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Guschanski, K.

Publications and source records attributed to Guschanski, K..

At least 19 recordsLinked to original sources

Shared and genus-specific impact of domestication on mammal oral microbiomes revealed through museomics

Animal domestication involves genetic, behavioural and ecological changes, all of which also impact the host-associated microbial communities. Early studies reported diversity loss in the gut microbiomes of domestic and captive animals, but comparisons across a wider diversity of host species showed that loss of microbiota does not always occur. For microbial communities other than the gut, comparisons of multiple domestic-wild pairs are lacking. Here, we use dental calculus metagenomics to investigate the impact of a domesticated lifestyle on the oral microbiome of three pairs of wild and domestic mammals from the genera Equus (plains zebra, horse), Ovis (argali, sheep) and Sus (wild boar, pig). We find that the oral microbiome of the three domesticates differs both in terms of taxonomic composition and functional capacity from their wild counterparts, but the change is smaller in Sus than the other two pairs. While the microbiomes of sheep and horses bear increased resemblance to those of humans compared to their wild relatives, this is unlikely to be due to colonisation by human-derived microbes, as our results suggest that ancestral lineages are mostly retained. Overall, the oral microbiome shows both a consistent signal of domestication, found across all three clades, and a host genus-dependent effect, which likely results from specific changes that underpinned each domestication event.

evolutionary biology↗

Karyotypic evolution in a diverse primate clade and the role of chromosomal fissions as barriers to gene flow

The classical model of chromosomal speciation is based on the observation that divergent species often differ in chromosome numbers and that heterokaryotypic hybrids show reduced fitness. Furthermore, positive correlations between the rates of karyotype evolution and speciation have been established in several groups of organisms. Yet, the mechanisms that make some lineages more prone to chromosomal fissions and fusions than others, and the causal role of such karyotype changes in speciation, are poorly understood. Here, we focus on the taxonomically and karyotypically diverse group of African monkeys, the guenons (tribe Cercopithecini), consisting of ~35 species with diploid chromosome numbers ranging from 48 to 72. We generated de novo genome assemblies for eight species with different karyotypes, and incorporated publicly available genomes from additionally three guenon species. Using the rhesus macaque as an outgroup, we identified 28 independent chromosomal fissions and 4 fusions in guenons. In line with previous cytogenetic studies, repeat composition around chromosomal breakpoints suggested that most fissions were non-centromeric, requiring the evolution of a new centromere in at least one of the fission products. In contrast to the expectation under strong underdominance, we found a paraphyletic distribution of several chromosomal fissions. Some of these phylogenetically discordant events could have resulted from interspecific hybridization, whereas others are more likely caused by incomplete lineage sorting, suggesting that fissioned and non-fissioned homologs segregated in ancestral guenon lineages for millions of years. Nevertheless, we find evidence for reduced introgression on rearranged chromosomes in an ancient cross-karyotypic gene flow event between Cercopithecus cephus and C. pogonias. Although this suggests that chromosomal fissions may have constituted barriers to gene flow in the guenon evolution, the signal was inconclusive or absent in two other investigated gene flow events. This study provides important first insights into the remarkable karyotypic diversification of guenons, and its role in generating reproductive barriers.

evolutionary biology↗

Museum specimens reveal evolutionary drivers and functions of oral microbiome in mammals

The microbiomes of wild animals, despite being integral to host survival, remain largely unexplored, particularly beyond the gut. Here, using > 450 museum-preserved dental calculus samples from 34 ecologically and phylogenetically diverse mammalian species, most of them previously unstudied, we determine the main drivers of oral microbiome evolution. We show that, similar to the gut, the oral microbiome is shaped by host ecology, particularly diet, and to a lesser extent host phylogenetic relationships. It may contribute to host adaptation, by synthesising essential micronutrients and degrading potentially harmful compounds. We also find that some oral microorganisms consistently associated with mammals throughout over evolutionary time scales and provide evidence for a likely oral origin of some rumen taxa. Together our findings demonstrate the importance of this mostly overlooked microbial community for mammalian biology.

