Genomics reveals introgression and purging of deleterious mutations in the Arabian leopard (Panthera pardus nimr)

In endangered species, low-genetic variation and inbreeding result from recent population declines. Genetic screenings in endangered populations help to assess their vulnerability to extinction and to create informed management actions toward their conservation efforts. The leopard, Panthera pardus, is a highly generalist predator with currently eight different subspecies. Yet, genomic data are still lacking for the Critically Endangered Arabian leopard (P. p. nimr). Here, we sequenced the whole genome of two Arabian leopards and assembled the most complete genomic dataset for leopards to date. Our phylogenomic analyses show that leopards are divided into two deeply divergent clades: the African and the Asian. Conservation genomic analyses indicate a prolonged population decline, which has led to an increase in inbreeding and runs of homozygosity, with consequent purging of deleterious mutations in both Arabian individuals. Our study represents the first attempt to genetically inform captive breeding programmes for this Critically Endangered subspecies

Targeted conservation genetics of the endangered chimpanzee

Populations of the common chimpanzee (Pan troglodytes) are in an impending risk of going extinct in the wild as a consequence of damaging anthropogenic impact on their natural habitat and illegal pet and bushmeat trade. Conservation management programmes for the chimpanzee have been established outside their natural range (ex situ), and chimpanzees from these programmes could potentially be used to supplement future conservation initiatives in the wild (in situ). However, these programmes have often suffered from inadequate information about the geographical origin and subspecies ancestry of the founders. Here, we present a newly designed capture array with ~60,000 ancestry informative markers used to infer ancestry of individual chimpanzees in ex situ populations and determine geographical origin of confiscated sanctuary individuals. From a test panel of 167 chimpanzees with unknown origins or subspecies labels, we identify 90 suitable non-admixed individuals in the European Association of Zoos and Aquaria (EAZA) Ex situ Programme (EEP). Equally important, another 46 individuals have been identified with admixed subspecies ancestries, which therefore over time, should be naturally phased out of the breeding populations. With potential for future re-introduction to the wild, we determine the geographical origin of 31 individuals that were confiscated from the illegal trade and demonstrate the promises of using non-invasive sampling in future conservation action plans. Collectively, our genomic approach provides an exemplar for ex situ management of endangered species and offers an efficient tool in future in situ efforts to combat the illegal wildlife trade.PF is supported by the Innovation Fund Denmark doctoral fellowship programme and the Candys Foundation. CF is supported by “la Caixa” doctoral fellowship programme. TSK is funded by Carlsberg grant CF19-0712 prepared within the framework of the HSE University Basic Research Program. TMB is supported by BFU2017-86471-P (MINECO/FEDER, UE), U01 MH106874 grant, Howard Hughes International Early Career, Obra Social “La Caixa” and Secretaria d’Universitats i Recerca and CERCA Programme del Departament d’Economia i Coneixement de la Generalitat de Catalunya (GRC 2017 SGR 880). EL is supported by CGL2017-82654-P (MINECO/FEDER, UE).Peer reviewe

Insights from the rescue and breeding management of Cuvier’s gazelle (Gazella cuvieri) through whole-genome sequencing

