Integrating population genetics and conservation biology in the era of genomics

As one of the final activities of the ESF-CONGEN Networking programme, a conference entitled ‘Integrating Population Genetics and Conservation Biology’ was held at Trondheim, Norway, from 23 to 26 May 2009. Conference speakers and poster presenters gave a display of the state-of-the-art developments in the field of conservation genetics. Over the five-year running period of the successful ESF-CONGEN Networking programme, much progress has been made in theoretical approaches, basic research on inbreeding depression and other genetic processes associated with habitat fragmentation and conservation issues, and with applying principles of conservation genetics in the conservation of many species. Future perspectives were also discussed in the conference, and it was concluded that conservation genetics is evolving into conservation genomics, while at the same time basic and applied research on threatened species and populations from a population genetic point of view continues to be emphasized.     

Conservation genetics in a globally changing environment: present problems,paradoxes and future challenges

Despite recent advances in conservation genetics and related disciplines and the growing impact that conservation genetics is having in conservation biology, our knowledge on several key issues in the field is still insufficient. Here we identify some of these issues together with addressing several paradoxes which have to be solved before conservation genetics can face new challenges that are appearing in the transitory phase from the population genetics into the population genomics era. Most of these issues, paradoxes and challenges, like the central dogma of conservation genetics, the computational, theoretical and laboratory experiment achievements and limitations in the conservation genetics field have been discussed. Further knowledge on the consequences of inbreeding and outbreeding depression in wild populations as well as the capacity of small populations to adapt to local environmental conditions is also urgently needed. The integration of experimental, theoretical and applied conservation genetics will contribute to improve our understanding of methodological and applied aspects of conservation genetics.     

An essay on the necessity and feasibility of conservation genomics

The basic premise of conservation genetics is that small populations may be genetically threatened. The two steps leading to this premise are: (1) due to prominent influence of random genetic drift and inbreeding allelic and genotypic diversity in small populations is expected to be low, and (2) low allelic diversity and high homozygosity are expected to lead to immediate fitness decreases (inbreeding depression) and a compromised potential for evolutionary adaptation. Conservation genetic research has been strongly stimulated by the application of neutral molecular markers like microsatellites and AFLPs. In general these marker studies have provided evidence for step 1. It is less evident how these markers may provide evidence for step 2. In this essay we argue that, in order to get detailed insight in step 2, adopting a conservation genomic approach, in which conservation genetics will use approaches from ecological and evolutionary functional genomics (ecogenomics), is both necessary and feasible. Conservation genomics is necessary for studying functional genomic variation as function of drift and inbreeding, for studying the mechanisms that relate low genetic variation to low fitness, for integrating environmental and genetic approaches to conservation biology, and for developing modern, fast monitoring tools. The rapid technical and financial developments in genomics currently make conservation genomics feasible, and will improve feasibility in the very near future even further. We therefore argue that conservation genomics personifies part of the near future of conservation genetics.     

Integrating terrestrial scavenging ecology into contemporary wildlife conservation and management

Scavenging plays a vital role in maintaining ecosystem health and contributing to ecological functions; however, research in this sub‐discipline of ecology is underutilized in developing and implementing wildlife conservation and management strategies. We provide an examination of the literature and recommend priorities for research where improved understanding of scavenging dynamics can facilitate the development and refinement of applied wildlife conservation and management strategies. Due to the application of scavenging research broadly within ecology, scavenging studies should be implemented for informing management decisions. In particular, a more direct link should be established between scavenging dynamics and applied management programs related to informing pharmaceutical delivery and population control through bait uptake for scavenging species, prevention of unintentional poisoning of nontarget scavenging species, the epidemiological role that scavenging species play in disease dynamics, estimating wildlife mortalities, nutrient transfer facilitated by scavenging activity, and conservation of imperiled facultative scavenging species. This commentary is intended to provide information on the paucity of data in scavenging research and present recommendations for further studies that can inform decisions in wildlife conservation and management. Additionally, we provide a framework for decision‐making when determining how to apply scavenging ecology research for management practices and policies. Due to the implications that scavenging species have on ecosystem health, and their overall global decline as a result of anthropic activities, it is imperative to advance studies in the field of scavenging ecology that can inform applied conservation and management programs.     

