumented genetic continuity among the EPC population for at least the past 500 years, highlighting how 'dark' museum specimens inform new conservation-relevant understandings of diversity.


Subject(s)
DNA , Rodentia , Animals , Humans , Phylogeny , Rodentia/genetics , Biological Evolution , Genomics
4.
Am Nat ; 200(1): 140-155, 2022 07.
Article in English | MEDLINE | ID: mdl-35737983

ABSTRACT

AbstractScientists recognize the Caribbean archipelago as a biodiversity hotspot and employ it for their research as a natural laboratory. Yet they do not always appreciate that these ecosystems are in fact palimpsests shaped by multiple human cultures over millennia. Although post-European anthropogenic impacts are well documented, human influx into the region began about 5,000 years prior. Thus, inferences of ecological and evolutionary processes within the Caribbean may in fact represent artifacts of an unrecognized human legacy linked to issues influenced by centuries of colonial rule. The threats posed by stochastic natural and anthropogenically influenced disasters demand that we have an understanding of the natural history of endemic species if we are to halt extinctions and maintain access to traditional livelihoods. However, systematic issues have significantly biased our biological knowledge of the Caribbean. We discuss two case studies of the Caribbean's fragmented natural history collections and the effects of differing governance by the region's multiple nation states. We identify knowledge gaps and highlight a dire need for integrated and accessible inventorying of the Caribbean's collections. Research emphasizing local and international collaboration can lead to positive steps forward and will ultimately help us more accurately study Caribbean biodiversity and the ecological and evolutionary processes that generated it.


Subject(s)
Biodiversity , Ecosystem , Biological Evolution , Caribbean Region , Humans
5.
Nature ; 532(7598): 232-5, 2016 Apr 14.
Article in English | MEDLINE | ID: mdl-27049941

ABSTRACT

As the last habitable continent colonized by humans, the site of multiple domestication hotspots, and the location of the largest Pleistocene megafaunal extinction, South America is central to human prehistory. Yet remarkably little is known about human population dynamics during colonization, subsequent expansions, and domestication. Here we reconstruct the spatiotemporal patterns of human population growth in South America using a newly aggregated database of 1,147 archaeological sites and 5,464 calibrated radiocarbon dates spanning fourteen thousand to two thousand years ago (ka). We demonstrate that, rather than a steady exponential expansion, the demographic history of South Americans is characterized by two distinct phases. First, humans spread rapidly throughout the continent, but remained at low population sizes for 8,000 years, including a 4,000-year period of 'boom-and-bust' oscillations with no net growth. Supplementation of hunting with domesticated crops and animals had a minimal impact on population carrying capacity. Only with widespread sedentism, beginning ~5 ka, did a second demographic phase begin, with evidence for exponential population growth in cultural hotspots, characteristic of the Neolithic transition worldwide. The unique extent of humanity's ability to modify its environment to markedly increase carrying capacity in South America is therefore an unexpectedly recent phenomenon.


Subject(s)
Human Migration/history , Population Dynamics/history , Agriculture/history , Archaeology , Climate , Geographic Mapping , History, Ancient , Humans , Radiometric Dating , Siberia/ethnology , South America
6.
Proc Natl Acad Sci U S A ; 116(51): 25745-25755, 2019 12 17.
Article in English | MEDLINE | ID: mdl-31772017

ABSTRACT

Venom systems are key adaptations that have evolved throughout the tree of life and typically facilitate predation or defense. Despite venoms being model systems for studying a variety of evolutionary and physiological processes, many taxonomic groups remain understudied, including venomous mammals. Within the order Eulipotyphla, multiple shrew species and solenodons have oral venom systems. Despite morphological variation of their delivery systems, it remains unclear whether venom represents the ancestral state in this group or is the result of multiple independent origins. We investigated the origin and evolution of venom in eulipotyphlans by characterizing the venom system of the endangered Hispaniolan solenodon (Solenodon paradoxus). We constructed a genome to underpin proteomic identifications of solenodon venom toxins, before undertaking evolutionary analyses of those constituents, and functional assessments of the secreted venom. Our findings show that solenodon venom consists of multiple paralogous kallikrein 1 (KLK1) serine proteases, which cause hypotensive effects in vivo, and seem likely to have evolved to facilitate vertebrate prey capture. Comparative analyses provide convincing evidence that the oral venom systems of solenodons and shrews have evolved convergently, with the 4 independent origins of venom in eulipotyphlans outnumbering all other venom origins in mammals. We find that KLK1s have been independently coopted into the venom of shrews and solenodons following their divergence during the late Cretaceous, suggesting that evolutionary constraints may be acting on these genes. Consequently, our findings represent a striking example of convergent molecular evolution and demonstrate that distinct structural backgrounds can yield equivalent functions.


