Temporal dynamics of woolly mammoth genome erosion prior to extinction.

A number of species have recently recovered from near-extinction. Although these species have avoided the immediate extinction threat, their long-term viability remains precarious due to the potential genetic consequences of population declines, which are poorly understood on a timescale beyond a few generations. Woolly mammoths (Mammuthus primigenius) became isolated on Wrangel Island around 10,000 years ago and persisted for over 200 generations before becoming extinct around 4,000 years ago. To study the evolutionary processes leading up to the mammoths' extinction, we analyzed 21 Siberian woolly mammoth genomes. Our results show that the population recovered quickly from a severe bottleneck and remained demographically stable during the ensuing six millennia. We find that mildly deleterious mutations gradually accumulated, whereas highly deleterious mutations were purged, suggesting ongoing inbreeding depression that lasted for hundreds of generations. The time-lag between demographic and genetic recovery has wide-ranging implications for conservation management of recently bottlenecked populations.

Standard Deviations: The Biological Bases of Transmission Ratio Distortion.

The rule of Mendelian inheritance is remarkably robust, but deviations from the equal transmission of alternative alleles at a locus [a.k.a. transmission ratio distortion (TRD)] are also commonly observed in genetic mapping populations. Such TRD reveals locus-specific selection acting at some point between the diploid heterozygous parents and progeny genotyping and therefore can provide novel insight into otherwise-hidden genetic and evolutionary processes. Most of the classic selfish genetic elements were discovered through their biasing of transmission, but many unselfish evolutionary and developmental processes can also generate TRD. In this review, we describe methodologies for detecting TRD in mapping populations, detail the arenas and genetic interactions that shape TRD during plant and animal reproduction, and summarize patterns of TRD from across the genetic mapping literature. Finally, we point to new experimental approaches that can accelerate both detection of TRD and characterization of the underlying genetic mechanisms.

Detecting inbreeding depression in structured populations.

Measuring inbreeding and its consequences on fitness is central for many areas in biology including human genetics and the conservation of endangered species. However, there is no consensus on the best method, neither for quantification of inbreeding itself nor for the model to estimate its effect on specific traits. We simulated traits based on simulated genomes from a large pedigree and empirical whole-genome sequences of human data from populations with various sizes and structures (from the 1,000 Genomes project). We compare the ability of various inbreeding coefficients ([Formula: see text]) to quantify the strength of inbreeding depression: allele-sharing, two versions of the correlation of uniting gametes which differ in the weight they attribute to each locus and two identical-by-descent segments-based estimators. We also compare two models: the standard linear model and a linear mixed model (LMM) including a genetic relatedness matrix (GRM) as random effect to account for the nonindependence of observations. We find LMMs give better results in scenarios with population or family structure. Within the LMM, we compare three different GRMs and show that in homogeneous populations, there is little difference among the different [Formula: see text] and GRM for inbreeding depression quantification. However, as soon as a strong population or family structure is present, the strength of inbreeding depression can be most efficiently estimated only if i) the phenotypes are regressed on [Formula: see text] based on a weighted version of the correlation of uniting gametes, giving more weight to common alleles and ii) with the GRM obtained from an allele-sharing relatedness estimator.

The genome of the black-footed cat: Revealing a rich natural history and urgent conservation priorities for small felids.