Bee conservation in the age of genomics

Many wild and managed bee pollinators have experienced population declines over the past several decades, and molecular and population genetic tools have been valuable in understanding conservation threats across the bee tree of life. Emerging genomic tools have the potential to improve classical applications of conservation genetics, such as assessing species status, and quantifying genetic diversity, gene flow and effective population sizes. Genomic tools can also revolutionize novel research in bee conservation and management, including the identification of loci underlying adaptive and economically desirable traits, such as those involved in disease susceptibility, responses to multiple environmental stressors, and even discovering and understanding the hidden diversity of beneficial microorganisms associated with bees. In this perspective, we provide a survey of some of the ways genomic tools can be applied to bee conservation to bridge the gap between basic and applied genomics research.     

Population genomics of marine fishes: identifying adaptive variation in space and time

Studies of adaptive evolution have experienced a recent revival in population genetics of natural populations and there is currently much focus on identifying genomic signatures of selection in space and time. Insights into local adaptation, adaptive response to global change and evolutionary consequences of selective harvesting can be generated through population genomics studies, allowing the separation of the effects invoked by neutral processes (drift-migration) from those due to selection. Such knowledge is important not only for improving our basic understanding of natural as well as human-induced evolutionary processes, but also for predicting future trajectories of biodiversity and for setting conservation priorities. Marine fishes possess a number of features rendering them well suited for providing general insights into adaptive genomic evolution in natural populations. These include well-described population structures, substantial and rapidly developing genomic resources and abundant archived samples enabling temporal studies. Furthermore, superior possibilities for conducting large-scale experiments under controlled conditions, due to the economic resources provided by the large and growing aquaculture industry, hold great promise for utilizing recent technological developments. Here, we review achievements in marine fish genomics to date and highlight potential avenues for future research, which will provide both general insights into evolution in high gene flow species, as well as specific knowledge which can lead to improved management of marine organisms.     

Applying genomic data in wildlife monitoring: Development guidelines for genotyping degraded samples with reduced single nucleotide polymorphism panels

The genomic era has led to an unprecedented increase in the availability of genome‐wide data for a broad range of taxa. Wildlife management strives to make use of these vast resources to enable refined genetic assessments that enhance biodiversity conservation. However, as new genomic platforms emerge, problems remain in adapting the usually complex approaches for genotyping of noninvasively collected wildlife samples. Here, we provide practical guidelines for the standardized development of reduced single nucleotide polymorphism (SNP) panels applicable for microfluidic genotyping of degraded DNA samples, such as faeces or hairs. We demonstrate how microfluidic SNP panels can be optimized to efficiently monitor European wildcat (Felis silvestris S.) populations. We show how panels can be set up in a modular fashion to accommodate informative markers for relevant population genetics questions, such as individual identification, hybridization assessment and the detection of population structure. We discuss various aspects regarding the implementation of reduced SNP panels and provide a framework that will allow both molecular ecologists and practitioners to help bridge the gap between genomics and applied wildlife conservation.     

