Ex situ conservation of two rare oak species using microsatellite and SNP markers.

Plant collections held by botanic gardens and arboreta are key components of ex situ conservation. Maintaining genetic diversity in such collections allows them to be used as resources for supplementing wild populations. However, most recommended minimum sample sizes for sufficient ex situ genetic diversity are based on microsatellite markers, and it remains unknown whether these sample sizes remain valid in light of more recently developed next-generation sequencing (NGS) approaches. To address this knowledge gap, we examine how ex situ conservation status and sampling recommendations differ when derived from microsatellites and single nucleotide polymorphisms (SNPs) in garden and wild samples of two threatened oak species. For Quercus acerifolia, SNPs show lower ex situ representation of wild allelic diversity and slightly lower minimum sample size estimates than microsatellites, while results for each marker are largely similar for Q. boyntonii. The application of missing data filters tends to lead to higher ex situ representation, while the impact of different SNP calling approaches is dependent on the species being analyzed. Measures of population differentiation within species are broadly similar between markers, but larger numbers of SNP loci allow for greater resolution of population structure and clearer assignment of ex situ individuals to wild source populations. Our results offer guidance for future ex situ conservation assessments utilizing SNP data, such as the application of missing data filters and the usage of a reference genome, and illustrate that both microsatellites and SNPs remain viable options for botanic gardens and arboreta seeking to ensure the genetic diversity of their collections.

Monitoring of species' genetic diversity in Europe varies greatly and overlooks potential climate change impacts.

Genetic monitoring of populations currently attracts interest in the context of the Convention on Biological Diversity but needs long-term planning and investments. However, genetic diversity has been largely neglected in biodiversity monitoring, and when addressed, it is treated separately, detached from other conservation issues, such as habitat alteration due to climate change. We report an accounting of efforts to monitor population genetic diversity in Europe (genetic monitoring effort, GME), the evaluation of which can help guide future capacity building and collaboration towards areas most in need of expanded monitoring. Overlaying GME with areas where the ranges of selected species of conservation interest approach current and future climate niche limits helps identify whether GME coincides with anticipated climate change effects on biodiversity. Our analysis suggests that country area, financial resources and conservation policy influence GME, high values of which only partially match species' joint patterns of limits to suitable climatic conditions. Populations at trailing climatic niche margins probably hold genetic diversity that is important for adaptation to changing climate. Our results illuminate the need in Europe for expanded investment in genetic monitoring across climate gradients occupied by focal species, a need arguably greatest in southeastern European countries. This need could be met in part by expanding the European Union's Birds and Habitats Directives to fully address the conservation and monitoring of genetic diversity.

Lessons from COP15 on effective scientific engagement in biodiversity policy processes.

The Kunming-Montreal Global Biodiversity Framework was adopted by parties to the Convention on Biological Diversity in December 2022. The aftermath of these negotiations provides an opportunity to draw lessons as to how ecological and evolutionary science can more effectively inform policy. We examined key challenges that limit effective engagement by scientists in the biodiversity policy process, drawing parallels with analogous challenges within global climate negotiations. Biodiversity is multifaceted, yet represents only one framing for nature's contributions to people, complicating the nexus between evidence and values in development of the framework's targets. Processes generating biodiversity and driving its loss are multiscalar, challenging development of an evidence base for globally standardized targets. We illustrated these challenges by contrasting development of 2 key elements of the framework. The genetic diversity element of the framework's target 4 is directly related to the framework's primary goals, but its complexity required development of novel engagement skills. The target for protected areas was easily communicated but more indirectly related to biodiversity outcomes; evidence from ecological and social science was essential to communicating the context and limitations of this relationship. Scientists can strengthen the effectiveness of global agreements and address challenges arising from complexity, scaling, capacity limitations, and the interplay of science and values, if they can prioritize communication, consensus-building, and networking skills and engage throughout the process, from development of an evidence base to implementation.

