Endangered island endemic plants have vulnerable genomes

Genome Sequencing of the Endangered Kingdonia uniflora (Circaeasteraceae, Ranunculales) Reveals Potential Mechanisms of Evolutionary Specialization.

Many endangered species suffer from the loss of genetic diversity, but some populations may be able to thrive even if genetically depleted. To investigate the underlying genetic processes of population bottlenecks, we apply an innovative approach for assessing genetic diversity in the last known population of the endangered Pale-headed Brushfinch (Atlapetes pallidiceps) in Ecuador. First, we measure genetic diversity at eleven neutral microsatellite loci and adaptive SNP variation in five Toll-like receptor (TLR) immune system genes. Bottleneck tests confirm genetic drift as the main force shaping genetic diversity in this species and indicate a 99 % reduction in population size dating back several hundred years. Second, we compare contemporary microsatellite diversity with historic museum samples of A. pallidiceps, finding no change in genetic diversity. Third, we compare genetic diversity in the Pale-headed Brushfinch with two co-occurring-related brushfinch species (Atlapetes latinuchus, Buarremon torquatus), finding a reduction of up to 91% diversity in the immune system genes but not in microsatellites. High TLR diversity is linked to decreased survival probabilities in A. pallidiceps. Low TLR diversity is thus probably an adaptation to the specific selection regime within its currently very restricted distribution (approximately 200 ha), but could severely restrict the adaptive potential of the species in the long run. Our study illustrates the importance of investigating both neutral and adaptive markers to assess the effect of population bottlenecks and for recommending specific management plans in endangered species.

Loss of genetic diversity increases the risk of extinction of a population through inbreeding depression. In addition, the number of deleterious genetic variations, which might accumulate in a small population through genetic drift, can also make the population vulnerable. Rhododendron boninense is a critically endangered azalea species, which grows on the Bonin Islands, a UNESCO World Heritage Site; its population size in the wild dropped to only a single individual. Although a governmental program for species conservation has been conducted, no successful natural regeneration or population growth was achieved. We hypothesized that the reduced genetic diversity and accumulated deleterious genetic variation might cause the vulnerability of the species, and conducted comparative genetic and genomic analyses between R. boninense and its congeners. Genetic analysis using microsatellite markers indicated that the genetic diversity of R. boninense was ultimately low; microsatellite loci of this species were all fixed, whereas the congeners maintain high allelic diversity. Based on comprehensive transcriptome analysis, the amount of deleterious variation of R. boninense was significantly greater than that of R. amanoi. Repeated generation transitions of the small population of R. boninense on the oceanic islands is likely to have resulted in low genetic diversity as well as more deleterious variations in the genome, and we speculated that the accumulated deleterious variation might result in vulnerability of R. boninense. This study indicates the possibility of evaluating the feasibility of effective conservation programs based on the genetic diversity and the amount of accumulated deleterious variation in the genome of critically endangered species.

Anthropogenic habitat loss and climate change are reducing species' geographic ranges, increasing extinction risk and losses of species' genetic diversity. Although preserving genetic diversity is key to maintaining species' adaptability, we lack predictive tools and global estimates of genetic diversity loss across ecosystems. We introduce a mathematical framework that bridges biodiversity theory and population genetics to understand the loss of naturally occurring DNA mutations with decreasing habitat. By analyzing genomic variation of 10,095 georeferenced individuals from 20 plant and animal species, we show that genome-wide diversity follows a mutations-area relationship power law with geographic area, which can predict genetic diversity loss from local population extinctions. We estimate that more than 10% of genetic diversity may already be lost for many threatened and nonthreatened species, surpassing the United Nations' post-2020 targets for genetic preservation.

