Best practices for genetic and genomic data archiving.

Genetic and genomic data are collected for a vast array of scientific and applied purposes. Despite mandates for public archiving, data are typically used only by the generating authors. The reuse of genetic and genomic datasets remains uncommon because it is difficult, if not impossible, due to non-standard archiving practices and lack of contextual metadata. But as the new field of macrogenetics is demonstrating, if genetic data and their metadata were more accessible and FAIR (findable, accessible, interoperable and reusable) compliant, they could be reused for many additional purposes. We discuss the main challenges with existing genetic and genomic data archives, and suggest best practices for archiving genetic and genomic data. Recognizing that this is a longstanding issue due to little formal data management training within the fields of ecology and evolution, we highlight steps that research institutions and publishers could take to improve data archiving.

The positive impact of conservation action.

Governments recently adopted new global targets to halt and reverse the loss of biodiversity. It is therefore crucial to understand the outcomes of conservation actions. We conducted a global meta-analysis of 186 studies (including 665 trials) that measured biodiversity over time and compared outcomes under conservation action with a suitable counterfactual of no action. We find that in two-thirds of cases, conservation either improved the state of biodiversity or at least slowed declines. Specifically, we find that interventions targeted at species and ecosystems, such as invasive species control, habitat loss reduction and restoration, protected areas, and sustainable management, are highly effective and have large effect sizes. This provides the strongest evidence to date that conservation actions are successful but require transformational scaling up to meet global targets.

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.

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.

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.

The evolutionary history and genomics of European blackcap migration.

Seasonal migration is a taxonomically widespread behaviour that integrates across many traits. The European blackcap exhibits enormous variation in migration and is renowned for research on its evolution and genetic basis. We assembled a reference genome for blackcaps and obtained whole genome resequencing data from individuals across its breeding range. Analyses of population structure and demography suggested divergence began ~30,000 ya, with evidence for one admixture event between migrant and resident continent birds ~5000 ya. The propensity to migrate, orientation and distance of migration all map to a small number of genomic regions that do not overlap with results from other species, suggesting that there are multiple ways to generate variation in migration. Strongly associated single nucleotide polymorphisms (SNPs) were located in regulatory regions of candidate genes that may serve as major regulators of the migratory syndrome. Evidence for selection on shared variation was documented, providing a mechanism by which rapid changes may evolve.

Every year as the seasons change, thousands of animals migrate huge distances in search of food or better climates. As far as migrations go, there might be none so impressive as the trans-oceanic flights made by small migrating songbirds. These birds can weigh as little as three grams and travel up to 15,000 kilometres. Most migrate alone and at night and yet still manage to return to the same location each year. Several strands of research suggest there could be a genetic basis to their migratory behaviour, but exactly which genes control this phenomenon remains poorly understood. One small songbird that has been studied for decades is the European blackcap. This species exhibits a real variety of migration patterns. Some blackcaps travel rather short distances, others much further, and some populations do not migrate at all. Populations that share the same breeding grounds in the summer may migrate in different directions in the autumn. These features make it a good species to study the genetic variation between populations that migrate in different directions and over different distances. However, only in recent years has advancing technology made it possible to comprehensively study an animal's entire genome, leaving no gene unturned. Now, Delmore et al. have used high-throughput sequencing technologies to trace the evolutionary history of migration in European blackcap and started by assembling a reference genome for the species. Then, the genomes of 110 blackcaps from several populations that take different annual migrations were compared to the reference. This revealed that the populations began to diverge some 30,000 years ago and that there was some apparent gene mixing between groups of migrating and resident blackcaps around 5,000 years ago. The analysis showed only a small set of genes code for their differences in migration. Additionally, while the candidate genes were shown to be common among blackcaps, the genes identified did not match those reported from studies of other migrating songbirds. Finally, Delmore et al. also noted that the differences between the populations tend to be in the parts of the genome that control whether a given gene is switched on or off, which could explain how new migratory behaviours can rapidly evolve. This study is one of the most comprehensive genomic analysis of migration to date. It is important work as songbirds, like other animals, are responding to increasing pressures of environmental and climate change. In time, the findings could be used to support conservation efforts whereby genetic analyses could determine if certain populations possess enough variation to respond to coming changes in their habitats.

Evaluating the effectiveness of retention forestry to enhance biodiversity in production forests of Central Europe using an interdisciplinary, multi-scale approach.