Lecciones de la COP15 sobre la participación científica efectiva en los procesos políticos de biodiversidad Resumen El Marco Global de la Biodiversidad de Kunming­Montreal lo adoptaron los participantes de la Convención sobre la Diversidad Biológica en diciembre 2022. Las consecuencias de estas negociaciones proporcionan una oportunidad para tomar lecciones de cómo la ciencia evolutiva y ecológica puede orientar de mejor manera a las políticas. Examinamos los retos clave que limitan la participación efectiva de los científicos en el proceso de políticas de la biodiversidad, estableciendo paralelismos con los retos análogos en las negociaciones climáticas mundiales. La biodiversidad es multifacética y aun así representa sólo un marco para las contribuciones que tiene la naturaleza para las personas, lo que complica el nexo entre la evidencia y los valores en el desarrollo de los objetivos del marco. Los procesos que generan la biodiversidad y causan su pérdida son multiescalares, lo que representa un reto para el desarrollo de una base de evidencias para tener objetivos mundiales estandarizados. Ilustramos estos retos con el contraste del desarrollo de dos elementos clave del marco. El elemento de la diversidad genética en el objetivo 4 del marco está relacionado directamente con los objetivos principales del marco, pero su complejidad requiere el desarrollo de habilidades novedosas de participación. El objetivo para las áreas protegidas se comunicó con facilidad, pero estuvo relacionado de forma más indirecta con los resultados de biodiversidad; la evidencia de las ciencias sociales y ecológicas fue esencial para comunicar el contexto y las limitaciones de esta relación. Los científicos pueden fortalecer la efectividad de los acuerdos globales y abordar los retos que surgen de la complejidad, el escalamiento, las limitaciones en la capacidad y la interacción de la ciencia y los valores, si pueden priorizar la comunicación, la llegada a consensos y el conocimiento de redes y participan durante el proceso, a partir del desarrollo de una evidencia base hasta la implementación.

Conserving a threatened North American walnut: a chromosome-scale reference genome for butternut (Juglans cinerea).

With the advent of affordable and more accurate third-generation sequencing technologies, and the associated bioinformatic tools, it is now possible to sequence, assemble, and annotate more species of conservation concern than ever before. Juglans cinerea, commonly known as butternut or white walnut, is a member of the walnut family, native to the Eastern United States and Southeastern Canada. The species is currently listed as Endangered on the IUCN Red List due to decline from an invasive fungus known as Ophiognomonia clavigignenti-juglandacearum (Oc-j) that causes butternut canker. Oc-j creates visible sores on the trunks of the tree which essentially starves and slowly kills the tree. Natural resistance to this pathogen is rare. Conserving butternut is of utmost priority due to its critical ecosystem role and cultural significance. As part of an integrated undergraduate and graduate student training program in biodiversity and conservation genomics, the first reference genome for Juglans cinerea is described here. This chromosome-scale 539 Mb assembly was generated from over 100 × coverage of Oxford Nanopore long reads and scaffolded with the Juglans mandshurica genome. Scaffolding with a closely related species oriented and ordered the sequences in a manner more representative of the structure of the genome without altering the sequence. Comparisons with sequenced Juglandaceae revealed high levels of synteny and further supported J. cinerea's recent phylogenetic placement. Comparative assessment of gene family evolution revealed a significant number of contracting families, including several associated with biotic stress response.

Conservation macrogenetics: harnessing genetic data to meet conservation commitments.

Genetic biodiversity is rapidly gaining attention in global conservation policy. However, for almost all species, conservation relevant, population-level genetic data are lacking, limiting the extent to which genetic diversity can be used for conservation policy and decision-making. Macrogenetics is an emerging discipline that explores the patterns and processes underlying population genetic composition at broad taxonomic and spatial scales by aggregating and reanalyzing thousands of published genetic datasets. Here we argue that focusing macrogenetic tools on conservation needs, or conservation macrogenetics, will enhance decision-making for conservation practice and fill key data gaps for global policy. Conservation macrogenetics provides an empirical basis for better understanding the complexity and resilience of biological systems and, thus, how anthropogenic drivers and policy decisions affect biodiversity.

Genetic diversity and IUCN Red List status.