While metapopulation theory offers tractable means to understand extinction risks for patchily-distributed endangered species, real systems often feature discrepant patch quality and accessibility, complex influences of environmental stochasticity, and regional and temporal autocorrelation. Spatially structured metapopulation models are flexible and can use real data but often at the cost of generality. Particularly as resources for management of such species are often critically limited, endangered species management guided by metapopulation modeling requires incorporation of biological realism. Here we developed a flexible, stochastic spatially structured metapopulation model of the profoundly endangered Amargosa vole, a microtine rodent with an extant population of only a few hundred individuals within 1km2 of habitat in the Mojave Desert. Drought and water insecurity are increasing extinction risks considerably. We modelled subpopulation demographics using a Ricker-like model with migration implemented in an incidence function metapopulation model. A set of scenarios was used to assess the effect of anthropogenic stressors or management actions on expected time to extinction (Te) including: 1) wildland fire, 2) anthropogenically-mediated losses of hydrologic flows, 3) drought, 4) intentional expansion of existing patches into ‘megamarshes’ (i.e. via restoration/enhancement), and 5) additive impacts of multiple influences. In isolation, marshes could be sources or sinks, but spatial context within the full metapopulation including adjacency could alter relative impacts of subpopulations on all other subpopulations. The greatest reductions in persistence occurred in scenarios simulated with impacts from drought in combination with fire or anthropogenically-mediated losses of hydrologic flows. Optimal actions to improve persistence were to prevent distant and smaller marshes from acting as sinks through strategic creation of megamarshes that act as sources of voles and stepping-stones. This research reinforces that management resources expended without guidance from empirically-based modeling can actually harm species’ persistence. This metapopulation-PVA tool could easily be implemented for other patchily-distributed endangered species and allow managers to maximize scarce resources to improve the likelihood of endangered species persistence.

Biodiversity indices often combine data from different species when used in monitoring programs. Heuristic properties can suggest preferred indices, but we lack objective ways to discriminate between indices with similar heuristics. Biodiversity indices can be evaluated by determining how well they reflect management objectives that a monitoring program aims to support. For example, the Convention on Biological Diversity requires reporting about extinction rates, so simple indices that reflect extinction risk would be valuable. We developed 3 biodiversity indices that are based on simple models of population viability that relate extinction risk to abundance. We based the first index on the geometric mean abundance of species and the second on a more general power mean. In a third index, we integrated the geometric mean abundance and trend. These indices require the same data as previous indices, but they also relate directly to extinction risk. Field data for butterflies and woodland plants and experimental studies of protozoan communities show that the indices correlate with local extinction rates. Applying the index based on the geometric mean to global data on changes in avian abundance suggested that the average extinction probability of birds has increased approximately 1% from 1970 to 2009.Conectando Índices para el Monitoreo de la Biodiversidad con la Teoría de Riesgo de ExtinciónResumenLos índices de biodiversidad combinan frecuentemente los datos de diferentes especies cuando se usan en los programas de monitoreo. Las propiedades heurísticas pueden sugerir índices preferidos, pero carecemos de medios objetivos para discriminar a los índices con propiedades heurísticas similares. Los índices de biodiversidad pueden evaluarse al determinar qué tan bien reflejan los objetivos de manejo que un programa de monitoreo busca apoyar. Por ejemplo, la Convención sobre la Diversidad Biológica requiere reportar las tasas de extinción, así que los índices que reflejan el riesgo de extinción serían valiosos. Desarrollamos 3 índices de biodiversidad que se basan en modelos sencillos de viabilidad de población y que relacionan el riesgo de extinción con la abundancia. Basamos el primer índice en la media geométrica de la abundancia de especies, y el segundo en una media de poder más general. En el tercer índice integramos la media geométrica y la tendencia. Estos índices requieren los mismos datos que índices previos, pero también se relacionan directamente con el riesgo de extinción. La información de campo sobre mariposas y plantas de bosque, y los estudios experimentales de comunidades protozoarias, muestran que los índices se correlacionan con las tasas locales de extinción. Al aplicar el índice basado en la media geométrica sobre los datos globales de los cambios en la abundancia de aves, sugirió que la probabilidad de extinción promedio de aves ha incrementado aproximadamente 1% desde 1970 hasta 2009.Palabras ClaveÍndice de biodiversidad, media geométrica, medida de la biodiversidad, riesgo de extinción