Subject(s)
Eutheria , Evolution, Molecular , Genome/genetics , Shrews , Venoms/genetics , Animals , Eutheria/classification , Eutheria/genetics , Eutheria/physiology , Gene Duplication , Male , Phylogeny , Proteomics , Shrews/classification , Shrews/genetics , Shrews/physiology , Tissue Kallikreins/genetics
7.
Mol Biol Evol ; 37(10): 2931-2943, 2020 10 01.
Article in English | MEDLINE | ID: mdl-32497204

ABSTRACT

Ancient biomolecule analyses are proving increasingly useful in the study of evolutionary patterns, including extinct organisms. Proteomic sequencing techniques complement genomic approaches, having the potential to examine lineages further back in time than achievable using ancient DNA, given the less stringent preservation requirements. In this study, we demonstrate the ability to use collagen sequence analyses via proteomics to assist species delimitation as a foundation for informing evolutionary patterns. We uncover biogeographic information of an enigmatic and recently extinct lineage of Nesophontes across their range on the Caribbean islands. First, evolutionary relationships reconstructed from collagen sequences reaffirm the affinity of Nesophontes and Solenodon as sister taxa within Solenodonota. This relationship helps lay the foundation for testing geographical isolation hypotheses across islands within the Greater Antilles, including movement from Cuba toward Hispaniola. Second, our results are consistent with Cuba having just two species of Nesophontes (N. micrus and N. major) that exhibit intrapopulation morphological variation. Finally, analysis of the recently described species from the Cayman Islands (N. hemicingulus) indicates that it is a closer relative to N. major rather than N. micrus as previously speculated. This proteomic sequencing improves our understanding of the origin, evolution, and distribution of this extinct mammal lineage, particularly with respect to the approximate timing of speciation. Such knowledge is vital for this biodiversity hotspot, where the magnitude of recent extinctions may obscure true estimates of species richness in the past.


Subject(s)
Biological Evolution , Collagen/chemistry , Shrews/genetics , Animals , Female , Male , Mandible/anatomy & histology , Phylogeography , Sequence Analysis, Protein , Sex Characteristics , Shrews/anatomy & histology , West Indies
8.
Proc Biol Sci ; 287(1927): 20200447, 2020 05 27.
Article in English | MEDLINE | ID: mdl-32429803

ABSTRACT

The human-mediated movement of species across biogeographic boundaries-whether intentional or accidental-is dramatically reshaping the modern world. Yet humans have been reshaping ecosystems and translocating species for millennia, and acknowledging the deeper roots of these phenomena is important for contextualizing present-day biodiversity loss, ecosystem functioning and management needs. Here, we present the first database of terrestrial vertebrate species introductions spanning the entire anthropogenic history of a system: the Caribbean. We employ this approximately 7000-year dataset to assess the roles of historical contingency and priority effects in shaping present-day community structure and conservation outcomes, finding that serial human colonization events contributed to habitat modifications and species extinctions that shaped the trajectories of subsequent species introductions by other human groups. We contextualized spatial and temporal patterns of species introductions within cultural practices and population histories of Indigenous, colonial and modern human societies, and show that the taxonomic and biogeographic diversity of introduced species reflects diversifying reasons for species introductions through time. Recognition of the complex social and economic structures across the 7000-year human history of the Caribbean provides the necessary context for interpreting the formation of an Anthropocene biota.