evolutionary biology↗

Lifestyle impacts the oral microbiome of Classical and Post-classical societies in Italy

ObjectivesThe fall of the Roman Empire (476 CE) profoundly affected the lives of its peoples due to the political, administrative, and territorial changes that occurred. The majority of written records of the time focus on the social elite, leaving larger parts of the population understudied. Here, we employ a bioarchaeological approach to understand how differences in lifestyle may be reflected in the oral microbiome of people from different social classes living before and after the fall. Material and MethodsWe analysed shotgun sequencing data from dental calculus, the preserved oral microbiome, of 67 individuals belonging to different social classes from two Classical cemeteries dated to I-III century CE (Lucus Feroniae and Isola Sacra) and one post-Classical cemetery dated to IV-VIII century CE (Selvicciola), all located in proximity to the city of Rome, Italy. ResultsWe detect significant differences in the oral microbiome taxonomic and functional composition across time periods and social classes, with the rural town of Lucus Feroniae standing out compared to its two counterparts. Reliable identification of dietary items was not possible. DiscussionThe distinct oral microbiome of Lucus Feroniae could reflect differences in general health and subsistence practices. The rural position of this community may have mitigated the cyclical food crises that, instead, affected the contemporary Isola Sacra and the later community of Selvicciola, thereby buffering against the nutritional stress observed in these two locations.

genomics↗

Dental calculus formation is linked to diet and phylogeny in mammals

O_LIAs a point of entry, the oral cavity serves as a potential first area of colonization of the host with environmental bacteria. As such, the oral microbial community not only affects a wide range of internal host processes, including health and digestion but may also reflect the external environment and ecology of the host. C_LIO_LIDental calculus, a mineralized form of dental plaque, preserves the DNA of the host microbiome through time, serving as a rich source of historical microbiota. Despite its potential to provide temporal information on the ecological and evolutionary processes of microbiomes, dental calculus has rarely been explored outside of humans and non-human primates. Hence, it remains unclear how ubiquitous it is across mammals. C_LIO_LIUsing natural history museum collections, we surveyed > 1600 specimens belonging to 142 species, representative of every mammalian order, to investigate the taxonomic distribution of dental calculus, and to identify factors that most strongly contribute to its formation. We found dental calculus to be abundant across mammalian taxa, with 104 of the surveyed species showing calculus deposits. C_LIO_LIHigh fiber diets were most strongly associated with calculus presence and abundance, whereas species with high protein and fat diets showed little to no calculus deposits. We also found evidence of phylogenetic signal in calculus formation, pointing to the effects of oral/dental morphology. In addition, captivity strongly affected dental calculus formation in almost all dietary categories. Using this information, we made predictions about the likelihood of finding dental calculus in unsurveyed mammalian species, with the aim of informing future investigations. C_LIO_LIOur study found that dental calculus is readily available in natural history museum collections, making it an easily accessible source of oral microbiota from wild animals. We highlight the taxonomic diversity of species presenting dental calculus and provide information and suggestions to researchers and museum curators interested in utilizing dental calculus for the study of oral microbiota, past and present. C_LI

ecology↗

Pleistocene reindeer dental calculus as a source for ancient oral and digestive flora