Extinction of island endemics: it is not inbreeding depression

The identification of areas of high priority for conservation is becoming a major endeavor for conservation biologists. Regions of high species richness and high concentrations of endemic and endangered species have been considered a priority for conservation. In this paper we use information about the species richness, composition, and distribution of mammals from Mexico for selecting priority areas for conservation. All species of terrestrial mammals were characterized by geographic range size, body mass, and conservation status, and their distributions were overlaid on a 2° × 2° grid to detect areas of high concentrations of species richness, endemicity, and endangered species. We focused our analyses at both species and biogeographic levels. At the species level we examined differences among endangered, endemic, and non-endemic species in ecological characteristics correlated with vulnerability to extinction. There were significant differences between endangered and non-endangered species, and between endemic and non-endemic mammals in body size and geographic range size. At the biogeographic level simple correlation analyses were carried out to determine the relation between latitude, total species richness, number of endemic species, and number of endangered species. We found a very low correspondence among areas of high diversity, high endemicity, or high number of endangered species. The distribution of many species with restricted geographic ranges, including endemic and non-endemic species, did not coincide with areas of high species richness, endemicity, or endangerment. We suggest a conservation strategy that gives priority to areas of high concentration of endangered species and of non-endangered species with restricted distributions. Among endangered species a higher priority should be given to endemic taxa vs. non-endemic species, and to restricted species over widespread taxa in these two groups.

Habitat fragmentation reduces gene flow, causing genetic differentiation and diversity loss in endangered species through genetic drift and inbreeding. However, the impact of habitat fragmentation on ectomycorrhizal (ECM) fungi remains unexplored, despite their critical roles in forest ecosystems. Here, we investigated the population genetic structure and the demographic history of Rhizopogon togasawarius, the ECM fungus specifically colonizing the host tree Pseudotsuga japonica, across its entire distribution range (>200 km). These two species are designated as endangered species on the IUCN Red List since they are found only in small, fragmented forests in Japan. We analysed 236 R. togasawarius individuals from five remaining populations across the Kii Peninsula and the Shikoku Island, separated by a sea channel. Simple sequence repeat analyses using 20 loci revealed strong genetic differentiation among populations (FST = 0.255), even significant in the nearest population pair separated by a distance of only 8 km (FST = 0.075), indicating extremely limited gene flow between populations. DIYABC-RF analyses implied that population divergence occurred approximately 6000 generations ago between the two regions, and nearly 1500 generations ago between the nearest populations within Shikoku Island, related to past climate events. Because of prolonged genetic isolation, significant inbreeding was confirmed in four of five populations, where effective population sizes became very small (Ne = 9.0-58.0). Although evaluation of extinction risks for microorganisms is challenging, our conservation genetic results indicated that habitat fragmentation increases extinction risk through population genetic mechanisms, and therefore should not be overlooked in biodiversity conservation efforts.

Genetic diversity at a major histocompatibility complex (MHC) class II B gene was examined for two wild and three captive populations of the endangered Tokyo bitterling Tanakia tanago. A specific primer set was first developed to amplify the MHC II B exon 2 locus. Using single strand conformation polymorphism (SSCP) and sequencing analysis, 16 DAB3 alleles were detected with 56 nucleotide substitutions in the 276-bp region. In the putative antigen-binding sites of exon 2, the rate of nonsynonymous substitutions was significantly higher than that of synonymous substitutions (dN/dS = 2.79), indicating positive selection on the retention of polymorphism. The population from the Handa Natural Habitat Conservation Area and that from the Tone River system exhibited low variation (one and three alleles, respectively), whereas the captive population that originated from a mix of three distinct populations had the highest amounts of variation (14 alleles). The levels of heterozygosity at the MHC varied considerably among populations and showed significant correlations with those at putative neutral microsatellite markers, suggesting that genetic drift following a bottleneck has affected MHC variability in some populations. Comparisons between endangered and non-endangered fish species in previous reports and the present results indicate that the number of MHC alleles per population is on average 70% lower in endangered species than non-endangered species. Considering the functional consequence of this locus, attention should be paid to captive and wild endangered fish populations in terms of further loss of MHC alleles.