Community‐based wildlife management area supports similar mammal species richness and densities compared to a national park

Community‐based conservation models have been widely implemented across Africa to improve wildlife conservation and livelihoods of rural communities. In Tanzania, communities can set aside land and formally register it as Wildlife Management Area (WMA), which allows them to generate revenue via consumptive or nonconsumptive utilization of wildlife. The key, yet often untested, assumption of this model is that economic benefits accrued from wildlife motivate sustainable management of wildlife. To test the ecological effectiveness (here defined as persistence of wildlife populations) of Burunge Wildlife Management Area (BWMA), we employed a participatory monitoring approach involving WMA personnel. At intermittent intervals between 2011 and 2018, we estimated mammal species richness and population densities of ten mammal species (African elephant, giraffe, buffalo, zebra, wildebeest, waterbuck, warthog, impala, Kirk's dik‐dik, and vervet monkey) along line transects. We compared mammal species accumulation curves and density estimates with those of time‐matched road transect surveys conducted in adjacent Tarangire National Park (TNP). Mammal species richness estimates were similar in both areas, yet observed species richness per transect was greater in TNP compared to BWMA. Species‐specific density estimates of time‐matched surveys were mostly not significantly different between BWMA and TNP, but elephants occasionally reached greater densities in TNP compared to BWMA. In BWMA, elephant, wildebeest, and impala populations showed significant increases from 2011 to 2018. These results suggest that community‐based conservation models can support mammal communities and densities that are similar to national park baselines. In light of the ecological success of this case study, we emphasize the need for continued efforts to ensure that the BWMA is effective. This will require adaptive management to counteract potential negative repercussions of wildlife populations on peoples' livelihoods. This study can be used as a model to evaluate the effectiveness of wildlife management areas across Tanzania.     

Precision wildlife medicine: applications of the human‐centred precision medicine revolution to species conservation

The current species extinction crisis is being exacerbated by an increased rate of emergence of epizootic disease. Human‐induced factors including habitat degradation, loss of biodiversity and wildlife population reductions resulting in reduced genetic variation are accelerating disease emergence. Novel, efficient and effective approaches are required to combat these epizootic events. Here, we present the case for the application of human precision medicine approaches to wildlife medicine in order to enhance species conservation efforts. We consider how the precision medicine revolution, coupled with the advances made in genomics, may provide a powerful and feasible approach to identifying and treating wildlife diseases in a targeted, effective and streamlined manner. A number of case studies of threatened species are presented which demonstrate the applicability of precision medicine to wildlife conservation, including sea turtles, amphibians and Tasmanian devils. These examples show how species conservation could be improved by using precision medicine techniques to determine novel treatments and management strategies for the specific medical conditions hampering efforts to restore population levels. Additionally, a precision medicine approach to wildlife health has in turn the potential to provide deeper insights into human health and the possibility of stemming and alleviating the impacts of zoonotic diseases. The integration of the currently emerging Precision Medicine Initiative with the concepts of EcoHealth (aiming for sustainable health of people, animals and ecosystems through transdisciplinary action research) and One Health (recognizing the intimate connection of humans, animal and ecosystem health and addressing a wide range of risks at the animal–human–ecosystem interface through a coordinated, collaborative, interdisciplinary approach) has great potential to deliver a deeper and broader interdisciplinary‐based understanding of both wildlife and human diseases.     

Conservation genomics of natural and managed populations: building a conceptual and practical framework

The boom of massive parallel sequencing (MPS) technology and its applications in conservation of natural and managed populations brings new opportunities and challenges to meet the scientific questions that can be addressed. Genomic conservation offers a wide range of approaches and analytical techniques, with their respective strengths and weaknesses that rely on several implicit assumptions. However, finding the most suitable approaches and analysis regarding our scientific question are often difficult and time‐consuming. To address this gap, a recent workshop entitled ‘ConGen 2015’ was held at Montana University in order to bring together the knowledge accumulated in this field and to provide training in conceptual and practical aspects of data analysis applied to the field of conservation and evolutionary genomics. Here, we summarize the expertise yield by each instructor that has led us to consider the importance of keeping in mind the scientific question from sampling to management practices along with the selection of appropriate genomics tools and bioinformatics challenges.     