The International Union for Conservation of Nature (IUCN) Red List is an important and widely used tool for conservation assessment. The IUCN uses information about a species' range, population size, habitat quality and fragmentation levels, and trends in abundance to assess extinction risk. Genetic diversity is not considered, although it affects extinction risk. Declining populations are more strongly affected by genetic drift and higher rates of inbreeding, which can reduce the efficiency of selection, lead to fitness declines, and hinder species' capacities to adapt to environmental change. Given the importance of conserving genetic diversity, attempts have been made to find relationships between red-list status and genetic diversity. Yet, there is still no consensus on whether genetic diversity is captured by the current IUCN Red List categories in a way that is informative for conservation. To assess the predictive power of correlations between genetic diversity and IUCN Red List status in vertebrates, we synthesized previous work and reanalyzed data sets based on 3 types of genetic data: mitochondrial DNA, microsatellites, and whole genomes. Consistent with previous work, species with higher extinction risk status tended to have lower genetic diversity for all marker types, but these relationships were weak and varied across taxa. Regardless of marker type, genetic diversity did not accurately identify threatened species for any taxonomic group. Our results indicate that red-list status is not a useful metric for informing species-specific decisions about the protection of genetic diversity and that genetic data cannot be used to identify threat status in the absence of demographic data. Thus, there is a need to develop and assess metrics specifically designed to assess genetic diversity and inform conservation policy, including policies recently adopted by the UN's Convention on Biological Diversity Kunming-Montreal Global Biodiversity Framework.

La diversidad genética y los estados de la Lista Roja de la UICN Resumen La Lista Roja de la Unión Internacional para la Conservación de la Naturaleza (UICN) es una importante herramienta de uso extendido para evaluar la conservación. La UICN utiliza datos sobre la distribución y tamaño poblacional de una especie, la calidad y niveles de fragmentación de su hábitat y sus tendencias de abundancia para valorar su riesgo de extinción, A pesar de que la diversidad genética afecta al riesgo de extinción, la UICN no la considera. La deriva génica y las tasas altas de endogamia afectan con mayor fuerza a las poblaciones en declinación, lo que puede reducir la eficiencia de la selección, derivar en la disminución de la aptitud y dificultar la capacidad de una especie de adaptarse ante el cambio ambiental. Se ha intentado encontrar la relación entre la diversidad genética y el estado en las listas rojas ya que su conservación es muy importante. Aun con lo anterior, no hay un consenso actual sobre si la diversidad genética está capturada en las categorías vigentes de la Lista Roja de la UICN de manera que sea informativa para la conservación. Para poder evaluar el poder predictivo de la correlación entre la diversidad genética y el estado en la Lista Roja de los vertebrados, sintetizamos trabajos previos y analizamos de nuevo los conjuntos de datos con base en tres tipos de información genética: ADN mitocondrial, microsatélites y genomas completos. Las especies con un estado de riesgo de extinción más alto fueron propensas a una diversidad genética más baja para todos los tipos de marcadores, aunque estas relaciones fueron débiles y variaron entre los taxones, lo cual es coherente con trabajos anteriores. Sin importar el tipo de marcador, la diversidad genética no fue un identificador certero de las especies amenazadas en ninguno de los grupos taxonómicos. Nuestros resultados indican que el estado de lista roja no es una medida útil para guiar las decisiones específicas por especie en relación con la protección de la diversidad genética. También indican que los datos genéticos no pueden usarse para identificar el estado de amenaza si no se tienen los datos demográficos. Por lo tanto, es necesario desarrollar y evaluar las medidas diseñadas específicamente para valorar la diversidad genética e informar las políticas de conservación, incluidas las que adoptó recientemente la ONU en el Convenio del Marco Mundial Kunming-Montreal de la Diversidad Biológica.

Genetic diversity goals and targets have improved, but remain insufficient for clear implementation of the post-2020 global biodiversity framework.

Genetic diversity among and within populations of all species is necessary for people and nature to survive and thrive in a changing world. Over the past three years, commitments for conserving genetic diversity have become more ambitious and specific under the Convention on Biological Diversity's (CBD) draft post-2020 global biodiversity framework (GBF). This Perspective article comments on how goals and targets of the GBF have evolved, the improvements that are still needed, lessons learned from this process, and connections between goals and targets and the actions and reporting that will be needed to maintain, protect, manage and monitor genetic diversity. It is possible and necessary that the GBF strives to maintain genetic diversity within and among populations of all species, to restore genetic connectivity, and to develop national genetic conservation strategies, and to report on these using proposed, feasible indicators.

Assessing ex situ genetic and ecogeographic conservation in a threatened but widespread oak after range-wide collecting effort.