Habitat degradation and loss of genetic diversity are common threats faced by almost all of today's wild cats. Big cats, such as tigers and lions, are of great concern and have received considerable conservation attention through policies and international actions. However, knowledge of and conservation actions for small wild cats are lagging considerably behind. The black-footed cat, Felis nigripes, one of the smallest felid species, is experiencing increasing threats with a rapid reduction in population size. However, there is a lack of genetic information to assist in developing effective conservation actions. A de novo assembly of a high-quality chromosome-level reference genome of the black-footed cat was made, and comparative genomics and population genomics analyses were carried out. These analyses revealed that the most significant genetic changes in the evolution of the black-footed cat are the rapid evolution of sensory and metabolic-related genes, reflecting genetic adaptations to its characteristic nocturnal hunting and a high metabolic rate. Genomes of the black-footed cat exhibit a high level of inbreeding, especially for signals of recent inbreeding events, which suggest that they may have experienced severe genetic isolation caused by habitat fragmentation. More importantly, inbreeding associated with two deleterious mutated genes may exacerbate the risk of amyloidosis, the dominant disease that causes mortality of about 70% of captive individuals. Our research provides comprehensive documentation of the evolutionary history of the black-footed cat and suggests that there is an urgent need to investigate genomic variations of small felids worldwide to support effective conservation actions.

Unraveling the genomic diversity and admixture history of captive tigers in the United States.

Genomic studies of endangered species have primarily focused on describing diversity patterns and resolving phylogenetic relationships, with the overarching goal of informing conservation efforts. However, few studies have investigated genomic diversity housed in captive populations. For tigers (Panthera tigris), captive individuals vastly outnumber those in the wild, but their diversity remains largely unexplored. Privately owned captive tiger populations have remained an enigma in the conservation community, with some believing that these individuals are severely inbred, while others believe they may be a source of now-extinct diversity. Here, we present a large-scale genetic study of the private (non-zoo) captive tiger population in the United States, also known as "Generic" tigers. We find that the Generic tiger population has an admixture fingerprint comprising all six extant wild tiger subspecies. Of the 138 Generic individuals sequenced for the purpose of this study, no individual had ancestry from only one subspecies. We show that the Generic tiger population has a comparable amount of genetic diversity relative to most wild subspecies, few private variants, and fewer deleterious mutations. We observe inbreeding coefficients similar to wild populations, although there are some individuals within both the Generic and wild populations that are substantially inbred. Additionally, we develop a reference panel for tigers that can be used with imputation to accurately distinguish individuals and assign ancestry with ultralow coverage (0.25×) data. By providing a cost-effective alternative to whole-genome sequencing (WGS), the reference panel provides a resource to assist in tiger conservation efforts for both ex- and in situ populations.

Demography and environment modulate the effects of genetic diversity on extinction risk in a butterfly metapopulation.

Linking genetic diversity to extinction is a common goal in genomic studies. Recently, a debate has arisen regarding the importance of genetic variation in conservation as some studies have failed to find associations between genome-wide genetic diversity and extinction risk. However, only rarely are genetic diversity and fitness measured together in the wild, and typically demographic history and environment are ignored. It is therefore difficult to infer whether a lack of an association is real or obscured by confounding factors. To address these shortcomings, we analyzed genetic data from 7,501 individuals with extinction data from 279 meadows and mortality of 1,742 larval nests in a butterfly metapopulation. We found a strong negative association between genetic diversity and extinction when considering only heterozygosity in models. However, this association disappeared when accounting for ecological covariates, suggesting a confounding between demography and genetics and a more complex role for heterozygosity in extinction risk. Modeling interactions between heterozygosity and demographic variables revealed that associations between extinction and heterozygosity were context-dependent. For example, extinction declined with increasing heterozygosity in large, but not currently small populations, although negative associations between heterozygosity, extinction, and mortality were detected in small populations with a recent history of decline. We conclude that low genetic diversity is an important predictor of extinction, predicting >25% increase in extinction beyond ecological factors in certain contexts. These results highlight that inferences about the importance of genetic diversity for population viability should not rely on genomic data alone but require investments in obtaining demographic and environmental data from natural populations.

Increased incidences of cervical ribs in deer indicate extinction risk.