红外相机技术在我国野生动物研究与保护中的应用与前景

20年来, 红外相机技术在国内外野生动物研究、监测与保护中得到了广泛应用。基于红外相机技术, 我国在野生动物生态学研究、动物行为学研究、稀有物种的探测与记录、动物本底资源调查、生物多样性监测及保护地管理与保护评价等领域取得了众多成果。目前, 数学模型、统计分析方法和新的概念正在促进红外相机技术在野生动物监测研究与保护管理中的发展和推广应用。同时, 随着红外相机技术的成熟、成本降低和应用普及, 这一技术也将会被更多的野生动物研究人员、管理人员和自然保护区管理者所采用, 并成为全国各级保护地和区域生物多样性监测研究的关键技术和方法。今后, 建立并完善系统化的监测网络和数据共享平台、开发新一代的数据分析方法与模型, 将是此项技术进一步发展和应用的主要方向。     

Genomic investigation of the Chinese alligator reveals wild-extinct genetic diversity and genomic consequences of their continuous decline

Critically endangered species are usually restricted to small and isolated populations. High inbreeding without gene flow among populations further aggravates their threatened condition and reduces the likelihood of their long-term survival. Chinese alligator (Alligator sinensis) is one of the most endangered crocodiles in the world and has experienced a continuous decline over the past c. 1 million years. In order to identify the genetic status of the remaining populations and aid conservation efforts, we assembled the first high-quality chromosome-level genome of Chinese alligator and explored the genomic characteristics of three extant breeding populations. Our analyses revealed the existence of at least three genetically distinct populations, comprising two breeding populations in China (Changxing and Xuancheng) and one breeding population in an American wildlife refuge. The American population does not belong to the last two populations of its native range (Xuancheng and Changxing), thus representing genetic diversity extinct in the wild and provides future opportunities for genetic rescue. Moreover, the effective population size of these three populations has been continuously declining over the past 20 ka. Consistent with this decline, the species shows extremely low genetic diversity, a large proportion of long runs of homozygous fragments, and mutational load across the genome. Finally, to provide genomic insights for future breeding management and conservation, we assessed the feasibility of mixing extant populations based on the likelihood of introducing new deleterious alleles and signatures of local adaptation. Overall, this study provides a valuable genomic resource and important genomic insights into the ecology, evolution, and conservation of critically endangered alligators.     

分子标记在濒危物种保护中的应用

分子标记可揭示种群遗传和进化信息, 为制定濒危物种保护措施、指导恢复实践提供重要依据。本文主要介绍了分子标记在濒危物种保护过程不同环节中的应用, 包括: (1)正确识别保护单元, 如排除隐存种和杂交种的影响; (2)确定优先保护单元, 包括优先保护区域、优先保护物种、优先保护种群等; (3)指导迁地保护; (4)对保护工作的动态监测和评估。文章最后探讨了分子标记应用于保护的发展方向, 如开展长期的种群遗传组成监测、切实应用于保护管理实践、将基因组学等遗传信息用于全球变化背景下保护策略的制定等, 期望为分子标记技术在生物多样性保护的研究和实践中提供参考。     

Molecular tools and bumble bees: revealing hidden details of ecology and evolution in a model system

Bumble bees are a longstanding model system for studies on behaviour, ecology and evolution, due to their well‐studied social lifestyle, invaluable role as wild and managed pollinators, and ubiquity and diversity across temperate ecosystems. Yet despite their importance, many aspects of bumble bee biology have remained enigmatic until the rise of the genetic and, more recently, genomic eras. Here, we review and synthesize new insights into the ecology, evolution and behaviour of bumble bees that have been gained using modern genetic and genomic techniques. Special emphasis is placed on four areas of bumble bee biology: the evolution of eusociality in this group, population‐level processes, large‐scale evolutionary relationships and patterns, and immunity and resistance to pesticides. We close with a prospective on the future of bumble bee genomics research, as this rapidly advancing field has the potential to further revolutionize our understanding of bumble bees, particularly in regard to adaptation and resilience. Worldwide, many bumble bee populations are in decline. As such, throughout the review, connections are drawn between new molecular insights into bumble bees and our understanding of the causal factors involved in their decline. Ongoing and potential applications to bumble bee management and conservation are also included to demonstrate how genetics‐ and genomics‐enabled research aids in the preservation of this threatened group.     