Although the genetic diversity and structure of in situ populations has been investigated in thousands of studies, the genetic composition of ex situ plant populations has rarely been studied. A better understanding of how much genetic diversity is conserved ex situ, how it is distributed among locations (e.g., botanic gardens), and what minimum sample sizes are needed is necessary to improve conservation outcomes. Here we address these issues in a threatened desert oak species, Quercus havardii Rydb. We assess the genetic, geographic, and ecological representation of 290 plants from eight ex situ locations, relative to 667 wild individuals from 35 in situ locations. We also leverage a recent dataset of >3000 samples from 11 other threatened plants to directly compare the degree of genetic conservation for species that differ in geographic range size. We found that a majority of Q. havardii genetic diversity is conserved; one of its geographic regions is significantly better conserved than the other; genetic diversity conservation of this widespread species is lower than documented for the 11 rarer taxa; genetic diversity within each garden is strongly correlated to the number of plants and number of source populations; and measures of geographic and ecological conservation (i.e., percent area and percent of ecoregions represented) were typically lower than the direct assessment of genetic diversity (i.e., percent alleles). This information will inform future seed sampling expeditions to ensure that the intraspecific diversity of threatened plants can be effectively conserved.

Reduced representation sequencing to understand the evolutionary history of Torrey pine (Pinus torreyana parry) with implications for rare species conservation.

Understanding the contribution of neutral and adaptive evolutionary processes to population differentiation is often necessary for better informed management and conservation of rare species. In this study, we focused on Pinus torreyana Parry (Torrey pine), one of the world's rarest pines, endemic to one island and one mainland population in California. Small population size, low genetic diversity, and susceptibility to abiotic and biotic stresses suggest Torrey pine may benefit from interpopulation genetic rescue to preserve the species' evolutionary potential. We leveraged reduced representation sequencing to tease apart the respective contributions of stochastic and deterministic evolutionary processes to population differentiation. We applied these data to model spatial and temporal demographic changes in effective population sizes and genetic connectivity, to identify loci possibly under selection, and evaluate genetic rescue as a potential conservation strategy. Overall, we observed exceedingly low standing variation within both Torrey pine populations, reflecting consistently low effective population sizes across time, and limited genetic differentiation, suggesting maintenance of gene flow between populations following divergence. However, genome scans identified more than 2000 candidate SNPs potentially under divergent selection. Combined with previous observations indicating population phenotypic differentiation, this indicates natural selection has probably contributed to the evolution of population genetic differences. Thus, while reduced genetic diversity, small effective population size, and genetic connectivity between populations suggest genetic rescue could mitigate the adverse effects of rarity, evidence for adaptive differentiation suggests genetic mixing could disrupt adaptation. Further work evaluating the fitness consequences of inter-population admixture is necessary to empirically evaluate the trade-offs associated with genetic rescue in Torrey pine.

Global genetic diversity status and trends: towards a suite of Essential Biodiversity Variables (EBVs) for genetic composition.

Biodiversity underlies ecosystem resilience, ecosystem function, sustainable economies, and human well-being. Understanding how biodiversity sustains ecosystems under anthropogenic stressors and global environmental change will require new ways of deriving and applying biodiversity data. A major challenge is that biodiversity data and knowledge are scattered, biased, collected with numerous methods, and stored in inconsistent ways. The Group on Earth Observations Biodiversity Observation Network (GEO BON) has developed the Essential Biodiversity Variables (EBVs) as fundamental metrics to help aggregate, harmonize, and interpret biodiversity observation data from diverse sources. Mapping and analyzing EBVs can help to evaluate how aspects of biodiversity are distributed geographically and how they change over time. EBVs are also intended to serve as inputs and validation to forecast the status and trends of biodiversity, and to support policy and decision making. Here, we assess the feasibility of implementing Genetic Composition EBVs (Genetic EBVs), which are metrics of within-species genetic variation. We review and bring together numerous areas of the field of genetics and evaluate how each contributes to global and regional genetic biodiversity monitoring with respect to theory, sampling logistics, metadata, archiving, data aggregation, modeling, and technological advances. We propose four Genetic EBVs: (i) Genetic Diversity; (ii) Genetic Differentiation; (iii) Inbreeding; and (iv) Effective Population Size (Ne ). We rank Genetic EBVs according to their relevance, sensitivity to change, generalizability, scalability, feasibility and data availability. We outline the workflow for generating genetic data underlying the Genetic EBVs, and review advances and needs in archiving genetic composition data and metadata. We discuss how Genetic EBVs can be operationalized by visualizing EBVs in space and time across species and by forecasting Genetic EBVs beyond current observations using various modeling approaches. Our review then explores challenges of aggregation, standardization, and costs of operationalizing the Genetic EBVs, as well as future directions and opportunities to maximize their uptake globally in research and policy. The collection, annotation, and availability of genetic data has made major advances in the past decade, each of which contributes to the practical and standardized framework for large-scale genetic observation reporting. Rapid advances in DNA sequencing technology present new opportunities, but also challenges for operationalizing Genetic EBVs for biodiversity monitoring regionally and globally. With these advances, genetic composition monitoring is starting to be integrated into global conservation policy, which can help support the foundation of all biodiversity and species' long-term persistence in the face of environmental change. We conclude with a summary of concrete steps for researchers and policy makers for advancing operationalization of Genetic EBVs. The technical and analytical foundations of Genetic EBVs are well developed, and conservation practitioners should anticipate their increasing application as efforts emerge to scale up genetic biodiversity monitoring regionally and globally.