Captive breeding programmes represent the most intensive type of ex situ population management for threatened species. One example is the Cuvier’s gazelle programme that started in 1975 with only four founding individuals, and after more than four decades of management in captivity, a reintroduction effort was undertaken in Tunisia in 2016, to establish a population in an area historically included within its range. Here, we aim to determine the genetic consequences of this reintroduction event by assessing the genetic diversity of the founder stock as well as of their descendants. We present the first whole-genome sequencing dataset of 30 Cuvier’s gazelles including captive-bred animals, animals born in Tunisia after a reintroduction and individuals from a genetically unrelated Moroccan population. Our analyses revealed no difference between the founder and the offspring cohorts in genome-wide heterozygosity and inbreeding levels, and in the amount and length of runs of homozygosity. The captive but unmanaged Moroccan gazelles have the lowest genetic diversity of all genomes analysed. Our findings demonstrate that the Cuvier’s gazelle captive breeding programme can serve as source populations for future reintroductions of this species. We believe that this study can serve as a starting point for global applications of genomics to the conservation plan of this species.K-P. Koepfli and B. Pukazhenthi acknowledge the Sichel Endowment Fund for research support on dama gazelle genomics. M.A.E. is supported by an FPI (Formación de Personal Investigador) PRE2018-083966 from Ministerio de Ciencia, Universidades e Investigación. P.D. was supported as a postdoctoral fellow by the Smithsonian Institution Fellowship Program. K.-P.K. was supported by funding from the Smithsonian Institution's George E. Burch Fellowship in Theoretical Medicine and Affiliated Theoretical Science. T.M.-B. is supported by funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement No. 864203), BFU2017-86471-P (MINECO/FEDER, UE), ‘Unidad de Excelencia María de Maeztu’, funded by the AEI (CEX2018-000792-M), Howard Hughes International Early Career and Secretaria d’Universitats i Recerca and CERCA Programme del Departament d’Economia i Coneixement de la Generalitat de Catalunya (GRC 2017 SGR 880). E.M. received financial support from the project PGC2018-097426-B-C22 (Spanish Ministry of Universities. Spanish State Research Agency. FEDER Program, European Union). E.L. is supported by CGL2017-82654-P (MINECO/FEDER, UE).Peer reviewe

Historic sampling of a vanishing beast: Population structure and diversity in the Black Rhinoceros

The black rhinoceros (Diceros bicornis L.) is a critically endangered species historically distributed across sub-Saharan Africa. Hunting and habitat disturbance have diminished both its numbers and distribution since the 19th century, but a poaching crisis in the late 20th century drove them to the brink of extinction. Genetic and genomic assessments can greatly increase our knowledge of the species and inform management strategies. However, when a species has been severely reduced, with the extirpation and artificial admixture of several populations, it is extremely challenging to obtain an accurate understanding of historic population structure and evolutionary history from extant samples. Therefore, we generated and analyzed whole genomes from 63 black rhinoceros museum specimens collected between 1775 and 1981. Results showed that the black rhinoceros could be genetically structured into six major historic populations (Central Africa, East Africa, Northwestern Africa, Northeastern Africa, Ruvuma, and Southern Africa) within which were nested four further subpopulations (Maasailand, southwestern, eastern rift, and northern rift), largely mirroring geography, with a punctuated north–south cline. However, we detected varying degrees of admixture among groups and found that several geographical barriers, most prominently the Zambezi River, drove population discontinuities. Genomic diversity was high in the middle of the range and decayed toward the periphery. This comprehensive historic portrait also allowed us to ascertain the ancestry of 20 resequenced genomes from extant populations. Lastly, using insights gained from this unique temporal data set, we suggest management strategies, some of which require urgent implementation, for the conservation of the remaining black rhinoceros diversity

Real-time genomics for One Health

The ongoing degradation of natural systems and other environmental changes has put our society at a crossroad with respect to our future relationship with our planet. While the concept of One Health describes how human health is inextricably linked with environmental health, many of these complex interdependencies are still not well-understood. Here, we describe how the advent of real-time genomic analyses can benefit One Health and how it can enable timely, in-depth ecosystem health assessments. We introduce nanopore sequencing as the only disruptive technology that currently allows for real-time genomic analyses and that is already being used worldwide to improve the accessibility and versatility of genomic sequencing. We showcase real-time genomic studies on zoonotic disease, food security, environmental microbiome, emerging pathogens, and their antimicrobial resistances, and on environmental health itself – from genomic resource creation for wildlife conservation to the monitoring of biodiversity, invasive species, and wildlife trafficking. We stress why equitable access to real-time genomics in the context of One Health will be paramount and discuss related practical, legal, and ethical limitations