Subject(s)
Biodiversity , Ecosystem , Animals , Biota , Caribbean Region , Conservation of Natural Resources , Extinction, Biological , Humans , Introduced Species
9.
Bioscience ; 69(11): 877-887, 2019 Nov 01.
Article in English | MEDLINE | ID: mdl-31719710

ABSTRACT

Drivers of Late Quaternary megafaunal extinctions are relevant to modern conservation policy in a world of growing human population density, climate change, and faunal decline. Traditional debates tend toward global solutions, blaming either dramatic climate change or dispersals of Homo sapiens to new regions. Inherent limitations to archaeological and paleontological data sets often require reliance on scant, poorly resolved lines of evidence. However, recent developments in scientific technologies allow for more local, context-specific approaches. In the present article, we highlight how developments in five such methodologies (radiocarbon approaches, stable isotope analysis, ancient DNA, ancient proteomics, microscopy) have helped drive detailed analysis of specific megafaunal species, their particular ecological settings, and responses to new competitors or predators, climate change, and other external phenomena. The detailed case studies of faunal community composition, extinction chronologies, and demographic trends enabled by these methods examine megafaunal extinctions at scales appropriate for practical understanding of threats against particular species in their habitats today.

11.
Biol Lett ; 12(6)2016 06.
Article in English | MEDLINE | ID: mdl-27330176

ABSTRACT

Understanding extinction drivers in a human-dominated world is necessary to preserve biodiversity. We provide an overview of Quaternary extinctions and compare mammalian extinction events on continents and islands after human arrival in system-specific prehistoric and historic contexts. We highlight the role of body size and life-history traits in these extinctions. We find a significant size-bias except for extinctions on small islands in historic times. Using phylogenetic regression and classification trees, we find that while life-history traits are poor predictors of historic extinctions, those associated with difficulty in responding quickly to perturbations, such as small litter size, are good predictors of prehistoric extinctions. Our results are consistent with the idea that prehistoric and historic extinctions form a single continuing event with the same likely primary driver, humans, but the diversity of impacts and affected faunas is much greater in historic extinctions.


Subject(s)
Extinction, Biological , Mammals/physiology , Animals , Body Size , Human Activities , Humans , Islands , Life Cycle Stages , Mammals/anatomy & histology , Mammals/classification , Phylogeny
12.
G3 (Bethesda) ; 14(4)2024 04 03.
Article in English | MEDLINE | ID: mdl-38366575

ABSTRACT

Reference genome assemblies have been created from multiple lineages within the Canidae family; however, despite its phylogenetic relevance as a basal genus within the clade, there is currently no reference genome for the gray fox (Urocyon cinereoargenteus). Here, we present a chromosome-level assembly for the gray fox (U. cinereoargenteus), which represents the most contiguous, non-domestic canid reference genome available to date, with 90% of the genome contained in just 34 scaffolds and a contig N50 and scaffold N50 of 59.4 and 72.9 Megabases, respectively. Repeat analyses identified an increased number of simple repeats relative to other canids. Based on mitochondrial DNA, our Vermont sample clusters with other gray fox samples from the northeastern United States and contains slightly lower levels of heterozygosity than gray foxes on the west coast of California. This new assembly lays the groundwork for future studies to describe past and present population dynamics, including the delineation of evolutionarily significant units of management relevance. Importantly, the phylogenetic position of Urocyon allows us to verify the loss of PRDM9 functionality in the basal canid lineage, confirming that pseudogenization occurred at least 10 million years ago.


Subject(s)
Chromosomes , Foxes , Animals , Foxes/genetics , Phylogeny , Chromosomes/genetics , DNA, Mitochondrial/genetics , Genome
13.
Ecol Evol ; 12(3): e8761, 2022 Mar.
Article in English | MEDLINE | ID: mdl-35356572