Crop genetic erosion: understanding and responding to loss of crop diversity.

Crop diversity underpins the productivity, resilience and adaptive capacity of agriculture. Loss of this diversity, termed crop genetic erosion, is therefore concerning. While alarms regarding evident declines in crop diversity have been raised for over a century, the magnitude, trajectory, drivers and significance of these losses remain insufficiently understood. We outline the various definitions, measurements, scales and sources of information on crop genetic erosion. We then provide a synthesis of evidence regarding changes in the diversity of traditional crop landraces on farms, modern crop cultivars in agriculture, crop wild relatives in their natural habitats and crop genetic resources held in conservation repositories. This evidence indicates that marked losses, but also maintenance and increases in diversity, have occurred in all these contexts, the extent depending on species, taxonomic and geographic scale, and region, as well as analytical approach. We discuss steps needed to further advance knowledge around the agricultural and societal significance, as well as conservation implications, of crop genetic erosion. Finally, we propose actions to mitigate, stem and reverse further losses of crop diversity.

Global Commitments to Conserving and Monitoring Genetic Diversity Are Now Necessary and Feasible.

Global conservation policy and action have largely neglected protecting and monitoring genetic diversity-one of the three main pillars of biodiversity. Genetic diversity (diversity within species) underlies species' adaptation and survival, ecosystem resilience, and societal innovation. The low priority given to genetic diversity has largely been due to knowledge gaps in key areas, including the importance of genetic diversity and the trends in genetic diversity change; the perceived high expense and low availability and the scattered nature of genetic data; and complicated concepts and information that are inaccessible to policymakers. However, numerous recent advances in knowledge, technology, databases, practice, and capacity have now set the stage for better integration of genetic diversity in policy instruments and conservation efforts. We review these developments and explore how they can support improved consideration of genetic diversity in global conservation policy commitments and enable countries to monitor, report on, and take action to maintain or restore genetic diversity.

Opportunities and challenges of macrogenetic studies.

The rapidly emerging field of macrogenetics focuses on analysing publicly accessible genetic datasets from thousands of species to explore large-scale patterns and predictors of intraspecific genetic variation. Facilitated by advances in evolutionary biology, technology, data infrastructure, statistics and open science, macrogenetics addresses core evolutionary hypotheses (such as disentangling environmental and life-history effects on genetic variation) with a global focus. Yet, there are important, often overlooked, limitations to this approach and best practices need to be considered and adopted if macrogenetics is to continue its exciting trajectory and reach its full potential in fields such as biodiversity monitoring and conservation. Here, we review the history of this rapidly growing field, highlight knowledge gaps and future directions, and provide guidelines for further research.

Charting a course for genetic diversity in the UN Decade of Ocean Science.

