INTRODUCTION The Anthropocene is marked by an accelerated loss of biodiversity, widespread population declines, and a global conservation crisis. Given limited resources for conservation intervention, an approach is needed to identify threatened species from among the thousands lacking adequate information for status assessments. Such prioritization for intervention could come from genome sequence data, as genomes contain information about demography, diversity, fitness, and adaptive potential. However, the relevance of genomic data for identifying at-risk species is uncertain, in part because genetic variation may reflect past events and life histories better than contemporary conservation status. RATIONALE The Zoonomia multispecies alignment presents an opportunity to systematically compare neutral and functional genomic diversity and their relationships to contemporary extinction risk across a large sample of diverse mammalian taxa. We surveyed 240 species spanning from the “Least Concern” to “Critically Endangered” categories, as published in the International Union for Conservation of Nature’s Red List of Threatened Species. Using a single genome for each species, we estimated historical effective population sizes ( N e ) and distributions of genome-wide heterozygosity. To estimate genetic load, we identified substitutions relative to reconstructed ancestral sequences, assuming that mutations at evolutionarily conserved sites and in protein-coding sequences, especially in genes essential for viability in mice, are predominantly deleterious. We examined relationships between the conservation status of species and metrics of heterozygosity, demography, and genetic load and used these data to train and test models to distinguish threatened from nonthreatened species. RESULTS Species with smaller historical N e are more likely to be categorized as at risk of extinction, suggesting that demography, even from periods more than 10,000 years in the past, may be informative of contemporary resilience. Species with smaller historical N e also carry proportionally higher burdens of weakly and moderately deleterious alleles, consistent with theoretical expectations of the long-term accumulation and fixation of genetic load under strong genetic drift. We found weak support for a causative link between fixed drift load and extinction risk; however, other types of genetic load not captured in our data, such as rare, highly deleterious alleles, may also play a role. Although ecological (e.g., physiological, life-history, and behavioral) variables were the best predictors of extinction risk, genomic variables nonrandomly distinguished threatened from nonthreatened species in regression and machine learning models. These results suggest that information encoded within even a single genome can provide a risk assessment in the absence of adequate ecological or population census data. CONCLUSION Our analysis highlights the potential for genomic data to rapidly and inexpensively gauge extinction risk by leveraging relationships between contemporary conservation status and genetic variation shaped by the long-term demographic history of species. As more resequencing data and additional reference genomes become available, estimates of genetic load, estimates of recent demographic history, and accuracy of predictive models will improve. We therefore echo calls for including genomic information in assessments of the conservation status of species. Genomic information can help predict extinction risk in diverse mammalian species. Across 240 mammals, species with smaller historical N e had lower genetic diversity, higher genetic load, and were more likely to be threatened with extinction. Genomic data were used to train models that predict whether a species is threatened, which can be valuable for assessing extinction risk in species lacking ecological or census data. [Animal silhouettes are from PhyloPic]
more »
« less
The crucial role of genome-wide genetic variation in conservation
The unprecedented rate of extinction calls for efficient use of genetics to help conserve biodiversity. Several recent genomic and simulation-based studies have argued that the field of conservation biology has placed too much focus on conserving genome-wide genetic variation, and that the field should instead focus on managing the subset of functional genetic variation that is thought to affect fitness. Here, we critically evaluate the feasibility and likely benefits of this approach in conservation. We find that population genetics theory and empirical results show that conserving genome-wide genetic variation is generally the best approach to prevent inbreeding depression and loss of adaptive potential from driving populations toward extinction. Focusing conservation efforts on presumably functional genetic variation will only be feasible occasionally, often misleading, and counterproductive when prioritized over genome-wide genetic variation. Given the increasing rate of habitat loss and other environmental changes, failure to recognize the detrimental effects of lost genome-wide genetic variation on long-term population viability will only worsen the biodiversity crisis.