Population dynamics and genetic connectivity in recent chimpanzee history

The European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement no. 864203) (to T.M.-B.). BFU2017-86471-P (MINECO/FEDER, UE) (to T.M.-B.). “Unidad de Excelencia María de Maeztu”, funded by the AEI (CEX2018-000792-M) (to T.M.-B.). Howard Hughes International Early Career (to T.M.-B.). NIH 1R01HG010898-01A1 (to T.M.-B.). Secretaria d’Universitats i Recerca and CERCA Program del Departament d’Economia i Coneixement de la Generalitat de Catalunya (GRC 2017 SGR 880) (to T.M.-B.). UCL’s Wellcome Trust ISSF3 award 204841/Z/16/Z (to A.M.A. and J.M.S.). Generalitat de Catalunya (2017 SGR-1040) (to M. Llorente). Wellcome Trust Investigator Award 202802/Z/16/Z (to D.A.H.). The Pan African Program: The Cultured Chimpanzee (PanAf) is generously funded by the Max Planck Society, the Max Planck Society Innovation Fund, and the Heinz L. Krekeler Foundation.Knowledge on the population history of endangered species is critical for conservation, but whole-genome data on chimpanzees (Pan troglodytes) is geographically sparse. Here, we produced the first non-invasive geolocalized catalog of genomic diversity by capturing chromosome 21 from 828 non-invasive samples collected at 48 sampling sites across Africa. The four recognized subspecies show clear genetic differentiation correlating with known barriers, while previously undescribed genetic exchange suggests that these have been permeable on a local scale. We obtained a detailed reconstruction of population stratification and fine-scale patterns of isolation, migration, and connectivity, including a comprehensive picture of admixture with bonobos (Pan paniscus). Unlike humans, chimpanzees did not experience extended episodes of long-distance migrations, which might have limited cultural transmission. Finally, based on local rare variation, we implement a fine-grained geolocalization approach demonstrating improved precision in determining the origin of confiscated chimpanzees.Publisher PDFPeer reviewe

Genomic analysis of wild and captive chimpanzee populations from non-invasive samples using target capture methods

Tesis llevada a cabo para conseguir el grado de Doctor por la Universidad Pompeu Fabra.--2020-12-17.--Genética[EN] Wild chimpanzee populations are considered to be under threat of extinction due to the damaging consequences of human impact into their natural habitat and illegal trade. Conservation genomics is an emerging field that has the potential to guide conservation efforts not only in the wild (in situ) but also outside their natural range (ex situ). In this thesis, we have explored to which extent target capture methods on specific genomic regions can provide insights into chimpanzee genetic diversity in captive and wild populations. Specifically, we have characterized the ancestry and inbreeding of 136 European captive chimpanzees to aid their management in captivity and inferred the origin of 31 confiscated individuals from illegal trade by sequencing ancestry informative SNPs. Also, we have examined molecular strategies to maximize the library complexity in target capture methods from fecal samples so they can be applied in large-scale genomic studies. Finally, we have captured the chromosome 21 from 828 fecal samples collected across the entire extant chimpanzee range. As a result of our high density sampling scheme, we have found strong evidence of population stratification in chimpanzee populations and we have discovered new local genetic diversity that is linked to its geographic origin. Finally, with this newly generated dataset and fine-grained geogenetic map, we have implemented a strategy for the geolocalization of chimpanzees which has a direct conservation application[CA] Les poblacions salvatges de ximpanzés estan en perill d'extinció a causa de les dramàtiques conseqüències associades a l’impacte humà en el seu hàbitat natural i al tràfic il·legal. La genòmica de la conservació és un camp emergent que té el potencial de guiar esforços de conservació d’espècies en perill d’extinció no només en el seu hàbitat natural (in situ) sinó també en captivitat (ex situ). En aquesta tesi, hem analitzat fins a quin punt els mètodes de captura de regions específiques del genoma són una bona eina per explorar la diversitat genètica dels ximpanzés tant en poblacions captives com salvatges. Concretament, hem caracteritzat la subespècie i els nivells de consanguinitat de 136 ximpanzés de zoos europeus amb l'objectiu de guiar-ne la seva gestió en captivitat, i hem inferit l'origen de 31 individus confiscats del tràfic il·legal a través de la seqüenciació de SNPs informatius de llinatge. També hem posat en pràctica estratègies moleculars per maximitzat la complexitat de les llibreries en la captura de regions específiques a partir de mostres fecals i així poder ser aplicades en estudis genòmics a gran escala. Finalment, hem capturat el cromosoma 21 de 828 mostres fecals recollides per tota la distribució geogràfica dels ximpanzé. Arran de l’alta densitat de mostreig, hem trobat evidències que apunten a una alta estratificació poblacional en els ximpanzés i hem desxifrat nova diversitat genètica vinculada a l’origen geogràfic dels individus. Finalment, amb el conjunt de dades generat i el mapa geogenètic obtingut, hem implementat una estratègia per la geolocalització de ximpanzés amb aplicació directe per a la conservació