Conservation genetics of South American aquatic mammals: an overview of gene diversity,population structure,phylogeography, non‐invasive methods and forensics

• 1 Most aquatic mammals have high dispersal potential, and there are often severe conservation concerns related to their legal or illegal harvesting. Therefore, economic, social and forensic factors often arise in decisions relating to their population management. Molecular markers are essential tools in modern conservation genetics, revealing previously unknown aspects of aquatic mammal behaviour, natural history, population structure and demography. Molecular markers also have been used to define management units, to recognize taxonomic units, to conduct forensic analyses and to control illegal wildlife trade, providing valuable information for decision‐making in wildlife conservation and management.
• 2 We review studies published in peer‐reviewed journals between 1993 and 2010, in which genetic approaches have been applied to conservation‐related issues involving natural populations of 25 species of aquatic mammals in South America. These studies cover just 34% of the 70 aquatic mammal species recorded in South America.
• 3 Most of the studies are related to population structure, phylogeography, gene flow and dispersal movements. In addition, recent findings relate to evolutionarily significant units, management units, forensics and conservation policy.
• 4 Finally, we look to the future and, based on numbers of studies and conservation concerns, suggest which species, geographic areas and genetic studies should be prioritized. Moreover, we discuss constraints on research and suggest collaborative works that would provide critical information towards the effective conservation and management of aquatic mammals in South America.

     

metapop2: Re‐implementation of software for the analysis and management of subdivided populations using gene and allelic diversity

Management programmes often have to make decisions based on the analysis of the genetic properties and diversity of populations. Expected heterozygosity (or gene diversity) and population structure parameters are often used to make recommendations for conservation, such as avoidance of inbreeding or migration across subpopulations. Allelic diversity, however, can also provide complementary and useful information for conservation programmes, as it is highly sensitive to population bottlenecks, and is more related to long‐term selection response than heterozygosity. Here we present a completely revised and updated re‐implementation of the software metapop for the analysis of diversity in subdivided populations, as well as a tool for the management and dynamic estimation of optimal contributions in conservation programmes. This new update includes computation of allelic diversity for population analysis and management, as well as a simulation mode to forecast the consequences of taking different management strategies over time. Furthermore, the new implementation in C++ includes code optimization and improved memory usage, allowing for fast analysis of large data sets including single nucleotide polymorphism markers, as well as enhanced cross‐software and cross‐platform compatibility.     

Causes and consequences of lags in basic and applied research into feral wildlife ecology: the case for feral horses

The biomass of feral wildlife is eclipsing that of native wildlife in many parts of the world. Consequently, feral species are playing an increasingly important role in ecological community dynamics. Artificially selected life-history traits of wild but once domesticated species can elicit population dynamics that differ substantially from that of native species. Yet, we continue to lag in our understanding of the ecology and evolution of feral species with direct consequences to resource management and biodiversity conservation. In part, this is because basic and applied research into the ecology of feral wildlife is fraught with social and political challenges unique to science. Feral populations of companion animals or livestock, especially, can evoke strong emotional reactions among advocacy groups, particularly around issues of animal welfare and management policy. Managers tasked with controlling feral populations are often bound by social license, including legislative restrictions, incomparable to that of other wildlife, and harassment or litigation of researchers and managers is not uncommon. Further, research and management of feral species is often delegated to agricultural instead of wildlife government agencies with clear differences in mandate, staff education, and training. Using examples primarily from feral horses in North America, we show how scientists conducting research independent of the management process can find themselves placed between managers, advocates, and opponents of feral species, implicitly tasked with satisfying multiple and often contradictory interests of stakeholders, sometimes with direct and litigious interference. These barriers are exacerbated by inter-disciplinary tendencies to dismiss the importance of basic and applied ecological research into feral species, despite its relevance to sound decision-making. Feral species therefore possess politically and biologically facilitated asymmetries that favor persistence, growth, and expansion relative to native wildlife, while the timely study of these characteristics in nature continues to suffer from ideological opposition.     