Due to substantial population decline and habitat fragmentation, the North African Afares oak (Quercus afares Pomel.) is currently vulnerable and highly threatened. Like many endangered species, Afares is susceptible to biological and anthropogenic threats that can lead to genetic diversity loss and, ultimately, a heightened risk of extinction. Therefore, assessing genetic diversity is imperative for informing conservation strategies. In this study, genetic diversity and structure of the extant Algerian populations of Q. afares were analyzed. Genetic diversity, population structure, as well as gene flow and potential bottleneck effects were estimated using 16 polymorphic nuclear microsatellite markers. We found an unexpectedly high level of genetic diversity (Ho = 0.64, He = 0.60, Ar = 7.16) across the studied localities for a threatened species with restricted distribution range. Moreover, there were high levels of gene flow based on pairwise genetic differentiation estimates and minimal genetic structuring, among the fragmented, outbreeding localities (Fis = −0.11, p ˃ 0.05) of Q. afares. Additionally, no correlation was found between genetic and geographical distances (Rxy = −0.29, p = 0.5). These findings suggest that Q. afares stands represent a metapopulation. Despite the high genetic diversity of Q. afares, local populations in each small habitat patch remain at risk of extinction due to habitat loss and increasing anthropogenic threats. To minimize further loss of genetic diversity and habitat degradation, effective protection measures should be applied to Q. afares forests in Algeria. Conservation efforts should focus on habitat management and raising awareness among residents neighboring Afares oak forests.

Intense and prolonged mortality caused by over-exploitation could drive the decay of genetic diversity which may lead to decrease species’ resilience to environmental changes, thus increasing their extinction risk. Swordfish is a high commercial value species, especially in the Mediterranean Sea, where it is affected by high catch levels. Mediterranean swordfish consist of a population genetically and biologically distinct from Atlantic ones and therefore managed as a separate stock. The last Mediterranean swordfish stock assessment reported that in the last forty years Mediterranean swordfish has been overfished and, to date, it is still subject to overfishing. A comparison between an available mitochondrial sequence dataset and a homologous current sample was carried out to investigate temporal genetic variation in the Mediterranean swordfish population over near twenty years. Our study provides the first direct measure of reduced genetic diversity for Mediterranean swordfish during a short period, as measured both in the direct loss of mitochondrial haplotypes and reduction in haplotype diversity. A reduction of the relative females’ effective population size in the recent sample has been also detected. The possible relationship between fishery activities and the loss of genetic diversity in the Mediterranean swordfish population is discussed.

Genetics and extinction

Inbreeding reduces survival and reproduction (i.e. it causes inbreeding depression), and thereby increases extinction risk. Inbreeding depression is due to increased homozygosity for harmful alleles and at loci exhibiting heterozygote advantage. Inbreeding depression is nearly universal in sexually reproducing organisms that are diploid or have higher ploidies. Impacts of inbreeding are generally greater in species that naturally outbreed than those that inbreed, in stressful than benign environments, and for fitness than peripheral traits. Harmful effects accumulate across the life cycle, resulting in devastating effects on total fitness in outbreeding species.Species face ubiquitous environmental change and must adapt or they will go extinct. Genetic diversity is the raw material required for evolutionary adaptation. However, loss of genetic diversity is unavoidable in small isolated populations, diminishing their capacity to evolve in response to environmental changes, and thereby increasing extinction risk.

Genetic approaches have proved valuable to the study and conservation of endangered populations, especially for monitoring programs, and there is potential for further developments in this direction by extending analyses to the genomic level. We assembled the genome of the wolverine (Gulo gulo), a mustelid that in Scandinavia has recently recovered from a significant population decline, and obtained a 2.42Gb draft sequence representing >85% of the genome and including >21,000protein-coding genes. We then performed whole-genome resequencing of 10Scandinavian wolverines for population genomic and demographic analyses. Genetic diversity was among the lowest detected in a red-listed population (mean genome-wide nucleotide diversity of 0.05%). Results of the demographic analyses indicated a long-term decline of the effective population size (Ne ) from 10,000well before the last glaciation to <500 after this period. Current Ne appeared even lower. The genome-wide FIS level was 0.089 (possibly signaling inbreeding), but this effect was not observed when analyzing a set of highly variable SNP markers, illustrating that such markers can give a biased picture of the overall character of genetic diversity. We found significant population structure, which has implications for population connectivity and conservation. We used an integrated microfluidic circuit chip technology to develop an SNP-array consisting of 96 highly informative markers that, together with a multiplex pre-amplification step, was successfully applied to low-quality DNA from scat samples. Our findings will inform management, conservation, and genetic monitoring of wolverines and serve as a genomic roadmap that can be applied to other endangered species. The approach used here can be generally utilized in other systems, but we acknowledge the trade-off between investing in genomic resources and direct conservation actions.