Mammals as a rule have seven cervical vertebrae, a number which remains remarkably conserved. Occasional deviations of this number are usually due to the presence of cervical ribs on the seventh vertebra, indicating a homeotic transformation from a cervical rib-less vertebra into a thoracic rib-bearing vertebra. These transformations are often associated with major congenital abnormalities or pediatric cancers (pleiotropic effects) that are, at least in humans, strongly selected against. Based on data from Late Pleistocene mammoths (Mammuthus primigenius) and woolly rhinoceroses (Coelodonta antiquitatis) from the North Sea, we hypothesized that high incidences of cervical ribs in declining populations are due to inbreeding and/or adverse conditions impacting early pregnancies. In this study, we investigated the incidence of cervical ribs in an extinct Late Pleistocene megaherbivore, giant deer (Megaloceros giganteus) from Ireland and in the extant highly inbred Père David deer (Elaphurus davidianus) and in twenty other extant species. We show that the incidence of cervical ribs is exceptionally high in both the Irish giant deer and the Père David deer and much higher than in extant outbred deer. Our data support the hypothesis that inbreeding and genetic drift increase the frequencies of maladaptive alleles in populations at risk of extinction. The high incidence of cervical ribs indicates a vulnerable condition, which may have contributed to the extinction of megaherbivore species in the Late Pleistocene. We argue that cervical rib frequency may be a good proxy for extinction risk in inbred populations.

Demographic drivers of reproductive failure in a threatened bird: Insights from a decade of data.

Hatching failure affects up to 77% of eggs laid by threatened bird species, yet the true prevalence and drivers of egg fertilization failure versus embryo mortality as underlying mechanisms of hatching failure are unknown. Here, using ten years of data comprising 4,371 eggs laid by a population of a threatened bird, the hihi (Notiomystis cincta), we investigate the relative importance of infertility and embryo death as drivers of hatching failure and explore population-level factors associated with them. We show that of the 1,438 eggs that failed to hatch (33% of laid eggs) between 2010 and 2020, 83% failed due to embryo mortality, with the majority failing in the early stages of embryonic development. In the most comprehensive estimates of infertility rates in a wild bird population to date, we find that fertilization failure accounts for around 17% of hatching failure overall and is more prevalent in years where the population is smaller and more male biased. Male embryos are more likely to die during early development than females, but we find no overall effect of sex on the successful development of embryos. Offspring fathered by within-pair males have significantly higher inbreeding levels than extra-pair offspring; however, we find no effect of inbreeding nor extra-pair paternity on embryo mortality. Accurately distinguishing between infertility and embryo mortality in this study provides unique insight into the underlying causes of reproductive failure over a long-term scale and reveals the complex risks of small population sizes to the reproduction of threatened species.

Whole Genomes Inform Genetic Rescue Strategy for Montane Red Foxes in North America.

A few iconic examples have proven the value of facilitated gene flow for counteracting inbreeding depression and staving off extinction; yet, the practice is often not implemented for fear of causing outbreeding depression. Using genomic sequencing, climatic niche modeling, and demographic reconstruction, we sought to assess the risks and benefits of using translocations as a tool for recovery of endangered montane red fox (Vulpes vulpes) populations in the western United States. We demonstrated elevated inbreeding and homozygosity of deleterious alleles across all populations, but especially those isolated in the Cascade and Sierra Nevada ranges. Consequently, translocations would be expected to increase population growth by masking deleterious recessive alleles. Demographic reconstructions further indicated shallow divergences of less than a few thousand years among montane populations, suggesting low risk of outbreeding depression. These genomic-guided findings set the stage for future management, the documentation of which will provide a roadmap for recovery of other data-deficient taxa.

Measuring the Efficiency of Purging by non-random Mating in Human Populations.

Human populations harbor a high concentration of deleterious genetic variants. Here, we tested the hypothesis that non-random mating practices affect the distribution of these variants, through exposure in the homozygous state, leading to their purging from the population gene pool. To do so, we produced whole-genome sequencing data for two pairs of Asian populations exhibiting different alliance rules and rates of inbreeding, but with similar effective population sizes. The results show that populations with higher rates of inbred matings do not purge deleterious variants more efficiently. Purging therefore has a low efficiency in human populations, and different mating practices lead to a similar mutational load.