Admixture in mammals and how to understand its functional implications: on the abundance of gene flow in mammalian species, its impact on the genome, and roads into a functional understanding

Admixture, the genetic exchange between differentiated populations appears to be common in the history of species, but has not yet been comparatively studied across mammals. This limits the understanding of its mechanisms and potential role in mammalian evolution. The authors want to summarize the current knowledge on admixture in non-human primates, and suggest that it is important to establish a comparative framework for this phenomenon in humans. Genetic observations in domesticated mammals and their wild counterparts are discussed, and a brief global overview on other clades is presented. Based on this, some of the consequences of gene flow, including incompatibilities and their genomic footprint, as well as adaptive introgression are discussed, and suggestions for a functional genomics approach are made. It is proposed that the field is moving beyond descriptive observations in single species, to a comprehensive analysis of admixture and its impact. Admixture is becoming an integral part of mammalian evolution.C.F. was supported by the “La Caixa” doctoral fellowship programme. T.M.‐B. was supported by BFU2017‐86471‐P (MINECO/FEDER, UE), U01 MH106874 grant, the Howard Hughes International Early Career, Obra Social “La Caixa” and Secretaria d'Universitats i Recerca, and CERCA Programme del Departament d'Economia i Coneixement de la Generalitat de Catalunya (GRC 2017 SGR 880). The project that gave rise to these results received the support of a fellowship from “la Caixa” Foundation (ID 100010434). The fellowship code is LCF/BQ/PR19/11700002

Demographic history and population structure of chimpanzees (Pan troglodytes) with implacations for global conservation strategies

Frandsen, Peter et al.-- Trabajo presentado en la Annual Meeting of the Society for Molecular Biology and Evolution (SMBE 2016), celebrada en Gold Coast (Queensland, Australia) del 3 al 7 de julio de 2016.Large-scale population genomics have recently provided novel insight to the diversity and evolutionary history of the great apes, including our own closest living relative, the chimpanzee. However, limited by a lack of precise geographical information, our knowledge on the local demographic history and fine-scale population structure of chimpanzees is still incomplete. Such knowledge is crucial when setting future conservation strategies for chimpanzees, both in situ and ex situ.To fill this knowledge gap, we have analyzed a comprehensive dataset of 60 wild born chimpanzee genomes, covering all four subspecies sampled across their natural distribution range. From this project, we present an unpreceded fine scale inference of complex demographic histories and a tight link between geography and local layers of genetic population structure. Apart from valuable insights to the local evolutionary past of the chimpanzee, these findings have allowed us to ide ntify ancestry informative markers (AIM). We will show how this panel of AIMs can be used to re-assign confiscated individuals to their geographical origin, demonstrating a novel tool to combat illegal trafficking of chimpanzees along with the means to provide an accurate genetic guidance for global ex situ conservation management plans.N