Population genomics for wildlife conservation and management

Biodiversity is under threat worldwide. Over the past decade, the field of population genomics has developed across nonmodel organisms, and the results of this research have begun to be applied in conservation and management of wildlife species. Genomics tools can provide precise estimates of basic features of wildlife populations, such as effective population size, inbreeding, demographic history and population structure, that are critical for conservation efforts. Moreover, population genomics studies can identify particular genetic loci and variants responsible for inbreeding depression or adaptation to changing environments, allowing for conservation efforts to estimate the capacity of populations to evolve and adapt in response to environmental change and to manage for adaptive variation. While connections from basic research to applied wildlife conservation have been slow to develop, these connections are increasingly strengthening. Here we review the primary areas in which population genomics approaches can be applied to wildlife conservation and management, highlight examples of how they have been used, and provide recommendations for building on the progress that has been made in this field.     

Population genomics and conservation management of a declining tropical rodent

Conservation management is improved by incorporating information about the spatial distribution of population genetic diversity into planning strategies. Northern Australia is the location of some of the world’s most severe ongoing declines of endemic mammal species, yet we have little genetic information from this regional mammal assemblage to inform a genetic perspective on conservation assessment and planning. We used next-generation sequencing data from remnant populations of the threatened brush-tailed rabbit-rat (Conilurus penicillatus) to compare patterns of genomic diversity and differentiation across the landscape and investigate standardised hierarchical genomic diversity metrics to better understand brush-tailed rabbit-rat population genomic structure. We found strong population structuring, with high levels of differentiation between populations (F_ST = 0.21–0.78). Two distinct genomic lineages between the Tiwi Islands and mainland are also present. Prioritisation analysis showed that one population in both lineages would need to be conserved to retain at least ~80% of alleles for the species. Analysis of standardised genomic diversity metrics showed that approximately half of the total diversity occurs among lineages (δ = 0.091 from grand total γ = 0.184). We suggest that a focus on conserving remnant island populations may not be appropriate for the preservation of species-level genomic diversity and adaptive potential, as these populations represent a small component of the total diversity and a narrow subset of the environmental conditions in which the species occurs. We also highlight the importance of considering both genomic and ecological differentiation between source and receiving populations when considering translocations for conservation purposes.Subject terms: Ecological genetics, Population genetics, Conservation biology, Biogeography     

居群遗传学原理及其在珍稀濒危植物保护中的应用

居群遗传学在珍稀濒危植物保护研究中有着重要的应用价值。本文首先介绍了居群遗传学中的几个重要概念——有效居群大小、近交繁殖、遗传漂变和基因流,然后详细叙述了居群遗传学原理在珍稀濒危植物保护中的应用途径和前景。     

Population genetics in the conservation of the Azorean shrub Viburnum treleasei Gand.

We assess population genetic structure and variability in the endangered Azorean endemic Viburnum treleasei Gand., an evergreen shrub or small tree, occurring in eight out of nine islands of the archipelago. We combine RAPD and ISSR markers in eight populations and four islands covering the three subgroups of islands that compose the archipelago, and one population of V. tinus from the Portuguese mainland. Most of the genetic variability was found within populations, which is in accordance with the bi-parental reproductive strategy favored by the taxon. Gene flow estimations for the combined RAPD and ISSR markers suggest that the main cause for population variability between the studied populations is genetic drift. In accordance with the genetic structure indicators obtained, conservation measures should consider that translocation of individuals between islands must be avoided. In specific cases, the analysed populations may require the implementation of augmentation strategies due to their depleted state. With this study, a genetic background is now available to better define conservation measures for the taxon.     