Dental calculus offers an extraordinary window into the past, preserving a rich archive of genetic material that can unlock new insights into ancient ecosystems. By capturing traces of oral microbiomes, dietary components, and even gut microbes regurgitated by ruminants, dental calculus provides an extraordinary window into the past to reconstruct ecological interactions and past environmental conditions. Here, we harness the power of ancient metagenomics to explore the oral microbiome, digestive microbiomes and diet of Pleistocene reindeer (Rangifer tarandus) from archaeological sites in France, a region that once served as a glacial refugium before reindeer disappeared from the area. We used shotgun metagenomic sequencing to assemble microbial genomes (MAGs) and classify microbial and dietary reads from dental calculus of 19 ancient reindeer (ca. 12,000 - 23,000 years BP) and 27 modern and historical (1861 - 1958 CE) Scandinavian reindeer. Notably, six bacterial taxa associated with the rumen microbiome were consistently detected across both ancient and modern samples, offering a rare glimpse into the continuity of digestive adaptations over thousands of years. Our recovery of oral microbial and putative dietary plant DNA suggest adaptive capability. Our results suggest a spatio-temporal turnover in oral microbiome and putative dietary plant DNA, which might be explained by ecological differences between Pleistocene France and contemporary Scandinavia. As soft tissue preservation is rare in ancient remains, dental calculus emerges as an exciting and powerful tool for reconstructing the environmental and ecological histories of both past and extinct populations.

evolutionary biology↗

Holotype genome of the lesula provides insights into demography and evolution of a threatened primate lineage

The rapid development of genome sequencing techniques in recent decades has revolutionized the field of evolutionary biology, facilitating the study of adaptation and speciation at the genome level. Genomic data has also become a cornerstone in conservation management, allowing inferences of population demography and genetic diversity. Here, we sequenced the genome of the holotype specimen of the elusive lesula (Cercopithecus lomamiensis), a recently described member of the guenons (tribe Cercopithecini) endemic to the Democratic Republic of the Congo. Using published and novel genomic data, we explore the evolutionary and demographic history of C. lomamiensis and its sister species C. hamlyni, the only two members of the hamlyni species group. We estimate that the two species split ca. 3-4 million years ago, and find that they both show high genetic diversity despite being listed as vulnerable on the IUCN Red List. We identify signatures of positive selection in the hamlyni group in genes involved in, e.g., pelage coloration and immune functions, as well as skeletal morphology and locomotor behavior, potentially related to their terrestrial lifestyle which stands out among the otherwise arboreal Cercopithecus genus. We specifically explored whether introgression from more distantly related terrestrial guenons was involved in the evolution of terrestriality in the hamlyni group. However, molecular convergence with other terrestrial species was low, suggesting that putative terrestrial adaptations occurred largely independently. By sequencing the C. lomamiensis genome, this study provides insights into the demography and evolutionary history in a threatened primate lineage, with relevance to conservation management.

evolutionary biology↗

Host traits impact the outcome of metagenomic library preparation from dental calculus samples across diverse mammals

Dental calculus metagenomics has emerged as a valuable tool for studying the oral microbiomes of humans and a few select mammals. With increasing interest in wild animal microbiomes, it is important to understand how widely this material can be used across the mammalian tree of life, refine the related protocols and understand the expected outcomes and potential challenges of dental calculus sample processing. In this study we significantly expand the breadth of studied host species, analysing laboratory and bioinformatics metadata of dental calculus samples from 32 ecologically and phylogenetically diverse mammals. While we confirm the presence of an oral microbiome signature in the metagenomes of all studied mammals, the fraction recognised as oral varies between host species, possibly due to both biological differences and methodological biases. The overall success rate of dental calculus processing, from extractions to sequencing, was ~74%. Although input sample weight was positively associated with the number of produced library molecules, we identify a negative impact of enzymatic inhibition on the library preparation protocol. The inhibition was most prevalent in herbivores and frugivores and is likely diet-derived. In contrast, hosts with an animalivore diet posed fewer challenges during laboratory processing, and yielded more DNA relative to sample weight. Our results translate into recommendations for future studies of dental calculus metagenomics from a variety of host species, identifying required sample amounts, and emphasising the utility of dental calculus in exploring the oral microbiome in relation to broader ecological and evolutionary questions.