The health of the world's oceans is intrinsically linked to the biodiversity of the ecosystems they sustain. The importance of protecting and maintaining ocean biodiversity has been affirmed through the setting of the UN Sustainable Development Goal 14 to conserve and sustainably use the ocean for society's continuing needs. The decade beginning 2021-2030 has additionally been declared as the UN Decade of Ocean Science for Sustainable Development. This program aims to maximize the benefits of ocean science to the management, conservation, and sustainable development of the marine environment by facilitating communication and cooperation at the science-policy interface. A central principle of the program is the conservation of species and ecosystem components of biodiversity. However, a significant omission from the draft version of the Decade of Ocean Science Implementation Plan is the acknowledgment of the importance of monitoring and maintaining genetic biodiversity within species. In this paper, we emphasize the importance of genetic diversity to adaptive capacity, evolutionary potential, community function, and resilience within populations, as well as highlighting some of the major threats to genetic diversity in the marine environment from direct human impacts and the effects of global climate change. We then highlight the significance of ocean genetic diversity to a diverse range of socioeconomic factors in the marine environment, including marine industries, welfare and leisure pursuits, coastal communities, and wider society. Genetic biodiversity in the ocean, and its monitoring and maintenance, is then discussed with respect to its integral role in the successful realization of the 2030 vision for the Decade of Ocean Science. Finally, we suggest how ocean genetic diversity might be better integrated into biodiversity management practices through the continued interaction between environmental managers and scientists, as well as through key leverage points in industry requirements for Blue Capital financing and social responsibility.

Macrogenetic studies must not ignore limitations of genetic markers and scale.

Millette et al. (Ecology Letters, 2020, 23:55-67) reported no consistent worldwide anthropogenic effects on animal genetic diversity using repurposed mitochondrial DNA sequences. We reexamine data from this study, describe genetic marker and scale limitations which might lead to misinterpretations with conservation implications, and provide advice to improve future macrogenetic studies.

Hybrid Breeding for Restoration of Threatened Forest Trees: Evidence for Incorporating Disease Tolerance in Juglans cinerea.

Hybridization is a potential tool for incorporating stress tolerance in plants, particularly to pests and diseases, in support of restoration and conservation efforts. Butternut (Juglans cinerea) is a species for which hybridization has only recently begun being explored. This North American hardwood tree is threatened due to Ophiognomonia clavigignenti-juglandacearum (Ocj), the causal fungus of butternut canker disease (BCD), first observed in 1967. Observational evidence in some wild J. cinerea populations indicates that naturalized hybrids of J. cinerea with Japanese walnut (Juglans ailantifolia) may be more tolerant to BCD than non-admixed J. cinerea, but this has not been formally tested in a controlled trial. We aimed to examine potential BCD tolerance within and between J. cinerea and J. cinerea × J. ailantifolia hybrids and to determine if there is a difference in canker growth between BCD fungal isolates. Five-year-old J. cinerea and hybrid trees were inoculated with two Ocj fungal isolates collected from natural infections found in two different sites in Indiana, United States, and a blank control (agar only). Measurements of both artificially induced and naturally occurring cankers were taken at 8-, 12-, 20-, 24-, and 32-month post-inoculation. Differences in canker presence/absence and size were observed by fungal isolate, which could help explain some of the differences in BCD severity seen between J. cinerea populations. Smaller and fewer cankers and greater genetic gains were seen in hybrid families, demonstrating that hybrids warrant further evaluation as a possible breeding tool for developing BCD-resistant J. cinerea trees.

Taxonomic similarity does not predict necessary sample size for ex situ conservation: a comparison among five genera.

Effectively conserving biodiversity with limited resources requires scientifically informed and efficient strategies. Guidance is particularly needed on how many living plants are necessary to conserve a threshold level of genetic diversity in ex situ collections. We investigated this question for 11 taxa across five genera. In this first study analysing and optimizing ex situ genetic diversity across multiple genera, we found that the percentage of extant genetic diversity currently conserved varies among taxa from 40% to 95%. Most taxa are well below genetic conservation targets. Resampling datasets showed that ideal collection sizes vary widely even within a genus: one taxon typically required at least 50% more individuals than another (though Quercus was an exception). Still, across taxa, the minimum collection size to achieve genetic conservation goals is within one order of magnitude. Current collections are also suboptimal: they could remain the same size yet capture twice the genetic diversity with an improved sampling design. We term this deficiency the 'genetic conservation gap'. Lastly, we show that minimum collection sizes are influenced by collection priorities regarding the genetic diversity target. In summary, current collections are insufficient (not reaching targets) and suboptimal (not efficiently designed), and we show how improvements can be made.