Retention forestry, which retains a portion of the original stand at the time of harvesting to maintain continuity of structural and compositional diversity, has been originally developed to mitigate the impacts of clear-cutting. Retention of habitat trees and deadwood has since become common practice also in continuous-cover forests of Central Europe. While the use of retention in these forests is plausible, the evidence base for its application is lacking, trade-offs have not been quantified, it is not clear what support it receives from forest owners and other stakeholders and how it is best integrated into forest management practices. The Research Training Group ConFoBi (Conservation of Forest Biodiversity in Multiple-use Landscapes of Central Europe) focusses on the effectiveness of retention forestry, combining ecological studies on forest biodiversity with social and economic studies of biodiversity conservation across multiple spatial scales. The aim of ConFoBi is to assess whether and how structural retention measures are appropriate for the conservation of forest biodiversity in uneven-aged and selectively harvested continuous-cover forests of temperate Europe. The study design is based on a pool of 135 plots (1 ha) distributed along gradients of forest connectivity and structure. The main objectives are (a) to investigate the effects of structural elements and landscape context on multiple taxa, including different trophic and functional groups, to evaluate the effectiveness of retention practices for biodiversity conservation; (b) to analyze how forest biodiversity conservation is perceived and practiced, and what costs and benefits it creates; and (c) to identify how biodiversity conservation can be effectively integrated in multi-functional forest management. ConFoBi will quantify retention levels required across the landscape, as well as the socio-economic prerequisites for their implementation by forest owners and managers. ConFoBi's research results will provide an evidence base for integrating biodiversity conservation into forest management in temperate forests.

Conservation genetics: Linking science with practice.

Conservation genetics is a well-established scientific field. However, limited information transfer between science and practice continues to hamper successful implementation of scientific knowledge in conservation practice and management. To mitigate this challenge, we have established a conservation genetics community, which entails an international exchange-and-skills platform related to genetic methods and approaches in conservation management. First, it allows for scientific exchange between researchers during annual conferences. Second, personal contact between conservation professionals and scientists is fostered by organising workshops and by popularising knowledge on conservation genetics methods and approaches in professional journals in national languages. Third, basic information on conservation genetics has been made accessible by publishing an easy-to-read handbook on conservation genetics for practitioners. Fourth, joint projects enabled practitioners and scientists to work closely together from the start of a project in order to establish a tight link between applied questions and scientific background. Fifth, standardised workflows simplifying the implementation of genetic tools in conservation management have been developed. By establishing common language and trust between scientists and practitioners, all these measures help conservation genetics to play a more prominent role in future conservation planning and management.

Parasites in space and time: a case study of haemosporidian spatiotemporal prevalence in urban birds.

Prevalence responses to anthropic factors differ across hosts and parasite species. We here analyzed the spatiotemporal variation of avian haemosporidian prevalence in bird assemblages of the Mooswald forest (i.e., urban greenspace; Freiburg, Germany), in response to local environmental features (e.g., water sources, human presence (visited)/absence (unvisited)) and bird-level traits (e.g., body condition, age, sex) in 2 years. We used a nested PCR protocol (mitochondrial (mt)DNA cytochrome b (cyt b) gene) and microscopy to determine haemosporidian infections. Prevalence was analyzed using a general linear multi-model (glmulti) approach with Akaike information criterion corrected for small samples (AICc), with subsequent model inferences using a GLMM on the best selected model, considering bird species as a random factor. Analyses were conducted for the main understory bird species (Blackcap - Sylvia atricapilla, Chaffinch - Coereba flaveola, Great Tit - Parus major, Blue Tit - Cyanistes caeruleus, European Robin - Erithacus rubecula, Blackbird - Turdus merula, Song Thrush - Turdus philomelos). We further conducted spatial autocorrelation analyses for all haemosporidian infections, and classification and regression trees (CARTs) for focal species. We analyzed a total of 544 samples of seven bird species. In 2011 prevalence for Haemoproteus/Plasmodium was 25.8% and 11.7% for Leucocytozoon. In 2013 prevalence for Haemoproteus/Plasmodium was 26.5% and 35.5% for Leucocytozoon. Haemosporidian prevalence was significantly different between some focal species. There was a negative association between distance to the nearest water source and prevalence in the year 2011, and the opposite pattern for the year 2013. However, when analyzed for the six focal species separately, such a relationship could change from a negative to a positive one, or there could be no relationship at all. For Leucocytozoon there was higher prevalence in the section of the forest visited by humans. We did not find spatial autocorrelation for prevalence across the study site, but there were statistically significant local spatial clusters in the visited section. Although there were similar responses of prevalence to some factors, infection patterns were generally bird species-specific. Thus, prevalence is a labile epidemiological parameter, varying spatiotemporally in an idiosyncratic way.