genomics↗

Genomic signatures of island colonization in highly diverse primates

Understanding how small populations cope with loss of genetic diversity and deleterious variation is crucial to address the current biodiversity crisis. Insular populations are particularly interesting as they have often persisted at low population sizes and higher inbreeding than their mainland counterparts. While the genome-wide consequences of inbreeding in threatened insular species have received some attention, comparative genomics between insular and mainland populations of wide-spread and genetically diverse species have rarely been performed. Yet, they are particularly well suited to inform about the consequences of drastic population declines from initially large populations - a phenomenon that is becoming increasingly common. The spot-nosed monkey (Cercopithecus petaurista), the Campbells monkey (Cercopithecus campbelli) and the green monkey (Chlorocebus sabaeus) are common and genetically diverse West African primates. Insular populations can be found at the Bijagos Archipelago, Guinea-Bissau. Here, we assessed the genome-wide diversity, inbreeding, genetic load and adaptive variation using whole genome sequencing data from insular and mainland populations. In the three species, island populations showed lower genome-wide diversity and higher inbreeding. Genetic drift has likely promoted the conversion of masked genetic load into realized load without increased purging of deleterious variation. Additionally, we found no evidence for accumulation of deleterious variation, suggesting that these populations are not yet at risk of extinction by genetic factors and may act as reservoirs of mainland genetic diversity. We highlight, however, that other anthropogenic factors are threatening these insular primates and therefore conservation management should target their immediate threats and safeguard against additional loss of diversity.

genomics↗

Avoidable false PSMC population size peaks occur across numerous studies

Inferring historical population sizes is key to identify drivers of ecological and evolutionary change, and crucial to predict the future of species on our rapidly changing planet. The pairwise sequentially Markovian coalescent (PSMC) method provided a revolutionary framework to reconstruct species demographic histories over millions of years based on the genome sequence of a single individual 1. Here, we detected and solved a common artifact in PSMC and related methods: recent population peaks followed by population collapses. Combining real and simulated genomes, we show that these peaks do not represent true population dynamics. Instead, ill-set default parameters cause false peaks in our own and published data, which can be avoided by adjusted parameter settings. Furthermore, we show that certain population structure changes can cause similar patterns. Newer methods like Beta-PSMC perform better, but do not always avoid this artifact. Our results suggest testing multiple parameters before interpreting recent population peaks followed by collapses, and call for the development of robust methods.

evolutionary biology↗

Screening great ape museum specimens for DNA viruses

Natural history museum collections harbour a record of wild species from the past centuries, providing a unique opportunity to study animals as well as their infectious agents. Thousands of great ape specimens are kept in these collections, and could become an important resource for studying the evolution of DNA viruses. Their genetic material is likely to be preserved in dry museum specimens, as reported previously for monkeypox virus genomes from historical orangutan specimens. Here, we screened 209 great ape museum specimens for 99 different DNA viruses, using hybridization capture coupled with short-read high-throughput sequencing. We determined the presence of multiple viruses within this dataset from historical specimens and obtained several near-complete viral genomes. In particular, we report high-coverage (>18-fold) hepatitis B virus genomes from one gorilla and two chimpanzee individuals, which are phylogenetically placed within clades infecting the respective host species.

genomics↗

Breaking the rule: An exceptional Y chromosome introgression between deeply divergent primate species

Hybridization between distinct lineages is widespread in nature, with important implications for adaptation and speciation. If hybrids are fertile, alleles can introgress across species boundaries. Hybrid fitness is often sex dependent, with heterogametic hybrids showing lower fitness than homogametic individuals, a phenomenon known as Haldanes rule. Consequently, loci inherited strictly through the heterogametic sex rarely introgress. We focus on the Y-chromosomal history of guenons (tribe Cercopithecini), a group of African primates that hybridized extensively throughout their evolutionary history. Although our inferences suggest that Haldanes rule is generally in place, we uncover a remarkable Y chromosome introgression event from Cercopithecus mitis into C. denti, which occurred ca. six million years after their initial divergence. Only a weak signal of autosomal gene flow is present, suggesting that the introgressing Y chromosome reached fixation in C. denti from a very low initial frequency. We use simulations to explore the evolutionary mechanisms at play, and find that selection is needed to achieve fixation of the novel Y chromosome. We identify a number of fixed protein differences between the introgressed and ancestral Y, with meiotic drive being an alternative mechanism to adaptive introgression. Our results show that the ability to produce viable and fertile heterogametic hybrids persisted for six million years in guenons, providing a remarkable exception to Haldanes rule.