more » « less- NSF-PAR ID:
- 10305280
- Publisher / Repository:
- Proceedings of the National Academy of Sciences
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 118
- Issue:
- 48
- ISSN:
- 0027-8424
- Page Range / eLocation ID:
- Article No. e2104642118
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Despite an increased focus on multiscale relationships and interdisciplinary integration, few macroecological studies consider the contribution of genetic-based processes to landscape-scale patterns. We test the hypothesis that tree genetics, climate, and geography jointly drive continental-scale patterns of community structure, using genome-wide SNP data from a broadly distributed foundation tree species (Populus fremontii S. Watson) and two dependent communities (leaf-modifying arthropods and fungal endophytes) spanning southwestern North America. Four key findings emerged: (1) Tree genetic structure was a significant predictor for both communities; however, the strength of influence was both scale- and community-dependent. (2) Tree genetics was the primary driver for endophytes, explaining 17% of variation in continental-scale community structure, whereas (3) climate was the strongest predictor of arthropod structure (24%). (4) Power to detect tree genotype—community phenotype associations changed with scale of genetic organization, increasing from individuals to populations to ecotypes, emphasizing the need to consider nonstationarity (i.e., changes in the effects of factors on ecological processes across scales) when inferring macrosystem properties. Our findings highlight the role of foundation tree species as drivers of macroscale community structure and provide macrosystems ecology with a theoretical framework for linking fine- and intermediate-scale genetic processes to landscape-scale patterns. Management of the genetic diversity harbored within foundation species is a critical consideration for conserving and sustaining regional biodiversity.more » « less
-
more » « less
Abstract As urbanization continues to increase, it is expected that two‐thirds of the human population will reside in cities by 2050. Urbanization fragments and degrades natural landscapes, threatening wildlife including economically important species such as bees. In this study, we employ whole genome sequencing to characterize the population genetics, metagenome and microbiome, and environmental stressors of a common wild bee,
Ceratina calcarata . Population genomic analyses revealed the presence of low genetic diversity and elevated levels of inbreeding. Through analyses of isolation by distance, resistance, and environment across urban landscapes, we found that green spaces including shrubs and scrub were the most optimal pathways for bee dispersal, and conservation efforts should focus on preserving these land traits to maintain high connectivity across sites for wild bees. Metagenomic analyses revealed landscape sites exhibiting urban heat island effects, such as high temperatures and development but low precipitation and green space, had the highest taxa alpha diversity across all domains even when isolating for potential pathogens. Notably, the integration of population and metagenomic data showed that reduced connectivity in urban areas is not only correlated with lower relatedness among individuals but is also associated with increased pathogen diversity, exposing vulnerable urban bees to more pathogens. Overall, our combined population and metagenomic approach found significant environmental variation in bee microbiomes and nutritional resources even in the absence of genetic differentiation, as well as enabled the potential early detection of stressors to bee health. -
BACKGROUND Madagascar is one of the world’s foremost biodiversity hotspots. Its unique assemblage of plants, animals, and fungi—the majority of which evolved on the island and occur nowhere else—is both diverse and threatened. After human arrival, the island’s entire megafauna became extinct, and large portions of the current flora and fauna may be on track for a similar fate. Conditions for the long-term survival of many Malagasy species are not currently met because of multiple anthropogenic threats. ADVANCES We review the extinction risk and threats to biodiversity in Madagascar, using available international assessment data as well as a machine learning analysis to predict the extinction risks and threats to plant species lacking assessments. Our compilation of global International Union for Conservation of Nature (IUCN) Red List assessments shows that overexploitation alongside unsustainable agricultural practices affect 62.1 and 56.8% of vertebrate species, respectively, and each affects nearly 90% of all plant species. Other threats have a relatively minor effect today but are expected to increase in coming decades. Because only one-third (4652) of all Malagasy plant species have been formally assessed, we carried out a neural network analysis to predict the putative status and threats for 5887 unassessed species and to evaluate biases in current assessments. The percentage of plant species currently assessed as under threat is probably representative of actual numbers, except in the case of the ferns and lycophytes, where significantly more species are estimated to be threatened. We find that Madagascar is home to a disproportionately high number of Evolutionarily Distinct and Globally Endangered (EDGE) species. This further highlights the urgency for evidence-based and effective in situ and ex situ conservation. Despite these alarming statistics and trends, we find that 10.4% of Madagascar’s land area is protected and that the network of protected areas (PAs) covers at least part of the range of 97.1% of terrestrial and freshwater vertebrates with known distributions (amphibians, freshwater fishes, reptiles, birds, and mammal species combined) and 67.7% of plant species (for threatened species, the percentages are 97.7% for vertebrates and 79.6% for plants). Complementary to this, ex situ collections hold 18% of vertebrate species and 23% of plant species. Nonetheless, there are still many threatened species that do not occur within PAs and are absent from ex situ collections, including one amphibian, three mammals, and seven reptiles, as well as 559 plants and more yet to be assessed. Based on