Next-generation conservation genetics and biodiversity monitoring.

This special issue of Evolutionary Applications consists of 10 publications investigating the use of next-generation tools and techniques in population genetic analyses and biodiversity assessment. The special issue stems from a 2016 Next Generation Genetic Monitoring Workshop, hosted by the National Institute for Mathematical and Biological Synthesis (NIMBioS) in Tennessee, USA. The improved accessibility of next-generation sequencing platforms has allowed molecular ecologists to rapidly produce large amounts of data. However, with the increased availability of new genomic markers and mathematical techniques, care is needed in selecting appropriate study designs, interpreting results in light of conservation concerns, and determining appropriate management actions. This special issue identifies key attributes of successful genetic data analyses in biodiversity evaluation and suggests ways to improve analyses and their application in current population and conservation genetics research.

Projected impacts of climate change on habitat availability for an endangered parakeet.

In tropical montane cloud forests, climate change can cause upslope shifts in the distribution ranges of species, leading to reductions in distributional range. Endemic species with small ranges are particularly vulnerable to such decreases in range size, as the population size may be reduced significantly. To ensure the survival of cloud forest species in the long term, it is crucial to quantify potential future shifts in their distribution ranges and the related changes in habitat availability in order to assure the long-term effectiveness of conservation measures. In this study, we assessed the influence of climate change on the availability of forested habitat for the endemic El Oro parakeet. We investigated the future range shift by modelling the climatic niche of the El Oro parakeets and projecting it to four different climate change scenarios. Depending on the intensity of climate change, the El Oro parakeets shift their range between 500 and 1700 m uphill by the year 2100. On average, the shift is accompanied by a reduction in range size to 15% and a reduction in forested habitat to only 10% of the original extent. Additionally, the connectivity between populations in different areas is decreasing in higher altitudes. To prevent a population decline due to habitat loss following an upslope range shift, it will be necessary to restore habitat across a large elevational span in order to allow for movement of El Oro parakeets into higher altitudes.

Decline in territory size and fecundity as a response to carrying capacity in an endangered songbird.

Density-dependent processes are fundamental mechanisms for the regulation of populations. Ecological theories differ in their predictions on whether increasing population density leads to individual adjustments of survival and reproductive output or to dominance and monopolization of resources. Here, we use a natural experiment to examine which factors limit population growth in the only remaining population of the endangered pale-headed brush finch (Atlapetes pallidiceps). For three distinct phases (a phase of population suppression, 2001-2002; expansion due to conservation management, 2003-2008; and equilibrium phase, 2009-2014), we estimated demographic parameters with an integrated population model using population size, the proportion of successfully breeding pairs and their productivity, territory size, and mark-recapture data of adult birds. A low proportion of successful breeders due to brood parasitism (0.42, 95% credible interval 0.26-0.59) limited population growth before 2003; subsequent culling of the brood parasite resulted in a two-fold increase of the proportion of successful breeders during the 'expansion phase'. When the population approached the carrying capacity of its habitat, territory size declined by more than 50% and fecundity declined from 1.9 (1.54-2.27) to 1.3 (1.12-1.53) chicks per breeding pair, but the proportion of successful breeders remained constant (expansion phase: 0.85; 0.76-0.93; equilibrium phase: 0.86; 0.79-0.92). This study demonstrates that limiting resources can lead to individual adjustments instead of despotic behavior, and the individual reduction of reproductive output at high population densities is consistent with the slow life-history of many tropical species.

Is It Time for Synthetic Biodiversity Conservation?

Evidence indicates that, despite some critical successes, current conservation approaches are not slowing the overall rate of biodiversity loss. The field of synthetic biology, which is capable of altering natural genomes with extremely precise editing, might offer the potential to resolve some intractable conservation problems (e.g., invasive species or pathogens). However, it is our opinion that there has been insufficient engagement by the conservation community with practitioners of synthetic biology. We contend that rapid, large-scale engagement of these two communities is urgently needed to avoid unintended and deleterious ecological consequences. To this point we describe case studies where synthetic biology is currently being applied to conservation, and we highlight the benefits to conservation biologists from engaging with this emerging technology.