Population genomics as a new tool for wildlife management

Admixture and introgression have varied effects on population viability and fitness. Admixture might be an important source of new alleles, particularly for small, geographically isolated populations. However, admixture might also cause outbreeding depression if populations are adapted to different ecological or climatic conditions. Because of the emerging use of translocation and admixture as a conservation and wildlife management strategy to reduce genetic load (termed genetic rescue), the possible effects of admixture have practical consequences ( Bouzat et al. 2009 ; Hedrick & Fredrickson 2010 ). Importantly, genetic load and local adaptation are properties of individual loci and epistatic interactions among loci rather than properties of genomes. Likewise, the outcome and consequences of genetic rescue depend on the fitness effects of individual introduced alleles. In this issue of Molecular Ecology, Miller et al. (2012) use model‐based, population genomic analyses to document locus‐specific effects of a recent genetic rescue in the bighorn sheep population within the National Bison Range wildlife refuge (NBR; Montana, USA). They find a subset of introduced alleles associated with increased fitness in NBR bighorn sheep, some of which experienced accelerated introgression following their introduction. These loci mark regions of the genome that could constitute the genetic basis of the successful NBR bighorn sheep genetic rescue. Although population genomic analyses are frequently used to study local adaptation and selection (e.g. Hohenlohe et al. 2010 ; Lawniczak et al. 2010 ), this study constitutes a novel application of this analytical framework for wildlife management. Moreover, the detailed demographic data available for the NBR bighorn sheep population provide a rare and powerful source of information and allow more robust population genomic inference than is often possible.     

溶藻弧菌群体基因组学研究

溶藻弧菌(Vibrio alginolyticus)是一种能够对人类以及鱼、虾、贝类等水产品致病的弧菌,给人类健康带来威胁,也给水产养殖业造成巨大的经济损失.目前该物种基于全基因组的遗传多样性和重要遗传元件研究报道较少.本研究对采集自全国4个省份的68株溶藻弧菌进行高通量测序,获得全基因组序列,并结合113株公开发表的...     

Population genetics and conservation implications for the endangered delta smelt in the San Francisco Bay-Delta

Over the last two decades, the collapse of the endangered delta smelt (Hypomesus transpacificus) in the San Francisco Bay-Delta has resulted in politically charged conservation decisions, including the rationing of valuable Delta water for use in California agriculture and urban centers. A fundamental question remaining in delta smelt conservation is whether current management strategies have been appropriately designed to protect the remaining genetic variation in delta smelt populations, rather than merely mitigating the decline of the species. We used 15 microsatellite markers to characterize genetic variation within and among sampling regions on geographic and temporal scales, to estimate changes in effective population size over time, to determine if a genetic bottleneck exists and to define conservation management units for this species. A genetic bottleneck was detected in each of the four sampling years, and a significant decline in effective population size was observed between sampling years 2003 and 2007. We also detected a weak geographic signal in any given sampling year that was unsupported by temporal consistency of this signal. We assessed two strategies for defining conservation units, and concluded that continuing to manage the species as a single, panmictic population throughout its range is the most feasible management strategy. The results of this study will inform conservation decisions and provide an effective means for genetically monitoring this imperiled species.     

Population genetic structure of the endangered Eastern Bristlebird, Dasyornis brachypterus; implications for conservation

For species that are habitat specialists or sedentary, population fragmentation may lead to genetic divergence between populations and reduced genetic diversity within populations, with frequent inbreeding. Hundreds of kilometres separate three geographical regions in which small populations of the endangered Eastern Bristlebird, Dasyornis brachypterus, a small, ground-dwelling passerine that occurs in fire-prone bushland in eastern Australia, are currently found. Here, we use mitochondrial and microsatellite DNA markers to: (i) assess the sub-specific taxonomy designated to northern range-edge, and central and southern range-edge D. brachypterus, respectively, and (ii) assess levels of standing genetic variation and the degree of genetic subdivision of remnant populations. The phylogenetic relationship among mtDNA haplotypes and their spatial distribution did not support the recognised subspecies boundaries. Populations in different regions were highly genetically differentiated, but in addition, the two largest, neighboring populations (located within the central region and separated by ~50 km) were moderately differentiated, and thus are likely closed to migration (microsatellites, F _ST = 0.06; mtDNA, F _ST = 0.12, ?? _ST = 0.08). Birds within these two populations were genotypically diverse and apparently randomly mating. A long-term plan for the conservation of D. brachypterus??s genetic diversity should consider individual populations as separate management units. Moreover, managers should avoid actively mixing birds from different populations or regions, to conserve the genetic integrity of local populations and avoid outbreeding depression, should further translocations be used as a recovery tool for this species.     