our updated vegetation map, we find that the current PA network provides good coverage of the major habitats, particularly mangroves, spiny forest, humid forest, and tapia, but subhumid forest and grassland-woodland mosaic have very low areas under protection (5.7 and 1.8% respectively). OUTLOOK Madagascar is among the world’s poorest countries, and its biodiversity is a key resource for the sustainable future and well-being of its citizens. Current threats to Madagascar’s biodiversity are deeply rooted in historical and present social contexts, including widespread inequalities. We therefore propose five opportunities for action to further conservation in a just and equitable way. First, investment in conservation and restoration must be based on evidence and effectiveness and be tailored to meet future challenges through inclusive solutions. Second, expanded biodiversity monitoring, including increased dataset production and availability, is key. Third, improving the effectiveness of existing PAs—for example through community engagement, training, and income opportunities—is more important than creating new ones. Fourth, conservation and restoration should not focus solely on the PA network but should also include the surrounding landscapes and communities. And finally, conservation actions must address the root causes of biodiversity loss, including poverty and food insecurity. In the eyes of much of the world, Madagascar’s biodiversity is a unique global asset that needs saving; in the daily lives of many of the Malagasy people, it is a rapidly diminishing source of the most basic needs for subsistence. Protecting Madagascar’s biodiversity while promoting social development for its people is a matter of the utmost urgency Visual representation of five key opportunities for conserving and restoring Madagascar’s rapidly declining biodiversity identified in this Review. The dashed lines point to representative vegetation types where these recommendations could have tangible effects, but the opportunities are applicable across Madagascar. ILLUSTRATION: INESSA VOETmore » « less
-
INTRODUCTION A major challenge in genomics is discerning which bases among billions alter organismal phenotypes and affect health and disease risk. Evidence of past selective pressure on a base, whether highly conserved or fast evolving, is a marker of functional importance. Bases that are unchanged in all mammals may shape phenotypes that are essential for organismal health. Bases that are evolving quickly in some species, or changed only in species that share an adaptive trait, may shape phenotypes that support survival in specific niches. Identifying bases associated with exceptional capacity for cellular recovery, such as in species that hibernate, could inform therapeutic discovery. RATIONALE The power and resolution of evolutionary analyses scale with the number and diversity of species compared. By analyzing genomes for hundreds of placental mammals, we can detect which individual bases in the genome are exceptionally conserved (constrained) and likely to be functionally important in both coding and noncoding regions. By including species that represent all orders of placental mammals and aligning genomes using a method that does not require designating humans as the reference species, we explore unusual traits in other species. RESULTS Zoonomia’s mammalian comparative genomics resources are the most comprehensive and statistically well-powered produced to date, with a protein-coding alignment of 427 mammals and a whole-genome alignment of 240 placental mammals representing all orders. We estimate that at least 10.7% of the human genome is evolutionarily conserved relative to neutrally evolving repeats and identify about 101 million significantly constrained single bases (false discovery rate < 0.05). We cataloged 4552 ultraconserved elements at least 20 bases long that are identical in more than 98% of the 240 placental mammals. Many constrained bases have no known function, illustrating the potential for discovery using evolutionary measures. Eighty percent are outside protein-coding exons, and half have no functional annotations in the Encyclopedia of DNA Elements (ENCODE) resource. Constrained bases tend to vary less within human populations, which is consistent with purifying selection. Species threatened with extinction have few substitutions at constrained sites, possibly because severely deleterious alleles have been purged from their small populations. By pairing Zoonomia’s genomic resources with phenotype annotations, we find genomic elements associated with phenotypes that differ between species, including olfaction, hibernation, brain size, and vocal learning. We associate genomic traits, such as the number of olfactory receptor genes, with physical phenotypes, such as the number of olfactory turbinals. By comparing hibernators and nonhibernators, we implicate genes involved in mitochondrial disorders, protection against heat stress, and longevity in this physiologically intriguing phenotype. Using a machine learning–based approach that predicts tissue-specific cis - regulatory activity in hundreds of species using data from just a few, we associate changes in noncoding sequence with traits for which humans are exceptional: brain size and vocal learning. CONCLUSION Large-scale comparative genomics opens new opportunities to explore how genomes evolved as mammals adapted to a wide range of ecological niches and to discover what is shared across species and what is distinctively human. High-quality data for consistently defined phenotypes are necessary to realize this potential. Through partnerships with researchers in other fields, comparative genomics can address questions in human health and basic biology while guiding efforts to protect the biodiversity that is essential to these discoveries. Comparing genomes from 240 species to explore the evolution of placental mammals. Our new phylogeny (black lines) has alternating gray and white shading, which distinguishes mammalian orders (labeled around the perimeter). Rings around the phylogeny annotate species phenotypes. Seven species with diverse traits are illustrated, with black lines marking their branch in the phylogeny. Sequence conservation across species is described at the top left. IMAGE CREDIT: K. MORRILLmore » « less