Ex situ breeding programs benefit from science-based cooperative management

Science-based management confers a variety of benefits to wildlife populations that are cooperatively managed by zoos and aquariums, including those managed through the Association of Zoos and Aquariums. Briefly, when management strategies are successful, they result in reproductively robust populations that better retain genetic diversity and limit inbreeding than unmanaged populations. Although the benefits of demographic and genetic management have been well documented throughout both the scientific and popular literature, it has also been established that the majority of managed populations in zoos and aquariums are not meeting the minimum criteria believed to convey long-term biological viability. For most of these populations, an inability to meet viability criteria is not an inherent failure of how cooperative management is implemented. Furthermore, in recent years, we have perceived that the need to meet specific viability goals sometimes has obscured the benefits that these populations receive from rigorous, science-based management. To better clarify the conversation surrounding population viability in zoos and aquariums, we seek to decouple viability measures and how they predict population persistence from the benefits conferred to populations through science-based management. A primary goal of population management is to facilitate the persistence of priority species for longer than would be expected if no such management were implemented. Although current viability measures and future projections of viability are important tools for assessing the likelihood of population persistence, they are not indicators of which populations may most benefit from science-based management. Here, we review the history and purpose of applying science-based management to zoo and aquarium populations, describe measures of population viability and caution against confusing those measures of viability with population management goals or long-term population sustainability, and clearly articulate the benefits conferred to zoo and aquarium populations by science-based management.     

Ancient Demographics Determine the Effectiveness of Genetic Purging in Endangered Lizards

The purging of deleterious alleles has been hypothesized to mitigate inbreeding depression, but its effectiveness in endangered species remains debatable. To understand how deleterious alleles are purged during population contractions, we analyzed genomes of the endangered Chinese crocodile lizard (Shinisaurus crocodilurus), which is the only surviving species of its family and currently isolated into small populations. Population genomic analyses revealed four genetically distinct conservation units and sharp declines in both effective population size and genetic diversity. By comparing the relative genetic load across populations and conducting genomic simulations, we discovered that seriously deleterious alleles were effectively purged during population contractions in this relict species, although inbreeding generally enhanced the genetic burden. However, despite with the initial purging, our simulations also predicted that seriously deleterious alleles will gradually accumulate under prolonged bottlenecking. Therefore, we emphasize the importance of maintaining a minimum population capacity and increasing the functional genetic diversity in conservation efforts to preserve populations of the crocodile lizard and other endangered species.     

An experimental evaluation with Drosophila melanogaster of a novel dynamic system for the management of subdivided populations in conservation programs

A dynamic method (DM) recently proposed for the management of captive subdivided populations was evaluated using the pilot species Drosophila melanogaster. By accounting for the particular genetic population structure, the DM determines the optimal mating pairs, their contributions to progeny and the migration pattern that minimize the overall coancestry in the population with a control of inbreeding levels. After a pre-management period such that one of the four subpopulations had higher inbreeding and differentiation than the others, three management methods were compared for 10 generations over three replicates: (1) isolated subpopulations (IS), (2) one-migrant-per-generation rule (OMPG), (3) DM aimed to produce the same or lower inbreeding coefficient than OMPG. The DM produced the lowest coancestry and equal or lower inbreeding than the OMPG method throughout the experiment. The initially lower fitness and lower variation for nine microsatellite loci of the highly inbred subpopulation were restored more quickly with the DM than with the OMPG method. We provide, therefore, an empirical illustration of the usefulness of the DM as a conservation protocol for captive subdivided populations when pedigree information is available (or can be deduced) and manipulation of breeding pairs is possible.