Population genomics and conservation of Gila Trout (Oncorhynchus gilae)

Conservation Genetics - Many salmonid species exist in highly structured and isolated populations, and are susceptible to habitat fragmentation and disturbances. Gila Trout (Oncorhynchus gilae) is...     

Genetic Structure and Conservation Considerations of Rare Endemic Abeliophyllum distichum Nakai (Oleaceae) in Korea

Abeliophyllum distichum , was assessed using starch gel electrophoresis. Although A. distichum maintained relatively high genetic diversity probably due to floral heteromorphism and preferred outcrossing, their genetic variation, where small effective size of population and genetic drift are of utmost importance, was lower than the other outbreeding plants. The calculated G_sT indicated a high level of genetic differentiation among populations, suggesting that gene flow was limited. The dendrogram based on Nei's genetic distance showed that the Pu-an and the Koe-san populations fell into two distinct groups, which were consistent with geographic distance and distribution. It was probable that in the populations of A. distichum sexually reproduced individuals rarely become established within the populations. From observations, Lassioglossum bee was found to be the most effective pollinator of A. distichum. Artificial crossing experiment indicated that pollinators contributed considerably to natural population and that pollinator limitation could potentially reduce fitness of A. distichum in wild populations. The management of rare plant species should include improvement of genetic exchanges among populations by artificial gene flow. From each of the four subpopulations, fresh twigs from 20 trees should be collected and propagated as the cutting for ex situ conservation. Received 30 April 1999/ Accepted in revised form 23 January 2000     

Reducing the conservation reliance of the endangered Kirtland's warbler through adaptive management

Species are considered conservation-reliant when their continued existence is dependent on human assistance. Conservation reliance challenges the conservation community in terms of their ability to sustain the funding and public-private partnerships needed for indefinite management. Although increased funding for conservation is critical, reducing conservation reliance through adaptive management represents an attractive alternative. We used a large-scale ecological experiment as a case study in the use of adaptive management to reduce conservation reliance. For >40 years, the United States Fish and Wildlife Service has trapped and lethally removed an obligate brood parasite, the brown-headed cowbird (Molothrus ater), to protect the Kirtland's warbler (Setophaga kirtlandii) from the negative effects that brood parasitism has on its reproductive success. To determine if the conservation reliance of the Kirtland's warbler could be reduced through optimization of the cowbird control program, we used an adaptive management approach. In collaboration with stakeholders, we experimentally reduced cowbird trapping effort across nearly all of the Kirtland's warbler breeding range. We monitored the resulting cowbird abundance and rate of parasitism, and then adjusted the scale of trap reductions based on the previous year's results. Despite reducing (2015–2017) and eventually eliminating (2018) cowbird trapping, we detected only 20 cowbirds (2015–2017) and found that just 4 of 514 (<1%) nests were parasitized (2015–2018). Our results indicate that the cowbird control program can at least temporarily be suspended, thereby reducing conservation reliance in the Kirtland's warbler and freeing funds for other management. We urge the conservation community to consider the use of adaptive management to reduce conservation reliance in other threatened and endangered taxa. © 2019 The Wildlife Society.     

Population ecology of the endangered butterflies Maculinea teleius and M. nausithous and the implications for conservation