evolutionary biology↗

Large-scale phylogenomics uncovers a complex evolutionary history and extensive ancestral gene flow in an African primate radiation

Understanding the drivers of speciation is fundamental in evolutionary biology, and recent studies highlight hybridization as a potential facilitator of adaptive radiations. Using whole-genome sequencing data from 22 species of guenons (tribe Cercopithecini), one of the worlds largest primate radiations, we show that rampant gene flow characterizes their evolutionary history, and identify ancient hybridization across deeply divergent lineages differing in ecology, morphology and karyotypes. Lineages experiencing gene flow tend to be more species-rich than non-admixed lineages. Mitochondrial transfers between distant lineages were likely facilitated by co-introgression of co-adapted nuclear variants. Although the genomic landscapes of introgression were largely lineage specific, we found that genes with immune functions were overrepresented in introgressing regions, in line with adaptive introgression, whereas genes involved in pigmentation and morphology may contribute to reproductive isolation. This study provides important insights into the prevalence, role and outcomes of ancestral hybridization in a large mammalian radiation.

evolutionary biology↗

Ghost admixture in eastern gorillas

Archaic admixture has had a significant impact on human evolution with multiple events across different clades, including from extinct hominins such as Neanderthals and Denisovans into modern humans. Within the great apes archaic admixture has been identified in chimpanzees and bonobos, but the possibility of such events has not been explored in other species. Here, we address this question using high-coverage whole genome sequences from all four extant gorilla subspecies, including six newly sequenced eastern gorillas from previously unsampled geographic regions. Using Approximate Bayesian Computation (ABC) with neural networks to model the demographic history of gorillas, we find a signature of admixture from an archaic ghost lineage into the common ancestor of eastern gorillas, but not western gorillas. We infer that up to 3% of the genome of these individuals is introgressed from an archaic lineage that diverged more than 3 million years ago from the common ancestor of all extant gorillas. This introgression event took place before the split of mountain and eastern lowland gorillas, likely more than 40 thousand years ago, and may have influenced perception of bitter taste in eastern gorillas. When comparing the introgression landscapes of gorillas, humans and bonobos, we find a consistent depletion of introgressed fragments on the X chromosome across these species. However, depletion in protein-coding content is not detectable in eastern gorillas, possibly as a consequence of stronger genetic drift in this species.

evolutionary biology↗

Dental calculus metagenomics suggest that ecology, not host phylogeny, shapes the oral microbiome in closely related species

Host-associated microbiomes are essential for a multitude of biological processes. Placed at the contact zone between external and internal environments, the little-studied oral microbiome has important roles in host physiology and health. Here we investigate the contribution of host evolutionary relationships and ecology in shaping the oral microbiome in three closely related gorilla subspecies (mountain, Grauers, and western lowland gorillas) using shotgun metagenomics of 46 museum-preserved dental calculus samples. We find that the oral microbiomes of mountain gorillas are functionally and taxonomically distinct from the other two subspecies, despite close evolutionary relationships and geographic proximity with Grauers gorillas. Grauers gorillas show intermediate bacterial taxonomic and functional, and dietary profiles. Altitudinal differences in gorilla subspecies ranges appear to explain these patterns, proposing a close connection between dental calculus microbiome and the environment, which is further supported by the presence of gorilla subspecies-specific phyllosphere/rhizosphere taxa. Mountain gorillas show high abundance of nitrate-reducing oral taxa, which may contribute to high altitude adaptation by modulating blood pressure. Our results suggest that ecology, rather than evolutionary relationships and geographic proximity, primarily shape the oral microbiome in these closely related species.