ABSTRACT

While trends in tropical deforestation are alarming, conservation biologists are increasingly recognizing the potential for species survival in human-modified landscapes. Identifying the factors underlying such persistence, however, requires basic ecological knowledge of a species' resource use. Here, we generate such data to guide conservation of an understudied venomous mammal, the Hispaniolan solenodon (Solenodon paradoxus), that occupies a mosaic landscape of agriculture and forest fragments in the western Dominican Republic. Using feces collected in both wet and dry seasons, we found significant differences in the stable isotope values of carbon (δ13C) between pasture (-24.63 ± 2.31‰, Las Mercedes) and agroforestry (-28.07 ± 2.10‰, Mencia). Solenodon populations in agricultural areas occupied wider isotopic niche spaces, which may be explained by more diverse resource within these patches or individuals combining resources across habitats. We detected elevated δ15N values in the dry season of pasture areas (8.22 ± 2.30‰) as compared to the wet season (5.26 ± 2.44‰) and overall narrower isotopic niche widths in the dry season, suggestive of the impacts of aridity on foraging behavior. Our work highlights the importance of considering a more nuanced view of variations in 'modified' or "agricultural" landscapes as compared with strictly protected national parks. We suggest that seasonal differences in foraging should be considered as they intersect with landscape modification by landowners for maintaining resources for focal consumers. This work adds to a growing body of literature highlighting that fecal stable isotopes are a non-invasive and cost-effective monitoring tool that is particularly well-suited for cryptic small mammal species, ensuring actionable and evidenced-based conservation practices in the tropic's rapidly changing landscapes.

14.
Ecol Evol ; 12(9): e9216, 2022 Sep.
Article in English | MEDLINE | ID: mdl-36177145

ABSTRACT

Cities are among the most extreme forms of anthropogenic ecosystem modification, and urbanization processes exert profound effects on animal populations through multiple ecological pathways. Increased access to human-associated food items may alter species' foraging behavior and diet, in turn modifying the normal microbial community of the gastrointestinal tract (GIT), ultimately impacting their health. It is crucial we understand the role of dietary niche breadth and the resulting shift in the gut microbiota as urban animals navigate novel dietary resources. We combined stable isotope analysis of hair and microbiome analysis of four gut regions across the GIT to investigate the effects of urbanization on the diet and gut microbiota of two sympatric species of rodents with different dietary niches: the omnivorous large Japanese field mouse (Apodemus speciosus) and the relatively more herbivorous gray red-backed vole (Myodes rufocanus). Both species exhibited an expanded dietary niche width within the urban areas potentially attributable to novel anthropogenic foods and altered resource availability. We detected a dietary shift in which urban A. speciosus consumed more terrestrial animal protein and M. rufocanus more plant leaves and stems. Such changes in resource use may be associated with an altered gut microbial community structure. There was an increased abundance of the presumably probiotic Lactobacillus in the small intestine of urban A. speciosus and potentially pathogenic Helicobacter in the colon of M. rufocanus. Together, these results suggest that even taxonomically similar species may exhibit divergent responses to urbanization with consequences for the gut microbiota and broader ecological interactions.

15.
Sci Rep ; 10(1): 5069, 2020 03 19.
Article in English | MEDLINE | ID: mdl-32193515

ABSTRACT

As fossilized feces, coprolites represent direct evidence of animal behavior captured in the fossil record. They encapsulate past ecological interactions between a consumer and its prey and, when they contain plant material, can also guide paleoenvironmental reconstructions. Here we describe the first coprolites from the lagerstätte Rancho La Brea (RLB) in Los Angeles, California, which also represent the first confirmed coprolites from an asphaltic ("tar pit") context globally. Combining multiple lines of evidence, including radiocarbon dating, body size reconstructions, stable isotope analysis, scanning electron microscopy, and sediment analyses, we document hundreds of rodent coprolites found in association with plant material, and tentatively assign them to the woodrat genus Neotoma. Neotoma nests (i.e., middens) and their associated coprolites inform paleoclimatic reconstructions for the arid southwestern US but are not typically preserved in coastal areas due to environmental and physiological characteristics. The serendipitous activity of an asphalt seep preserved coprolites and their original cellulosic material for 50,000 years at RLB, yielding a snapshot of coastal California during Marine Isotope Stage 3. This discovery augments the proxies available at an already critical fossil locality and highlights the potential for more comprehensive paleoenvironmental analyses at other asphaltic localities globally.