Butterflies of the genus Maculinea are highly endangered in Europe. The cuckoo species M. rebeli has been thoroughly investigated through both empirical and modelling studies, but less is known about the population ecology of predatory Maculinea. We present the findings of a 2-year research study on sympatric populations of two endangered butterflies: Maculinea teleius and M. nausithous in the Kraków region, southern Poland. The study comprised mark–release–recapture sampling and laboratory rearing of butterflies from larvae collected in the field. For both species the sex ratio was slightly, but consistently, female-biased and there was little year-to-year change in the seasonal population sizes. Daily numbers showed greater variation between the 2 years of the study due to the differences in daily survival rate. The average life span of laboratory-raised butterflies kept in ideal conditions was more than 6 days, compared to only 2–3 days in the field. The recruitment of both males and females consistently followed a bimodal pattern. A small proportion of individuals (maximum 25%) changed sites, in spite of relatively short distances of ca. 100 m separating them. The results indicate that populations of both species are typically stable within their sites, possibly due to larval polymorphism, but there is little inter-site mobility and thus landscape corridors seem necessary to enhance metapopulation viability. A further problem to be considered in the conservation of Maculinea butterflies is the fact that their very short life span in relation to flight-period length reduces the effective population size.     

Population structure and conservation genetic assessment of the endangered Pugnose Shiner,Notropis anogenus

The Pugnose Shiner is a small minnow with a fragmented distribution across the Great Lakes and Upper Mississippi River in North America. The species is listed federally as endangered in Canada, and in the United States its status varies by state, from Special Concern to Endangered (as well as Extirpated). We conducted a thorough genetic assessment of the Pugnose Shiner using both microsatellite loci and mitochondrial DNA collected for samples across the species range. Our results indicate high levels of population differentiation suggesting restricted dispersal, in some cases at very small geographical scales. We also found strong evidence of small effective population sizes and one case of a genetic bottleneck. Although significant range-wide genetic variation was observed in both microsatellite loci and mitochondrial DNA, the species is best characterized as a single evolutionarily significant unit for conservation purposes.     

Harnessing genomics for delineating conservation units

Genomic data have the potential to revolutionize the delineation of conservation units (CUs) by allowing the detection of adaptive genetic variation, which is otherwise difficult for rare, endangered species. In contrast to previous recommendations, we propose that the use of neutral versus adaptive markers should not be viewed as alternatives. Rather, neutral and adaptive markers provide different types of information that should be combined to make optimal management decisions. Genetic patterns at neutral markers reflect the interaction of gene flow and genetic drift that affects genome-wide variation within and among populations. This population genetic structure is what natural selection operates on to cause adaptive divergence. Here, we provide a new framework to integrate data on neutral and adaptive markers to protect biodiversity.     

青藏高原濒危兽类保护与管理研究进展

青藏高原是全球生物多样性热点区域和优先保护区,分布着多种重点保护物种及青藏高原特有种,物种丰富度高且濒危物种占比大。本文针对青藏高原分布的有蹄类、猫科、熊科、犬科、鼬科、翼手目、小型兽类7个动物类群,从濒危现状、濒危成因、已开展的研究工作和管理对策、取得的保护成效等角度分别论述了各类群的保护与管理研究进展。在青藏高原有蹄类中特有种占比远高于其他类群;81% ~ 100%的有蹄类、猫科、熊科、犬科动物被列为国家重点保护野生动物;45% ~ 100%的有蹄类、猫科、熊科动物被中国脊椎动物红色名录或IUCN红色名录列为受威胁物种,远高于全球平均水平。全球变暖、栖息地破碎化、环境污染、过度放牧、偷猎与非法贸易是青藏高原濒危兽类生存的主要威胁。相关法律法规的贯彻实施、自然保护地建设及开展的大量调查监测和研究,为青藏高原濒危兽类保护生物学研究提供了法律保障和科学依据。鉴于目前保护与管理工作的局限性,建议构建全面系统的大数据平台,开展青藏高原地区保护成效快速评估及自然保护地空间优化布局研究,将国际先进的交叉学科理论方法与实践创新优势相结合,为濒危兽类的保护与管理提供指导与建议,从而为我国生物多样性保护和生态文明建设提供重要的科技支撑。     