evolutionary biology↗

Isolated Grauer's gorilla populations differ in diet and gut microbiome

The animal gut microbiome has been implicated in a number of key biological processes, ranging from digestion to behavior, and has also been suggested to facilitate local adaptation. However, studies in wild animals rarely compare multiple populations that differ ecologically, which is the level at which local adaptation may occur. Further, few studies simultaneously characterize diet and the gut microbiome from the same sample, despite the likely presence of co-dependencies. Here, we investigate the interplay between diet and gut microbiome in three geographically isolated populations of the critically endangered Grauers gorilla, which we show to be genetically differentiated. We find population- and social group-specific dietary and gut microbial profiles and co-variation between diet and gut microbiome, despite the presence of core microbial taxa. There was no detectable effect of age, sex, or genetic relatedness on the microbiome. Diet differed considerably across populations, with the high-altitude population consuming a lower diversity of plants compared to low-altitude populations, consistent with food plant availability constraining diet. The observed pattern of covariation between diet and gut microbiome is likely a result of long-term social and ecological factors. Our study suggests that the gut microbiome is sufficiently plastic to support flexible food selection and hence contribute to local adaptation.

ecology↗

Wild animal oral microbiomes reflect the history of human antibiotics use

Following the advent of industrial-scale antibiotics production in the 1940s, antimicrobial resistance (AMR) has been on the rise and now poses a major global health threat. Because AMR can be exchanged between humans, livestock and wildlife, evaluating the potential of wild animals to act as AMR reservoirs is essential. We used shotgun metagenomics sequencing of dental calculus, the calcified form of the oral microbial biofilm, to determine the abundance and repertoire of AMR genes in the oral microbiome of Swedish brown bears from museum specimens collected over the last 200 years. Our temporal metagenomics approach allowed us to establish a baseline of natural AMR in the pre-antibiotics era and to quantify a significant increase in total AMR load and diversity of AMR genes that is correlated with human antibiotics use. We also demonstrated that Swedish public health policies were effective in limiting AMR spillover into wildlife.

microbiology↗

Conservation Genomic Analyses of African and Asiatic Cheetahs (Acinonyx jubatus) Across Their Current and Historic Species Range.

Cheetahs (Acinonyx jubatus) are majestic carnivores and the fastest land animals; yet, they are quickly heading towards an uncertain future. Threatened by habitat loss, human-interactions and illegal trafficking, there are only approximately 7,100 individuals remaining in the wild. Cheetahs used to roam large parts of Africa, and Western and Southern Asia. Today they are confined to about 9% of their original distribution. To investigate their genetic diversity and conservation status, we generated genome-wide data from historical and modern samples of all four currently recognized subspecies, along with mitochondrial DNA (mtDNA) and major histo-compatibility complex (MHC) data. We found clear genetic differentiation between the sub-species, thus refuting earlier assumptions that cheetahs show only little population differentiation. Our genome-wide nuclear data indicate that cheetahs from East Africa may be more closely related to A. j. soemmeringii than they are to A. j. jubatus. This supports the need for further research on the classification of cheetah subspecies, as East African cheetahs are currently included in the Southern Africa subspecies, A. j. jubatus. We detected stronger inbreeding in individuals of the Critically Endangered A. j. venaticus (Iran) and A. j. hecki (Northwest Africa), and show that overall genome-wide heterozygosity in cheetah is lower than that reported for other threatened and endangered felids, such as tigers and lions. Furthermore, we show that MHC class II diversity in cheetahs is generally higher than previously reported, but still lower than in other felids. Our results provide new and important information for efficient genetic monitoring, subspecies assignments and evidence-based conservation policy decisions.

evolutionary biology↗