Showing papers by "Stephen J. O'Brien published in 2022"

A decade of GigaScience: A perspective on conservation genetics

Abstract: Abstract Wide interest in species conservation is young. To many it began early in 1903 when Teddy Roosevelt and John Muir set up a camp under the Grizzly Giant in the Mariposa Grove of California's Yosemite Valley. Over three days they decided to broaden the US National Park footprint across the USA. Conservationists were inspired in the coming decades by the writings of wildlife conservation pioneers—Osa Johnson (I Married Adventure), Karen Blixen (Out of Africa) and Rachel Carson (The Silent Spring). Countless crusaders developed a passion for preserving dwindling species in those early days, yet none of these conservation advocates mentioned the word genetics, let alone genomics. The genome sequencing projects that have followed on from these have brought in an enormous amount of data, including whole genome sequences for thousands of non-human species, both individual and population wide. This huge resource has revolutionized conservation genetics, bringing in ways to assess the health of at-risk populations, devise genetic-driven breeding strategies, and other means to attempt to preserve the over 1 million species (and growing) under threat today.

Ancient DNA Reveals China as a Historical Genetic Melting Pot in Tiger Evolution

Abstract: The contrast between the tiger’s (Panthera tigris) 2-3 My age and extant tigers’ coalescence approximately 110,000 years ago suggests an ancient demographic bottleneck. Here we collected over 60 extinct specimens across mainland Asia and generated whole genome sequences from a 10,600-year-old Russian Far East (RFE) specimen (RUSA21, 8ξ coverage), 14 South China tigers (0.1-12ξ), three Caspian tigers (4-8ξ), plus 17 new mitogenomes. RUSA21 clustered within modern Northeast Asian phylogroups and partially derived from an extinct Late Pleistocene lineage. While some 8,000-10,000-year-old RFE mitogenomes are basal to all tigers, one 2,000-year-old specimen resembles present Amur tigers. The Caspian tiger likely dispersed from an ancestral Northeast Asian population and experienced gene flow from southern Bengal tigers. Lastly, genome-wide monophyly supported the South China tiger as a distinct subspecies, albeit with mitochondrial paraphyly, hence resolving its longstanding taxonomic controversy. The distribution of mitochondrial haplogroups corroborated by biogeographical modeling suggested Southwest China was a Late Pleistocene refugium for a relic basal lineage. As suitable habitat returned, Eastern China became a genetic melting pot to foster divergent lineages to merge into South China tigers and other subsequent northern subspecies to develop. Genomic information retrieved from ancient tigers hence sheds light on the species’ full evolutionary history leading to nine modern subspecies and resolves the natural history of surviving tigers.

The Pioneer Advantage: Filling the blank spots on the map of genome diversity in Europe

Abstract: Abstract Documenting genome diversity is important for the local biomedical communities and instrumental in developing precision and personalized medicine. Currently, tens of thousands of whole-genome sequences from Europe are publicly available, but most of these represent populations of developed countries of Europe. The uneven distribution of the available data is further impaired by the lack of data sharing. Recent whole-genome studies in Eastern Europe, one in Ukraine and one in Russia, demonstrated that local genome diversity and population structure from Eastern Europe historically had not been fully represented. An unexpected wealth of genomic variation uncovered in these studies was not so much a consequence of high variation within their population, but rather due to the “pioneer advantage.” We discovered more variants because we were the first to prospect in the Eastern European genome pool. This simple comparison underscores the importance of removing the remaining geographic genome deserts from the rest of the world map of the human genome diversity.