Colonization potential of an endangered riparian shrub species

Riparian areas and their plant communities are threatened due to human exploitation and habitat loss. Conservation of riparian vegetation requires knowledge on limiting factors in the biology of species preventing its spread along suitable areas. It needs to be assessed if an endangered species is trapped in an extinction vortex or whether it can recover from its current bottleneck situation by management measurements. We investigate the recovery potential of an endangered riparian shrub species of European rivers, the German tamarisk, Myricaria germanica, by combining field and lab experiments on seed production, germination and wind dispersal with a modelling approach on species distribution. While the seed potential is high, wind-mediated dispersal is average, with a majority of seeds falling next to the mother shrub. The modelled dispersal kernel shows highest goodness-of-fit with a polynomic function. Including this kernel in a model on the future distribution of the species based on identification of suitable habitat, limited spread to new areas in Switzerland after 20 and 50 dispersal events is predicted. Given the current limited distribution of the German tamarisk in Switzerland, conservation efforts are required to allow for the formation of new riparian habitat. Additionally, connectivity along river networks has to be enhanced to help the species to escape the extinction vortex it is trapped in.     

Population genetics of the endangered Canarian endemic Atractylis arbuscula (Asteraceae): implications for taxonomy and conservation

We use the information provided by 36 RAPD loci and 15 morphological traits to describe and construe the population differentiation in A. arbuscula, a Canarian endemic Asteraceae threatened with extinction that exhibits a disjunct distribution in the islands of Gran Canaria (var. schizogynophylla) and Lanzarote (var. arbuscula). Our evaluation of morphological characters and the extent of RAPD differentiation found sets the stage for a taxonomic restructuring to hoist both var. arbuscula and var. schizogynophylla to subspecies category. Our genetic results suggest that fragmentation and generally low population sizes are jeopardising the survival of this species through a predominance of stochastic processes in microevolutionary dynamics, especially in Gran Canaria, where subpopulations exhibit the lowest levels of genetic variation and gene flow. If, as most Asteraceae, these plants have a sporophytic self-incompatibility system, the scarce reproductive turnover observed in the much smaller subpopulations from Gran Canaria (ssp. schizogynophylla) is possibly more influenced by a deficiency of S-alleles (that would be provoking the unavailability of compatible mating types, and a cascade of deleterious effects associated with the Allee effect) than by a reduced pollinator visitation frequency. Based on the depauperated values of genetic parameters for this subspecies, urgent mixed subpopulation reinforcements and reintroductions (with specimens belonging to the same subspecies) seem advisable on the grounds that they might allow the isolated habitat remnants to retrieve from inbreeding through the introduction of a new stock of S-alleles and the subsequent production of genotypes that may have a higher selective value.     

Strong population genetic structure and its implications for the conservation and management of the endangered Itasenpara bitterling

To infer the population genetic structure and genetic diversity of Itasenpara bitterling (Acheilognathus longipinnis), a cyprinid species endemic to Japan and distributed in only three specific regions, we investigated mitochondrial DNA variation. The distribution of the haplotypes among the three regions showed distinct geographic structure, and no common haplotypes were observed among regions. Analysis of molecular variance revealed a significant proportion of the genetic variance was partitioned among regions (93.1 %, P < 0.001), and pairwise estimates of D_A and Φ_ST between regions also revealed strong population structure. Given the strong genetic structure and low genetic diversity within regions, we strongly suggest that each region should be treated as a separate unit in any conservation program and any inter-regional translocations should be avoided.     

Perspectives of genomics for genetic conservation of livestock

Genomics provides new opportunities for conservation genetics. Conservation genetics in livestock is based on estimating diversity by pedigree relatedness and managing diversity by choosing those animals that maximize genetic diversity. Animals can be chosen as parents for the next generation, as donors of material to a gene bank, or as breeds for targeting conservation efforts. Genomics provides opportunities to estimate diversity for specific parts of the genome, such as neutral and adaptive diversity and genetic diversity underlying specific traits. This enables us to choose candidates for conservation based on specific genetic diversity (e.g. diversity of traits or adaptive diversity) or to monitor the loss of diversity without conservation. In wild animals direct genetic management, by choosing candidates for conservation as in livestock, is generally not practiced. With dense marker maps opportunities exist for monitoring relatedness and genetic diversity in wild populations, thus enabling a more active management of diversity.     

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.