16.
Sci Rep ; 10(1): 15172, 2020 09 16.
Article in English | MEDLINE | ID: mdl-32938967

ABSTRACT

An accurate understanding of biodiversity of the past is critical for contextualizing biodiversity patterns and trends in the present. Emerging techniques are refining our ability to decipher otherwise cryptic human-mediated species translocations across the Quaternary, yet these techniques are often used in isolation, rather than part of an interdisciplinary hypothesis-testing toolkit, limiting their scope and application. Here we illustrate the use of such an integrative approach and report the occurrence of North America's largest terrestrial mammalian carnivore, the short-faced bear, Arctodus simus, from Daisy Cave (CA-SMI-261), an important early human occupation site on the California Channel Islands. We identified the specimen by corroborating morphological, protein, and mitogenomic lines of evidence, and evaluated the potential natural and anthropogenic mechanisms of its transport and deposition. While representing just a single specimen, our combination of techniques opened a window into the behavior of an enigmatic species, suggesting that A. simus was a wide-ranging scavenger utilizing terrestrial and marine carcasses. This discovery highlights the utility of bridging archaeological and paleontological datasets to disentangle complex biogeographic scenarios and reveal unexpected biodiversity for island systems worldwide.


Subject(s)
Animal Migration , Ecosystem , Phylogeography/methods , Ursidae , Animals , Biodiversity , California , Fossils , Humans , Islands
17.
Trends Ecol Evol ; 35(7): 551-554, 2020 07.
Article in English | MEDLINE | ID: mdl-32416950

ABSTRACT

Species reintroductions involve considerable uncertainty, especially in highly altered landscapes. Historical, geographic, and taxonomic analogies can help reduce this uncertainty by enabling conservationists to better assess habitat suitability in proposed reintroduction sites. We illustrate this approach using the example of the California grizzly, an iconic species proposed for reintroduction.


Subject(s)
Conservation of Natural Resources , Ecosystem , Uncertainty
18.
Science ; 355(6325)2017 02 10.
Article in English | MEDLINE | ID: mdl-28183912

ABSTRACT

Conservation of species and ecosystems is increasingly difficult because anthropogenic impacts are pervasive and accelerating. Under this rapid global change, maximizing conservation success requires a paradigm shift from maintaining ecosystems in idealized past states toward facilitating their adaptive and functional capacities, even as species ebb and flow individually. Developing effective strategies under this new paradigm will require deeper understanding of the long-term dynamics that govern ecosystem persistence and reconciliation of conflicts among approaches to conserving historical versus novel ecosystems. Integrating emerging information from conservation biology, paleobiology, and the Earth sciences is an important step forward on the path to success. Maintaining nature in all its aspects will also entail immediately addressing the overarching threats of growing human population, overconsumption, pollution, and climate change.


Subject(s)
Biodiversity , Conservation of Natural Resources/methods , Conservation of Natural Resources/trends , Extinction, Biological , Animals , Climate Change , Endangered Species , Environmental Pollution , Gorilla gorilla , Humans , Introduced Species , Policy , Population Dynamics
20.
PLoS One ; 9(10): e111856, 2014.
Article in English | MEDLINE | ID: mdl-25360617

ABSTRACT

The muskrat, Ondatra zibethicus, is a semiaquatic rodent native to North America that has become a highly successful invader across Europe, Asia, and South America. It can inflict ecological and economic damage on wetland systems outside of its native range. Anecdotal evidence suggests that, in the early 1900s, a population of muskrats was introduced to the Isles of Shoals archipelago, located within the Gulf of Maine, for the purposes of fur harvest. However, because muskrats are native to the northeastern coast of North America, their presence on the Isles of Shoals could be interpreted as part of the native range of the species, potentially obscuring management planning and biogeographic inferences. To investigate their introduced status and identify a historic source population, muskrats from Appledore Island of the Isles of Shoals, and from the adjacent mainland of Maine and New Hampshire, were compared for mitochondrial cytochrome b sequences and allele frequencies at eight microsatellite loci. Appledore Island muskrats consistently exhibited reduced genetic diversity compared with mainland populations, and displayed signatures of a historic bottleneck. The distribution of mitochondrial haplotypes is suggestive of a New Hampshire source population. The data presented here are consistent with a human-mediated introduction that took place in the early 1900s. This scenario is further supported by the zooarchaeological record and island biogeographic patterns. This is the first genetic study of an introduced muskrat population within US borders and of any island muskrat population, and provides an important contrast with other studies of introduced muskrat populations worldwide.


Subject(s)
Arvicolinae/genetics , Genetic Variation , Introduced Species , Animals , Cytochromes b/genetics , DNA, Mitochondrial/genetics , Geography , Haplotypes/genetics , Islands , Microsatellite Repeats/genetics , North America , Population Density , Time Factors
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