Taxonomic species recognition should be consistent

Abstract: Criteria for species naminghave been contentious since the time of Carl Linnaeus. With no clear ‘right or wrong’ convention for species naming, biologists strive to simply convince their peers. ThisNSR compendiumoffers detailed guidance [1–6] that adds quantitative genomic inference to the cacophony. Certain taxonomic assemblages (e.g. mammals, fish, fungi, insects, terrestrial and marine invertebrates, plants, bacteria) are sufficiently distinctive that any generalization is fraught with natural exceptions. The biological species concept (BSC), which became the default species definition over 30 different species concepts, defines species as ‘groups of actually or potentially interbreeding populations that are reproductively isolated from other such groups’ [7]. Our opinions derive from decades of molecular genetic research on the∼40 species of the Felidae and othermammals. The cats enjoy a rich paleontological record, morphometric details, extensive ecology, natural history lore, and a robust molecular phylogeny [8–11]. Combining well-accepted species distinctions (lion-tiger, cheetah-puma, leopard-jaguars, ocelotsmargay, each complying with the BSC criteria of reproductive isolation) we compared multiple corelative criteria to specify novel species. In nominating new species of the clouded leopard, orangutan, elephant and pampas cat, we reported synapomorphic molecular, morphological and cytogenetic traits, distinct nucleotide single nucleotide polymorphisms (SNPs) and microsatellite alleles [12–15]. The new species display reciprocal monophyly, genetic distance corresponding to 1–4 MYA, a high fraction of molecular variance between species, reduced gene flow, and localized hybrid zones. These species identifications have held up with IUCN (the International Union for Conservation of Nature), CITES (the Convention on International Trade in Endangered Species of Wild Fauna and Flora), ESA (the Endangered Species Act), zoo displays and numerous other classifications. Speciation is clearly a dynamic process and achieving reproductively isolated species status in mammals takes time, over a million years for most radiations [16]. With certain caveats, the species status using consistent correlates of the speciation process for these species seems to have been achieved and become widely accepted. Subspecies is another matter. The subspecies concept itself is controversial. Originally specified by Charles Darwin, subspecies protection has been adopted by theUSFish andWildlife Service, CITES and IUCN for categorizing endangered species and subspecies needing protection. O’Brien and Mayr defined subspecies as ‘a geographically distinct aggregate of local populations which differ taxonomically from other subdivisions of the species’ [17]. A subspecies has four possible fates: (i) extinction; (ii) connecting and interbreeding with another subspecies to become a new mixed subspecies; (iii) evolution into a new species; and (iv) staying the same [17]. Subspecies are generally distinguished by fixed genetic differences from other subspecies. The key point of designating subspecies is consistency of multiple distinctive criteria, since as for species, there is no right or wrong way to describe subspecies. We further elaborate this point in the Felidae. Robust genome-wide analyses parsed living tigers into six distinguished subspecies of equivalent genetic distance from eachother [18,19]. Yet a proposed revision of Felidae taxonomy ignored the molecular data and lumped all five mainland tiger subspecies into one subspecies, distinct from the Sumatran tiger subspecies [20]. The same revision [20] elevated the Chinese mountain cat, Felis silvestris bieti, to a full species designation Felis bieti, though it is clearly a subspecies of F. silvestris (the wildcat) equidistant from four other F. silvestris subspecies such as the Asiatic wildcat Felis silvestris ornata [21]. In Southeast Asia, the leopard cat Prionailurus bengalensis may reflect a case of ‘failed speciation’, in which two once-diverging Indochinese and Sundaic lineages reconnected, interbred and mixed on today’s Malay Peninsula [22]. Therefore, elevating them into two species as proposed [20] seems arbitrary and inconsistent. The inconsistencies here derive from embracing incorrect historical precedents or guesses, and from considering principally morphometric characters while ignoring transformative genomic analyses. Since morphological data are well known to be imprecise, even misleading in phylogenetic considerations [23], these taxonomic mis-classifications are prime examples of ill-informed taxonomic classification due to data denialism. The lessonhere is that considerationofmultiple independent measures/correlates of genetic differentiation leads to overall consistency for the taxonomic recognition of species. This is what we personally endorse, particularly in cases where dated fossils, morphology and molecular data are available, more and more the case in today’s genomic era.

In Memoriam: Diane R. O’Brien (1945–2021): Transformative Managing Editor—Journal of Heredity

Abstract: The world genetics community, the American Genetic Association (AGA), and countless dear friends and colleagues lost an amazing compassionate human being and champion of scientific publishing with the passing of Diane R. O’Brien on October 22, 2021 in her hometown of Frederick, Maryland. She was 76 years old (Figure 1). Diane was appointed Managing Editor of the Journal of Heredity alongside myself, her husband and life partner, as Editor, from 1987 to 2007. Her dedication, business acumen, prescience, and bright human spirit transformed the near broken AGA society to the strong and financially robust organization it is today. In a time before electronic submission and transmittal, Diane and I gathered a coterie of associate editors who would deliver manuscript reviews after charming telephone reminder from Diane at the AGA Office. Her management skills led to prompt reviews, and to loyalty to the Journal’s brand and mission of featuring organismal genetics advances as a prelude to the genomics era. Diane’s attention to fine detail, plus her knack in encouraging authors, reviewers, and science publication personnel, navigated the Journal of Heredity to its firm reputation as an interesting, timely, and influential genetics journal.